text:
Armin K. Thron

Vascular Anatomy of the Spinal CordRadioanatomy as the Key to Diagnosis and Treatment2nd ed. 2016

Armin K. Thron

Aachen, Germany

ISBN 978-3-319-27438-6e-ISBN 978-3-319-27440-9

DOI 10.1007/978-3-319-27440-9

Library of Congress Control Number: 2016933135

© Springer International Publishing 2016

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Foreword

Between 1977 and 1979, Armin Thron, at that time a young general radiologist, taught himself neuroradiology. He and the upcoming crème de la crème in neurology (H. J. v. Büdingen, P. Clarenbach, J. Dichgans, Ch. Diener, V. Dietz, H.-J. Freund, V. Koenig, G. Leopold, K.-H. Mauritz, J. Noth, G. Oepen, G.-M. von Reutern, U. Thoden, U. Weitbrecht) belonged to the famous Department of Neurology and Neurophysiology at the University of Freiburg, Germany. Being a neurosurgical consultant, I had the chance to follow Armin's metamorphosis from a common radiologist to a neuroradiologist in this steam boiler of alpha-types led by Professor Richard Jung.

And yet again, from 1979 to 1987, Armin Thron provided a large number of neurologists and neurosurgeons (E.H. Grote, W. Hassler, H. Steinmetz, J. Zentner) with his neuroradiological knowledge as assistant professor under the directorship of Karsten Voigt in the Neuroadiological Department at the University of Tübingen. It was there that he started his experimental and clinical investigations about the vascular blood supply and vascular diseases of the spinal cord, thus creating the basis for the first edition of his book.

After fulfilling necessary criteria to obtain a leading position, Professor Armin Thron spent the rest of his professional life, from 1987 to 2010, at the University Hospital of the RWTH Aachen University. From 1989 until our respective retirements, we cooperated well: he as the leading neuroradiologist, me as his neurosurgical counterpart.

Every day from 7:30 to 8:30 a.m., we held our neurosurgical-neuroradiological conference where Armin and his compatriots taught us neuroradiology and we got the chance to defend our surgical misadventures and the sometimes controversial indications for surgical interventions. To my personal disappointment, many of my neurosurgical co-workers identified these conferences as the most defining part of their training.

Just as at Freiburg and Tübingen, at the University Hospital in Aachen, Armin again trained many upcoming leading neurosurgeons (H. Bertalanffy, V. Coenen, F.H. Hans, A. Harders, V. Rohde, K. Schmieder, U. Sure, E. Uhl, J. Warnke).

Armin and I were both born in 1945 and belong to the 68-generation. Therefore, it was not surprising that we first had to define our professional and team positions in Aachen before we could become friends and also enjoy a good and successful professional time together.

For this new version of his book, Professor Thron spent a lot of his sparse private time as a pensioner in order to help his readers. But as is typical for Armin, he is fully dedicated to the cause of his work without regard for the achievement of personal recognition.

Thanks to Armin's favourite topic, spinal vascular disease, we had the chance to come across numerous interesting cases and most fortunately could help many of the concerned patients owing to our fruitful neuroradiological-neurosurgical cooperation. Therefore, I highly recommend that one consider this book not only as a basic textbook but also as a key to microsurgical treatments of spinal vascular disorders.

Joachim Gilsbach

Aachen, Germany

September 2015

Preface

> The excitement which the subject represents to us lies in the fact that buildings with what is in principle an identical function exist in such a variety of diverse forms
>
> Bernd and Hilla Bechers

The idea for a treatise on the radiological anatomy of superficial and deep spinal cord blood vessels evolved from daily routine neuroradiological work in the early 1980s at the University of Tübingen. The topic was not induced but promoted by guest stays at hospitals in Paris, especially at the Neuroradiology Department of Lariboisière Hospital. Jean-Jacques Merland, the head of the department at that time, and his predecessor René Djindjian were highly renowned for practising selective spinal angiography at the highest level. This met very well with my long-lasting interest in diseases of the spinal cord.

Progress in selective angiography of the spinal cord in suspected disease of vascular origin demanded an advanced understanding of spinal cord blood vessel anatomy and its variations. Parallel to this development, progress in neurosurgery and especially the rapidly developing endovascular treatments in interventional neuroradiology improved our knowledge in this field and broadened the spectrum of treatment options. Significantly ameliorated disease classifications could be established, reflecting an improved understanding of pathogenetic aspects of vascular diseases like in cases of arteriovenous malformations, dural arteriovenous fistulas or vascular tumours of spine and spinal cord.

The first version of this book, Vascular Anatomy of the Spinal Cord , published in 1988, was a monograph, bearing the subtitle Neuroradiological Investigations and Clinical Syndromes . Thus, it was subdivided into an anatomical part with post-mortem examinations of arteries, capillaries and veins of the spinal cord in normal and pathological conditions and in a clinical section. The latter reflected the progress in diagnostic imaging mentioned above, mainly in selective digital subtraction angiography (DSA). Computed tomography (CT) was not very helpful for intraspinal details at that time and magnetic resonance imaging (MRI) was in its modest beginnings, at least concerning imaging of the spinal cord. Only two figures of this book from 1988 illustrate a clinical case example using MRI. Myelography using water-soluble contrast media was still the established standard technique to outline the structures within the dural sac.

The rapid technical progress in non-invasive imaging techniques in the fields of MRI, MR angiography or modern CT technologies, but also upgraded DSA units with higher spatial/contrast resolution, offered new detailed insights into the intraspinal compartments.

Consequently the diagnostic methods illustrating the clinical part of the treatise published in 1988 are only of historical value today with the exception of selective angiography. Not only for this reason, we have abstained from including this type of clinical section in this second edition. We concentrate on what we consider fundamental in this context: vascular anatomy and its correlation with spinal angiography in normal and pathological conditions.

This field of basic classical anatomy has maintained its essential importance. It has been established for a long time and has not been the subject of fast and dramatic modifications. The basic principles are generally well known, but the knowledge of details depends on whether physicians are able to make use of them for patient care or scientific purposes. But, to give an example, details about the blood vessels and the blood circulation within and around the spinal cord could be neglected to a certain degree as long as nobody was in need of this knowledge; and as long as nobody was able to perform successful diagnostic and therapeutic interventions based on this knowledge. But during the last 25 years this situation has changed substantially both for diagnostic and therapeutic modalities.

Nevertheless, a clear conception of the vascular radioanatomy of the spinal cord and its variations remains an obvious challenge for many physicians, even for those working in disciplines which are involved in patients suffering from spinal cord diseases. This is the reason why the anatomical knowledge presented in the previous edition has maintained if not augmented its significance.

We have tried to simplify the basic principles by using schemes and graphics to facilitate learning and training by an improved didactic presentation. Anatomical evaluations of angiographic findings in vascular malformations and special notes on dangerous pitfalls or examination requirements are included in order to address some important problems in the clinical application of blood vessel anatomy.

The many details presented in the microangiogram section mainly address those concerned with either scientific questions or with invasive therapeutic techniques and who are familiar with the interpretation of radioanatomic findings.

A comprehensive description of medullary vascular syndromes would be beyond the scope of this treatise. It would require a different approach with more interdisciplinary contributions from physiologists, neurologists, neuroradiologists, neurosurgeons and neuropathologists.

Armin K. Thron

Aachen, Germany

January 2015

Acknowledgement

The first group of radioanatomical investigations on the spinal cord were performed at the Department of Neuroradiology, University of Tübingen, in the 1980s. It is to the department's head at that time, Prof. Dr. K. Voigt, that I express my sincere gratitude for stimulating and supervising my initial scientific projects, and for constant support.

Encouraged by Prof. Dr. W. Dauber from the Department of Anatomy of the University of Tübingen, we made the first steps to inspect the anatomy of spinal cord blood vessels and to test techniques of radiographic work-up of the contrast-injected specimens.

Prof. Dr. J. Peiffer, a neuropathologist, and his collaborators from the Institute for Brain Research at the University of Tübingen also gave valuable support and kindly provided their laboratory facilities for us.

After I had changed to the University Hospital of Aachen in 1987 to become Head of the Neuroradiological Department, additional anatomical, functional and clinical studies were planned and could be carried out during the 1990s thanks to excellent support from the Institute of Neuropathology. Therefore I owe special thanks to Prof. Dr. J. Schröder, the former Head of this Institute, for not only providing laboratory facilities for us but also for participating in cooperative investigations initiated by our department.

Special thanks are further expressed to Mrs. Virginia Müller and Prof. Dr. H. Steinmetz for the translation of the first edition of the book and Springer International Publishing AG for copy-editing the final manuscript of the second edition.

Furthermore, I would like to thank Prof. Dr. J. J. Merland (Hopital Lariboisière, Paris) and Prof. Dr. B. KendaIl (National Hospital, Queens Square, London) for the inspiration gained through their work and for the fruitful exchange of ideas and friendly personal contact.

To accomplish a scientific project resulting in a monograph and a textbook like the one presented, you need help from many people.

This is why I want to list those who practically assisted in one way or another in the realization of this project with my grateful thanks.

Dr. Christine Rossberg

At the time of the initial neuroanatomical study she worked at the Neuropathological Department of the University of Marburg (Head Prof. Dr. H. D. Mennel). I owe special thanks to her for removing and preparing most of the post-mortem specimens which we were able to evaluate macro- and microangiographically. Her contribution included the first radiographic documentation of the prepared specimen. She was a member of the Department of Neuroradiology in Tübingen in the early 1980s before she changed to the Department of Neuropathology in Marburg. She died in October 2001. Without her practical and professional assistance, the post-mortem anatomical study could not have been realized, at least not with this quality of specimen preparations.

Prof. Dr. Angel Mironow

Comprehensive post-mortem and clinical investigations are impossible without the assistance of colleagues and the exchange of views and experiences on an advanced level. I owe special thanks to my former colleague Prof. Dr. A. Mironow for his initial help in conceptual considerations and post-mortem preparations.

Walter Korr

He is a former graphic artist of the University Clinic of the RWTH Aachen University.

The concept for the second edition of the book followed the ambitious plan to make the book useful not only as an instructive atlas for scientific purposes but at the same time as a textbook or a teaching file for the neuro-specialities. Therefore I was very happy to meet him and to benefit from his special abilities. His professional help is evident in the computer graphic design of the diagrams in this book, which I had conceptualized and outlined for didactic purposes over several years.

In the context of our continuous research on anatomy, clinical imaging and endovascular treatment of vascular diseases of the spine and spinal cord at the University Clinic of Aachen, I owe sincere thanks to the following colleagues and collaborators:

Assistant professor Dr. Michael Mull, and Prof. Dr. Timo Krings

For their highly qualified everyday support and especially for their keen interest in the basic scientific and advanced clinical imaging projects of the department. Guided by our primary principles of intellectual honesty in research and patient safety in interventional procedures they helped to maintain a high level of competence and patient confidence in diagnostic and interventional challenges over many years.

Dr. Juergen Otto , and Dr. Tibor Jacobs

Were medical students working on a thesis for a doctorate in medicine under my guidance. They elaborated topics on morphological and functional anatomy of spinal cord veins.

Contents

1 Introduction 1

1.1 Historical Background 1

1.1.1 Previous Studies 1

1.1.2 Anatomical Methods and Materials 2

1.1.3 Injection Techniques 2

1.2 Radiological Examination Techniques 3

1.2.1 Post-mortem Macro- and Microangiography 3

1.2.2 Clinical Spinal Angiography 3

1.2.3 CT and Magnetic Resonance Angiography 4

1.3 Own Investigations 4

1.3.1 Contrast Medium and Injection Technique 4

1.3.2 X-Ray Techniques for Standard Images 4

1.3.3 Preservation 5

1.3.4 Microangiography 5

References 6

2 Arterial Blood Supply 9

2.1 Embryology 9

2.2 Segmental Supply to the Spine and Spinal Cord 10

2.2.1 Extra- and Intraspinal Extradural Anastomoses 10

2.2.2 The Segmental Spinal Branch 10

2.3 Radicular and Radiculomedullary Arteries 15

2.4 Superficial Arteries of the Spinal Cord 20

2.5 Intrinsic Arteries 27

2.5.1 Central Arteries 28

2.5.2 Peripheral System 39

2.5.3 Capillaries of the Spinal Cord 39

2.6 Arterial Territories of Supply 42

2.7 Arterioarterial Anastomoses 45

2.7.1 Superficial Anastomoses 45

2.7.2 Transparenchymal Anastomoses 45

2.7.3 Intrinsic Anastomoses 45

2.8 Specific Patterns of Arterial Supply in the Cervical Spinal Cord 49

2.9 Specific Patterns of Arterial Supply in the Upper- and Mid-Thoracic Spinal Cord 59

2.10 Specific Patterns of Arterial Supply in the Thoracolumbar Spinal Cord and Cauda Equina 68

2.11 Anatomical and Haemodynamical Aspects of Arterial Supply 79

2.11.1 Anastomotic Capacity of Longitudinal Trunks and Distribution of Supplying Arteries 79

2.11.2 Spinal Cord Ischemia and Infarct 81

References 82

3 Venous Drainage 85

3.1 Intrinsic Veins 87

3.2 Superficial Veins 94

3.2.1 Longitudinal Venous Trunks 94

3.2.2 Pial Venous Networks of Lower Degree 94

3.3 Transmedullary Venous Anastomoses 100

3.4 Specific Patterns of Venous Drainage in the Cervical Spinal Cord 108

3.5 Specific Patterns of Venous Drainage in the Thoracic Spinal Cord 110

3.6 Specific Patterns of Venous Drainage in the Thoracolumbar and Sacral Spinal Cord 115

3.7 Radiculomedullary Veins and the Transdural Course 122

3.8 Extradural Intraspinal and Extraspinal Venous Systems 131

3.9 Anatomical and Haemodynamical Aspects of Venous Drainage 134

3.9.1 Intrinsic Veins 134

3.9.2 Intrinsic Venous Anastomoses 134

3.9.3 Superficial and Radiculomedullary Veins 135

3.9.4 Circulatory Disturbances of Venous Origin 135

References 136

4 Clinical Applications 137

4.1 Applications in Normal Spinal Digital Subtraction Angiography and Interpretation of Uncommon Blood Vessels on Tomographic Imaging 138

4.2 Applications in SAVMs 143

4.2.1 Definition and Classification 143

4.2.2 Angiographical Findings 144

4.2.3 Conclusions 145

4.3 Applications in Spinal Dural AV Fistulas 161

4.3.1 History and Definition 161

4.3.2 Localization 161

4.3.3 Aetiological and Pathophysiological Aspects 161

4.3.4 Pathogenesis of Spinal Cord Damage 162

4.3.5 Angiographical Findings 162

4.3.6 Diagnostic Management 163

4.3.7 The Question of Chronic Myelopathies in the Absence of AV Shunt Disorders 163

4.3.8 Open Questions 163

4.4 Applications in Vertebrospinal and Medullary Vascular Tumours 181

4.5 Potential Pitfalls in Spinal Angiographic Examinations and Evaluations 186

References 187

Index191

About the Author

Armin K. Thron

is Professor of Neuroradiology. Until March 2010 he was the Head of the Department of Neuroradiology at the University Clinic of the University of Technology Aachen, Germany. From 1996 to 1999 he was the President of the German Society of Neuroradiology and from 1996 to 2002 he was the President of the Professional Association of German Neuroradiologists. He was member of the Board of the European Society of Neuroradiology from 1993 to 1996 and President of the XXIX Congress of the European Society of Neuroradiology 2004 in Aachen, Germany. Prof. Thron has a special interest in spinal diseases and vascular diseases of the spinal cord. He is author of various textbook contributions concerning mainly diagnostic and interventional neuroradiology.

© Springer International Publishing 2016

Armin K. ThronVascular Anatomy of the Spinal Cord10.1007/978-3-319-27440-9_1

# 1. Introduction

Armin K. Thron1

(1)

Aachen, Germany

Because of progress in microneurosurgery and interventional neuroradiology, intramedullary lesions have become more and more accessible and treatable. Unfortunately, a lack of knowledge about spinal vascular anatomy is evident in many conferences with neurologists and sometimes even with neurosurgeons and neuroradiologists. This lack of knowledge might be a reason for unsatisfactory clinical results in the treatment of spinal vascular diseases by invasive therapeutic techniques. Furthermore, magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) of blood vessels in and around the spinal cord have substantially improved. To provide a correct anatomical interpretation of the demonstrated blood vessels, knowledge of the anatomy of spinal cord blood vessels is the first prerequisite.

## 1.1 Historical Background

### 1.1.1 Previous Studies

Our limited knowledge about the physiology and pathology of the spinal blood supply contrasts with anatomical descriptions of the spinal vascular system from as early as the end of the nineteenth century by Adamkiewicz (1881, 1882) and, with a precision that has hardly been achieved since, by Kadyi (1889). Earlier studies, such as those by Duret (1873) and Ross (1880), were less defined, incomplete and unsystematic. Until about the middle of the twentieth century, the spinal vascular system was seldom the object of thorough anatomical research. However, one must mention the comprehensive works of Tureen (1938) and Suh and Alexander (1939), who called back to mind the results of Kadyi (1889).

According to these previous investigations, one ventral and two dorsal arterial trunks supply the spinal cord. They originate at the cranial end by feeders from the distal segment of the vertebral arteries, as well as by a varying number of lateral feeders of different calibre entering with the nerve roots at different levels. These radicular arteries originate from segmental arteries or homologous vessels.

On the basis of this anatomical knowledge, Bolton (1939) carried out injection studies to examine blood flow direction and vascularization territories of the medulla. As of 1950, the interest in problems of spinal vascular supply was stimulated by progress and new questions raised by clinical work. Some examples of these are neurological complications following surgery on the aorta and spinal column (Adams and van Geertruyden 1956; Hogan and Romanul 1966; Adams 1984), neurological syndromes of assumed vascular origin (Kalm 1953; Zülch 1954, 1976; Gruner and Lapresle 1962) and the spinal vascular malformations that had become diagnosable with the introduction of clinical spinal angiography (Djindjian et al. 1963, 1970; Di Chiro et al. 1967; Doppman et al. 1969). These clinical challenges have led to an expansion and deepening of our knowledge. Noteworthy are the studies of Gillilan (1958, 1970), of Lazorthes (1972) and co-workers (1958, 1962, 1966, 1971, 1973), Noeske (1958), Roll (1958), Perese and Fracasso (1959), Clemens and v. Quast (1960), Corbin (1961), Houdart et al. (1965), Romanes (1965), Hassler (1966), Jellinger and Neumayer (1972), Mannen (1966), Turnbull et al. (1966), Fazio and Agnoli (1970), Manelfe et al. (1972), Piscol (1972), Dommisse (1975), Tveten (1976a, b, c), Crock and Yoshizawa (1977), Moes and Maillot (1981), Crock et al. (1986). Except for a few studies by authors such as Kadyi (1889), Suh and Alexander (1939), Clemens and v. Quast (1960) and Crock and Yoshizawa (1977), the arterial system was more extensively, if not exclusively, examined. Venous anatomy was focussed upon in the studies of v. Quast (1961) as well as Gillilan (1970) and in the detailed treatise of Moes and Maillot (1981) about the superficial veins of the human spinal cord. Breschet (1828–1832) and later on Batson (1957) and Clemens (1961) demonstrated quite early the vertebral venous system and its connection to the veins of the medulla. Mainly Woollam and Millem (1955), Jellinger (1966a, b) and Tveten (1976a) conducted comparative animal experiments.

### 1.1.2 Anatomical Methods and Materials

Anatomical investigative techniques for the spinal vascular system are based upon preparations using macroscopic-microscopic inspection, histological serial sections and numerous methods of vascular injection. The last of these are especially valuable for demonstrating continuous vessel courses. In addition to non-hardening staining fluids such as ink, usually mixed with gelatine (Bolton 1939; Herren and Alexander 1939; Suh and Alexander 1939; Gillilan 1958; Corbin 1961; Vuia and Alexaniu 1969; Moes and Maillot 1981), many hardening substances were used as well. Adamkiewicz (1881) and Kadyi (1889) injected stained gluten and a Teichman cement of chalk and linseed oil. Other notable substances are PANSCH-mass (Noeske 1958; Roll 1958), celloidin (Bolton 1939), latex solution (Gillilan 1958; Clemens 1961; Jellinger 1966a; Dommisse 1975) or neoprene latex solution (Perese and Fracasso 1959), synthetic resin (Lazorthes et al. 1958; Corbin 1961) or polymerized plastics such as plastoid (Gillilan 1958; Piscol 1972). These and other substances which harden out well facilitate corrosive preparations after maceration in potassium hydroxide solution.

Not all substances are equally good for filling both large and small vessels and may easily cause extravasation. Therefore, different methods were often applied separately, especially if visualization of the outer and inner medullary vessels was intended. For the study of vessels within the parenchyma, Adamkiewicz (1881) and Kadyi (1889) used a clearing method with clove oil. This technique, further developed by Spalteholz (1914), renders tissue sections transparent, so that the stained vessels can be pursued over a certain length under the microscope by turning the knurled screw.

Even without vascular injection, the superficial medullary vessels of the exposed spinal cord can be studied both macroscopically and with a microscope. This is easy with veins of large calibre (v. Quast 1961), but can also be applied to the determination of radicular feeders and the course and calibre of the ventral and dorsal spinal arteries (Jellinger 1966a; Mannen 1966).

### 1.1.3 Injection Techniques

As feeding and draining vessels of the medulla originate from various vascular territories, particular problems are encountered in injection techniques. No method exists as of yet which is qualitatively suitable for a complete demonstration of both the extra- and intraspinal vessels.

In principle, the most appropriate technique is considered to be a global filling of all feeders via the aorta, imitating natural conditions. This was employed by Gillilan (1958), Dommisse (1975) and Tveten (1976) for all of the examined specimens, and by Corbin (1961), Hassler (1966) and Jellinger (1966a) only for a part. Apart from the unfeasibility for routine examinations, the large injection volume of several litres necessary even after ligation of the peripheral major arterial trunks poses an additional problem. Gillilan (1958), Dommisse (1975) and Tveten (1976b, c) reduced this problem by studying perinatal autopsy cases. The injection technique is well suited for determining the extraspinal sources of arterial supply and their collaterals. Corbin (1961) and Hassler (1966) additionally carried out selective filling of radicular arteries on the removed spinal cord to demonstrate the inner spinal vessels.

Adamkiewicz (1881) and Kadyi (1889) had already applied this selective injection technique. Despite numerous collaterals on the medullary surface, complete filling is usually impossible, unless several anterior radicular feeders are injected simultaneously or successively. This deficiency, on the other hand, is advantageous for studying vascular territories on transverse and longitudinal sections if enough fractioned injections can be applied. Nevertheless, only very restricted conclusions concerning in vivo haemodynamics can be deduced from post-mortem injection experiments (Turnbull et al. 1966; Piscol 1972).

Noeske (1958), Roll (1958), and Corbin (1961) discussed at length the difficulties of an adequate filling technique, yet the authors rarely quote exact data on the rate of success.

The quality and completeness of filling depend on many factors:

  * The type and quantity of the injected medium

  * The specimen's state of preservation (autolysis, thrombi)

  * The occurrence of vascular perforation in the vicinity of the injection site or intraparenchymal extravasations

  * Leakage of contrast medium from small disrupted vessels in removed spinal cords

  * The impossibility of filling very small radicular arteries

For that reason the material for evaluating the outer and inner microvascular architecture must be assembled like a mosaic from a large number of cases in order to obtain a complete picture of all medullary segments. One of the main reasons for divergent results can certainly be seen in these methodological problems, which can only be solved at great expense.

The injection techniques applicable for the spinal drainage system differ because satisfactory filling of the subarachnoid veins from outside of the dural sac was supposed to be impossible. The disappointing results from post-mortem investigations (Breschet 1828– 1832; Batson 1957; Clemens 1961; Crock et al. 1986; Crock 1996) were supported by results of spinal in vivo phlebography with only occasional simultaneous filling of intradural spinal cord veins (Théron and Moret 1978; Vogelsang 1980). Consequently, the presence of valves in the radiculomedullary veins was assumed and the few existing studies on intradural and intramedullary veins were based on macroscopic-microscopic inspection (v. Quast 1961; Jellinger 1966a; Dommisse 1975) or selective intradural filling of radicular veins (Adamkiewicz 1881, 1882; Kadyi 1889; Suh and Alexander 1939; Lazorthes et al. 1962; Gillilan 1970). Satisfactory post-mortem filling through arteries and capillaries into the veins has seldom been achieved (Dommisse 1975).

## 1.2 Radiological Examination Techniques

### 1.2.1 Post-mortem Macro- and Microangiography

Lazorthes et al. (1958) and later Corbin (1961) combined classical methods and injection techniques with post-mortem X-ray arteriograms after injecting barium sulphate, thereby contributing essentially to the radioanatomy of the spinal vascular system. Several further studies, e.g. by Houdart et al. (1965), Doppman (1975), Tveten (1976a, b, c), Doppman and Girton (1977), and Doppman et al. (1979), made use of the excellent contrast characteristics of barium sulphate. With its average grain size of 0.5 μm (Treichel et al. 1977) it is likewise applicable to capillary preparations. Piscol (1972) carried out flow tests with iodine contrast media, partially using serial angiography.

The possibility of also demonstrating histological structures by the use of extremely fine-grained film and soft X-rays led to the development of microangiography, thus named by Bellman (1953). This technique of radiological microscopy and microradiography is based on the physical investigations of Cosslet et al. (1957) and Engström et al. (1960). Microangiographical techniques were conducted on the central nervous system with a focus on the cerebral vessels (Saunders 1960; Lazorthes 1961; Dor and Salomon 1970; Salomon 1973; Duvernoy 1978).

Neuroradiological studies of embryonic cerebral development by Voigt and Stoeter (1980) and of experimental cerebral tumours by Schumacher (1981) employed microangiographical techniques. These works include extensive surveys of the literature and methodological discussions on microangiography.

Microangiography of spinal vascular structures has received only sporadic attention. Saunders (1960) demonstrated it exemplarily on a foetal spinal cord in the context of an extensive study on the cerebral vessels. The first systematic, strictly microradiographical investigations are the studies by Turnbull, Breig and Hassler (1966) on the cervical spinal cord and by Hassler (1966) on the thoracolumbar region. Yet these studies only refer to the arterial component. Furthermore, one must mention the microangiographical investigations of the spinal dura mater by Manelfe et al. (1972).

The studies of Tveten (1976a, b, c) on the spinal vascular system in men and rats are partially based on microradiological methods. Extended applications of this method can be found in animal experiments (Doppman 1975; Doppman and Girton 1976; Doppman and Girton 1977, 1979).

### 1.2.2 Clinical Spinal Angiography

The present state of selective spinal angiography as a relatively safe diagnostic procedure is a result of methodological developments in the early 1960s. On the one hand, these consisted of improvements in radiological technology and the possibilities of image subtraction (photographically or through digital image processing). On the other hand, global injection methods were replaced by a selective catheterization of segmental nutrifying arteries or their equivalents. In addition, the application of less neurotoxic contrast media was facilitated by the introduction of non-ionic and almost iso-osmolar substances at the beginning of the 1980s.

The now largely standardized technique of selective spinal angiography is based on the pioneering studies of Djindjian (1978a, b), Djindjian and co-workers (1963, 1975) as well as Di Chiro and Doppman (Di Chiro et al. 1967; Di Chiro and Doppman 1969; Di Chiro 1972). Under the present technological conditions, only radicular arteries and sections of the anterior and posterolateral spinal arteries with calibres of more than 0.2 mm can be demonstrated angiographically. For the demonstration of blood flow directions in the longitudinal anastomoses, in vivo angiographies of normal spinal cords are most suitable, as they reflect the physiological conditions most realistically. According to Adamkiewicz's partial flow theory (1881) deduced from anatomical findings, the bloodstreams of the radicular arteries divide and reach the medullary surface in two partial streams, one running cranially and one caudally. Consequently, opposing partial flows approach each other in the longitudinal anastomosis between two inflow regions.

Spinal angiography is diagnostically essential in arteriovenous disorders and in highly vascularized tumours of the spine and spinal cord (Djindjian et al. 1970; Merland et al. 1980; Vogelsang 1980). All surgical procedures on the spinal column that involve a mechanical alteration of the roots should be preceded by a preoperative visualization of the large anterior radicular feeders (Hilal and Keim 1972). On the other hand, spinal angiography is of limited value for arteriosclerotic vascular disease or the so-called anterior spinal artery syndrome, although such cases have occasionally been examined (Di Chiro 1971).

The major limitations of this method are due to the time-consuming examination technique as well as to the insufficient visualization of small vessels and of the venous part of the spinal circulation. Even in spinal phlebography (Théron and Moret 1978), a reflux-impeding or at least-modulating mechanism at the dural or epidural level normally interferes with free flow of contrast medium from the epidural venous plexus into the intradural superficial system.

### 1.2.3 CT and Magnetic Resonance Angiography

MR angiography of the spine and spinal cord has become an attractive non-invasive tool for the detection and evaluation of spinal cord blood vessels in normal and pathological conditions (Mull et al. 2007; Nijenhuis et al. 2006; Backes and Nijenhuis 2008).

## 1.3 Own Investigations

For the radioanatomical study of the previous edition macro- and microangiographies were performed post-mortem on a total of 66 human spinal cords. Following a complete laminectomy, the intact dural sac was excised with the roots severed as peripherally as possible. The only selective factor applied to autopsy cases was an effort to examine space-occupying lesions or spinal vascular diseases. Such pathological cases represented 12 % (8/66). Consequently, the majority of the examined spinal cords were chosen from randomly distributed autopsy cases with varying causes of death. Age distribution had its maximum in the sixth and seventh decade of life and an average of 64 years (36–84 years). Male cases predominated over female by 2:1. Classification according to spinal cord segment and arterial or venous vascular filling shows the following distribution (Table 1.1).

Table 1.1

Distribution of spinal cord regions and site of contrast injection in the examined specimens

Spinal cord region | Site of contrast injection

|  |  |
---|---|---|---|---
|

Arterial | Venous | Arterial + venous | Total no.

Cervicothoracic | 7 | 4 | 1 | 12

Thoracolumbar | 24 | 13 | 9 | 46

Complete spinal cord | 7 | 0 | 1 | 8

|  |  |  |

–

|  |  |  |

66

In the context of two doctoral (research) studies, performed in our department of neuroradiology in Aachen, supported by the department of neuropathology, on the reflux-impeding mechanism by J. Otto and on the specification of radicular and radiculomedullary veins by T. Jacobs, another 71 specimens could be evaluated, using different techniques of examination.

### 1.3.1 Contrast Medium and Injection Technique

The contrast medium prepared for filling the unfixated specimens consisted of 8 parts of a 90 % aqueous suspension of barium sulphate (Micropaque °R) mixed with 2 parts of gelatine solution (25 g gelatine dissolved in 100 ml physiological saline solution at 40 °C) and 4 % phenol. In this dilution, barium sulphate suspension reaches at least the precapillary arterioles. Tests with a less concentrated suspension were unsatisfactory as a result of increased contrast medium extravasations and poorer contrast in the X-ray images. Adding gelatine (heated to 37–40 °C) hardens the contrast bolus and prevents contrast medium from leaking when dissecting the fixated specimens. This was occasionally unavoidable mainly for superficial veins with wide lumen and thin walls.

After dissection of the dural sac the radicular arteries (or veins) of largest calibre were localized, probed with a blunt lymphographic needle and bound. Further radicular vessels of large calibre in the same filling territory were ligated temporarily along with the cranial end of the cord. Thus, rapid leakage of contrast medium was avoided, while unligated small calibre vessels permitted injection into the thereby partially open system. Contrast suspension was injected manually under visual control of filling in the superficial vascular network. Depending on the filling achieved, additional vessels were probed and injected in order to procure the most complete vascular visualization possible. On the arterial side, this was most difficult in the mid and upper thoracic regions. For the upper cervical region, ligatures were applied to the proximal basilar artery below the origin of the anterior inferior cerebellar artery (AICA) and to the posterior inferior cerebellar artery (PICA) followed by contrast injection in both vertebral arteries.

### 1.3.2 X-Ray Techniques for Standard Images

Following vascular filling, but before fixation, radiographs were taken using a soft tissue technique on a mammography device with 25 kV and 0.5 s, or on a Packard Faxitron with 30 kV and 1.5 min exposure. The images thus obtained allowed the evaluation of filling quality and were valuable in determining the plane of section for subsequent microradiography.

### 1.3.3 Preservation

Specimens were fixed in 4 % formaldehyde for at least 5 days. Deposition in a stretched position prevented deformations due to incorrect storage, but could not exclude the effects of erratic shrinking processes.

### 1.3.4 Microangiography

For microradiography the specimens were cut with microtome blades into 1- to 3-mm-thick axial (horizontal), frontal or sagittal sections, as seen in Fig. 1.1. The format of spectroscopic blades used in microradiography allowed a maximal section length of 2.5 cm. A few spinal cords were cut into contiguous sagittal or frontal sections. In most cases, sectioning alternated in order to obtain different views of each spinal cord segment from various specimens.

Fig. 1.1

Orientation of the sections cut for the microangiographic evaluation (Reproduced from Thron 1988)

The slices were prepared for paraplast embedment by alcohol and benzene treatment in an Autotechnicon (model Duo2.A.). The paraffin-embedded pieces were suitable for microradiography after excess wax had been removed on a hot plate. Contact radiographs were obtained with a special microstructure X-ray device (Philips X-ray generator PW 1720) under the following exposure conditions: 30 kV, 23 mA, 6–15 min depending on specimen thickness. The film material exposed in direct contact with the specimens consisted of Kodak spectroscopic plates, type 649–0, with especially fine-grained emulsion. The use of consistent photographic enlargement allowed consecutive segments of frontal or sagittal sections to be joined together without gaps, making a longitudinal reconstruction of extensive cord regions possible.

Inner vessel diameters of the most important arteries and veins were determined from the contact radiographs in ten different specimens with a PET 2001 series minicomputer (Commodore) and a Summagraphics magnetic plate (Table 1.2).

Histology was obtained from all cases of suspected spinal cord disease and from the majority of routine autopsy cases (provided by Christine Rossberg M.D., Department of Neuropathology, Institute of Pathology, University of Marburg, FRG).

Table 1.2

Range of inner vessel diameters for the most important arteries and veins of the spinal cord

Vessel | Spinal cord region

---|---

Cervical (mm) | Thoracic (upper two thirds) (mm) | Thoracolumbar (mm)

Ant. rad. med. artery | <0.6 | <0.5 | <1

Ant. spinal artery | 0.2–0.5 | 0.2–0.4 | 0.5–0.8

"Narrow segments" | 0.1 | 0.1 | –

Arcades of the cone

|  |  |

<0.3

Post. rad. med. artery | 0.2–0.4 | <0.2 | 0.2–0.5

Posterolat. + post. spinal artery | 0.1–0.2 | 0.1–0.2 | 0.1–0.4

Central artery | 0.1–0.25 | 0.08–0.2 | 0.2–0.26

Penetr. branch (Vasocor.) | <0.05

|  |

0.06

Ant. + post. rad. med. veins (+median spin. veins) | 0.5–1.5 | 0.4–1.0 | <2.0

Central vein | 0.1–0.25 | 0.08–0.2 | 0.1–0.26

Radial (peripheral) vein | 0.1–0.25 | 0.1–0.25 | 0.1–0.2

Midline anastomoses | <0.4 | <0.7 | <0.2

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© Springer International Publishing 2016

Armin K. ThronVascular Anatomy of the Spinal Cord10.1007/978-3-319-27440-9_2

# 2. Arterial Blood Supply

Armin K. Thron1

(1)

Aachen, Germany

## 2.1 Embryology

Only a few investigations and observations exist on the embryonic development of the spinal vessels in humans. Ontogenetic studies by His (1887) and more recently by Torr (1957a, b) and Di Chiro et al. (1973) are supplemented by detailed phylogenetic studies, especially those by Sterzi (1904). The examination of early vascularization patterns is facilitated by the apparent similarity of the embryonic development of the spinal vessels in higher vertebrates.

The segmental feeders to the developing spine are branches of the dorsolateral somatic intersegmental arteries originating from the aorta. In the thoracic and upper lumbar regions the intersegmental arteries persist as intercostal and lumbar arteries (Hamilton et al. 1959). In the cervical and sacral regions the intersegmental arterial pattern is considerably modified by the development of the vertebral and iliac arteries, respectively. Longitudinal anastomoses, which are formed between successive intersegmental arteries in the cervical region in a postcostal position, form a large portion of the vertebral artery.

Precostal anastomoses in the cervical and upper thoracic regions persist to form the thyrocervical trunk and the superior intercostal stem. Persistence of the post-transverse anastomoses provides an origin for the deep cervical artery.

The spinal cord vascularization originates from a bilateral capillary network on the ventrolateral surface of the medulla connected to the segmental, dorsal branches of the aorta. After undergoing numerous transformations, two primitive longitudinal systems are formed at the same site. The capillary networks expand to the ventral and dorsal sides. By the end of the second embryonic month, the primitive ventrolateral longitudinal systems are transformed into a solitary anteromedian longitudinal vessel, the so-called anterior spinal artery. This artery was shown by Torr (1957a, b) and later by Di Chiro et al. (1973) using microangiograms in 10- to 14-week-old embryos to be a quite attenuated vessel. Although at this time the differentiation of the vertical systems on the dorsal side already takes place, a plexus-like pattern of vessels remains visible much longer there, as well as on the ventral side of the upper cervical region (Di Chiro et al. 1973). According to His (1887) and Torr (1957 b), the formation of the anterior spinal artery is the result of a medial movement and fusion of the primitive ventrolateral tracts (analogous to the formation of the aorta), whereas Sterzi (1904) assumes a segmental and irregularly alternating involution of the primitive longitudinal tracts.

The development of the anterior spinal artery is followed by an individually varying regression of the originally 31 bilateral segmental feeders. This numerical reduction is most pronounced in the lumbar region, where usually only one artery remains as a ventral feeder. The reduction is completed around the end of the fourth embryonic month. Consequently, the final number and distribution of the arteries supplying the medulla is determined by this time.

At the craniocervical junction the modifications of segmental supply need to be explained in more detail. The terminal intracranial part of the vertebral artery and its descending branch to the ventral surface of the upper spinal cord are homologous to the anterior radiculomedullary artery of the first spinal nerve (Arteria radicalis anterioris nervi primi; Kadyi 1889; Fig. 2.10). The ascending branch corresponds to the intracranial end-portion of the vertebral artery, running to the ventral side of the medulla oblongata. The descending branch is the cephalad origin of the so-called anterior spinal artery. The basilar artery has to be regarded as the continuation of this anterior arterial longitudinal tract of the spinal cord towards the brain stem. The other branches of the vertebral artery are, together, homologous to a posterior radiculomedullary artery of the first spinal nerve. The so-called posterior spinal artery, originating from the vertebral artery or from the posterior inferior cerebellar artery (PICA), corresponds to the descending branch. The PICA, with branches to brain and medulla oblongata, is homologous to an ascending branch of the posterior radiculomedullary artery of the first spinal nerve (Kadyi 1889).

To our knowledge there are no studies of the embryonic development of the medullary veins.

## 2.2 Segmental Supply to the Spine and Spinal Cord

The blood supply to the vertebral body, the paraspinal muscles, the dura, the nerve root and the spinal cord is derived from segmental arteries. This is modified but not essentially changed during embryonic life.

Fig. 2.1

Blood supply of spinal column and spinal cord. Schematic representation in axial view. With regard to the supply of the spinal (vertebral) canal and it's content the division of the posterior intercostal artery in a ventral and dorsal branch is the essential anatomical detail. The ventral branch follows the wall of the chest anteriorly in the intercostal space. Only the dorsal branch further divides into arteries which supply structures in and around the vertebral canal. Aside of branches to the dorsal paraspinal muscles a spinal branch regularly enters the spinal canal. But as a result of the embryonic desegmentation process the territory of supply is restricted to nerve root, dura mater and bony structures in the majority of segmental spinal branches. But at certain levels spinal branches have preserved anterior and/or posterior radiculomedullary branches to the spinal cord as shown on this schematic illustration (Modified from Thron 2008)

Fig. 2.2

Main sources of arterial supply to the anterior surface of the spinal cord. (a) X-ray in a.p. view. Infantile autopsy case following global filling of the large perispinal arteries with barium sulphate suspension. Only the two dominant feeders to the cervical and thoracolumbar enlargements of the spinal cord can be delineated (arrows). The artery of the cervical enlargement, originates from the thyreocervical trunk. The artery of the thoracolumbar enlargement, also called the great anterior radicular artery of Adamkiewicz originates from T12 on the right side in this example. Differences in vessel size between spinal cord arteries compared to segmental and paraspinal sources of supply can well be appreciated. (b) Schematic illustration of the potential sources of anterior arterial supply with accentuation of the main features of radiculomedullary arteries and the anterior superficial anastomotic tract, called anterior spinal artery. Connection with the posterior longitudinal channels of arteries at the level of the cone is delineated with dotted lines (b Modified from Thron 2008)

As outlined in Sect. 2.1, the pattern of segmental supply changes in the cervical and lumbosacral regions. Intrauterine vascular rearrangements result in the formation of longitudinal arteries in the cervical region. On each side, three vessels become potential sources of segmental spinal blood supply in this region, namely, the vertebral artery, the deep cervical artery and the ascending cervical artery.

In the sacral and lower lumbar regions, sacral arteries and the iliolumbar artery (supplying the L5 level) derived from the internal iliac arteries are established for the most important supply to the caudal spine. In the majority of the thoracolumbar region, segmental vessels persist as intercostal and lumbar arteries. The supreme intercostal artery connects several segmental arteries in the upper thoracic region. An angiographic evaluation of the entire spinal canal has to demonstrate all these potential sources of arterial supply.

But parallel to the vascular rearrangements concerning the pattern of segmental supply and parallel to the formation of the superficial spinal cord arteries, the embryonic transformation process also results in a reduced segmental supply of the spinal cord (Figs. 2.2, 2.7, and 2.8). Therefore, after the end of the fourth embryonic month most of the spinal branches do not have a branch supplying the spinal cord. They only divide into an anterior and a posterior artery of the vertebral canal, which supply the spinal column, and a radicular artery, supplying the dura and the nerve root at this level (Fig. 2.1). According to Manelfe et al. (1972), this radicular branch can be demonstrated at almost every segmental level and reflects the initially strictly segmental pattern of supply. Numerous illustrations concerning segmental supply of the spine are provided in the atlases and textbooks of Crock (1996), Crock and Yoshizawa (1977) and Crock et al. (1986).

### 2.2.1 Extra- and Intraspinal Extradural Anastomoses

1.

An extraspinal system connects the neighbouring segmental arteries longitudinally. The vessels course on the lateral aspect of the vertebra or transverse process (Figs. 2.1, 2.3, and 2.4). This system is highly developed in the cervical region, where the vertebral artery and the deep cervical and ascending cervical arteries form the most effective longitudinal anastomoses.

Fig. 2.3

Extra- and intraspinal anastomoses between segmental arteries at thoracolumbar levels. Contrast medium was injected selectively into the 12th intercostal artery. Note the hemivertebral blush at the level and side of injection. Numerous homolateral as well as contralateral segmental vessels are opacified through the anastomotic channels. The typical hexagonal configuration of the retrocorporeal intraspinal anastomosis (large arrows) is seen. The extraspinal pretransverse or anterolateral anastomoses are smaller in this example (small arrow) (Reproduced from Thron 2002)

2.

The intraspinal extradural system is mainly a transverse anastomosis, but also has longitudinal interconnections. The retrocorporeal and prelaminar arteries are the relevant vessels for the supply of bone and dura (Figs. 2.1 and 2.3). These anastomoses provide an excellent collateral circulation and therefore numerous segmental arteries can be visualized by injection into one segmental artery (Fig. 2.3). The extra- and intraspinal anastomoses protect the spinal cord against ischemia when pathologies, such as arteriosclerotic disease of the aorta, cause focal vessel occlusion.

Fig. 2.4

Anastomoses between segmental arteries at upper thoracic and lower cervical levels. (a) Supreme intercostal artery, supplying several upper cervical segments. An anastomosis exists to a muscular branch of the thyreocervical trunk (large arrow). The arrowhead points to a retrocorporeal anastomosis. (b) The thyreocervical trunk and its branches give rise to a cervical radiculomedullary artery (small arrowheads). The anastomosis with the supreme intercostal artery is again marked with a large arrow, as shown in (a) (same patient) (Reproduced from Thron 2002)

### 2.2.2 The Segmental Spinal Branch

The posterior intercostal (segmental) artery divides into a dorsal and a ventral branch. In the thoracic region the ventral branch is running circumferentially under the rib and meets the anterior intercostal artery. The dorsal branch, occasionally named the dorsospinal artery (Chiras and Merland 1979; Clavier et al. 1987), has a spinal branch to the vertebral canal (Fig. 2.1). It enters the vertebral canal through the intervertebral foramen and regularly divides into three branches: an anterior and posterior artery of the vertebral canal, which supply the spinal column, and a radicular artery, which supplies the dura and nerve root at every segmental level. Dorsal muscles and bony parts of the spinal column are other structures supplied by this dorsal branch (Fig. 2.1).

The hemivertebral blush, resulting from injection into a segmental artery, may help in identifying the artery (Fig. 2.5c). At the thoracic level, the artery is named according to the number of the rib under which it courses.

Occasionally, the proximal part of a segmental artery gives rise to two (or more) ventral branches of neighbouring intercostal arteries, as shown in Fig. 2.5a. This means that the common stem supplies two intercostal spaces. But as long as only one dorsal branch can be shown, demonstration of the other one is missing and the presence of a pseudo-bimetameric trunk has to be presumed. Consequently, a separate small posterior intercostal artery, from which the spinal branch of the second metamere arises, has to be looked for. This constellation is demonstrated by Fig. 2.5b. A small seperate artery from the aorta represents the posterior branch of the T8 segmental artery and supplies the corresponding spinal structures, examplified by the intense hemivertebral blush, shown in Fig. 2.5c. This may be crucial when searching for the site of a dural arteriovenous fistula or the origin of a radiculomedullary artery (Lasjaunias et al. 2001; Mosimann et al. 2014).

Fig. 2.5

Spinal angiography demonstrating pseudo-bimetameric supply of T9 and T8. (a) One posterior intercostal (segmental) artery (T9) is the common stem for two ventral branches (large arrow). (b) The proximal posterior intercostal artery T8 together with the posterior branch of this segment are originating as a separate small artery from the aorta (small branch). (c) Note the vascular blush of the T8 hemivertebra on the digital subtraction image. Concerning arterial supply of spinal column and spinal cord and its surrounding structures the posterior branch of the segmental artery is the relevant feeder which has to be looked for (Reproduced from Thron 1988)

## 2.3 Radicular and Radiculomedullary Arteries

Several nomenclatures and classifications have been used to describe spinal cord arteries. This is an ongoing cause of misunderstanding. In the past, the main problem occurred with the term "radicular artery". It was not clear whether it meant (a) a blood vessel supplying only a "root" ("radix") or (b) an artery supplying a root and going along with the "radix" to reach and supply the spinal cord. These two different types of arteries both exist, because of the individually varying regression of an initially purely segmental supply of the entire myelomere during embryological life. Therefore, the introduction of the term "radiculomedullary artery" is a helpful and anatomically correct specification of terminology. We therefore suggest this slight modification of the older anatomical classifications with the following differentiation of spinal radicular arteries:

1.

Radicular arteries supplying only nerve root and dura mater, but not the spinal cord. This type of vessel exists at every level and both sides.

2.

Anterior radiculomedullary arteries in which the persistent medullary branch is running with the anterior nerve root to join the longitudinal trunk, which has been called the anterior spinal artery (Figs. 2.1 and 2.6).

3.

Posterior radiculomedullary arteries in which the persistent medullary branch accompanies the posterior nerve root and joins the longitudinal systems on the posterior aspect of the spinal cord. They have been called posterolateral and/or posterior spinal (Figs. 2.1 and 2.6).

A classification proposed by Lasjaunias and Berenstein (1990) differentiates three types of spinal radicular arteries: radicular, radiculopial and radiculomedullary.

The first type of spinal radicular artery is the small branch, present at every segmental level, which is restricted to the supply of the nerve root. The second type supplies the nerve root and superficial pial plexus (e.g. posterior radicular artery). The third type is characterized by it's predominant ramification in the central grey matter of the medulla.

This classification may offer some advantages for the interventional neuroradiologist when compared to a classical anatomical differentiation. It stresses the importance of the anterior (central artery) supply for the grey matter of the spinal cord parenchyma and the potentially higher risk when embolization in this territory is performed. From an anatomical and functional point of view, however, this classification is not convincing. Some arguments shall be mentioned.

Anterior and posterior radiculomedullary arteries share in the blood supply not only of the outer fibre tracts (white matter), but also of the centrally located grey matter. The respective proportions vary between individuals and between different spinal cord regions. In the upper cervical spinal cord an anteromedian tract may not be present at all. Instead, a pial network of superficial arteries may cover the ventral surface (Figs. 2.35a, c and 2.36b). In other spinal cord regions only the very central part of the grey matter and the very peripheral part of the fibre tracts have exclusive supply from the central or the peripheral system. In an intermediate zone, branches from both systems may replace each other. This can be appreciated in Figs. 2.28, 2.29, and 2.30 demonstrating the areas of supply in the transverse section. Anterior and posterior longitudinal tracts represent pial arteries (Kadyi 1889) contributing to the pial network covering the entire spinal cord. Both systems anastomose with each other, not only around the cone but also through other superficial and different types of intrinsic anastomotic interconnections (Sects. 2.4 and 2.7).

Radiculomedullary arteries feed into the longitudinal tracts at various segmental levels. The branching of a radiculomedullary artery in a ventral and dorsal feeder at the same level is the exception in man (Jellinger 1966a). The vessel pierces the dura ventrocaudally of the nerve root.

Fig. 2.6

Schematic illustration of radiculomedullary supply. These arteries, restricted to some segmental levels, accompany either an anterior or a posterior nerve root or occasionally anterior and posterior roots at the same level to reach the surface of the spinal cord and constitute the longitudinal anastomotic systems. The tract of the anterior spinal artery is running on the anterior midline. It is supplemented by longitudinal systems, which may be located in posterior and/or posterolateral position with regard to the entry of the posterior nerve root

Fig. 2.7

Origin and number of anterior radiculomedullary arteries, which are reduced to an average of six segmental feeders at the end of the fourth month of embryonic life. This numerical reduction is most pronounced in the lumbar region, where usually only one artery remains as an anterior feeder. (Modified from Thron 2008)

Fig. 2.8

Origin and number of posterior radiculomedullary arteries (schematic drawing). The number of these arteries is less drastically reduced to 11–16 feeders during the embryonic transformation processes. The sources of supply do not differ from the arteries, which reinforce the anterior longitudinal tract. The complex posterior network of longitudinal and transverse channels is demonstrated in a schematic, simplified manner

The number, calibre and entrance level of anterior and posterior radiculomedullary vessels were determined by numerous authors. As Jellinger (1966a) and Piscol (1972) have shown, statistical evaluation of a big number of cases and comparisons with previous studies produced relatively reliably results without essentially diverging from the description of Kadyi (1889).

Out of initially 31 paired feeders from all segmental levels in early embryonic life only 2–14 anterior radiculomedullary feeders, on average six persist at the end of the fourth month of embryonic life to reinforce the spinal cord's superficial arteries on the anterior and anterolateral surface (Fig. 2.7) (Jellinger 1966a; Piscol 1972).

Kadyi (1889) and Piscol (1972) described an inverse correlation between number and calibre of the anterior radiculomedullary vessels supplying the entire spinal cord. When they are few in number (two to five), which is called paucisegmental type, these vessels are of large calibre and they are concentrated in the cervical and thoracolumbar regions. The presence of at least six feeders is called plurisegmental type and results in small calibres (Fig. 2.9).

Dominant radiculomedullary arteries typically supply the large volumes of grey matter in the enlargements of the spinal cord. The arteria radicularis magna (Adamkiewicz artery) is the dominant anterior radiculomedullary feeder at the thoracolumbar level. It mostly arises at the lower thoracic or upper lumbar level (T9–L1) and more frequently on the left than on the right side. The artery of the cervical enlargement (Lazorthes et al. 1958) arises from the lower thoracic level (C5–C7) more often as a segmental branch of the ascending or deep cervical arteries than of the vertebral artery (Figs. 2.7 and 2.34).

Fig. 2.9

Pluri- and paucisegmental supply exemplified on X-rays of two spinal cord specimens. (a) This specimen is an example of a rather plurisegmental type of supply with at least six anterior radiculomedullary arteries (open arrowheads). The feeder to the thoracolumbar enlargement entering at the T11 level is considerably larger than the additional five radiculomedullary contributors to the remaining spinal cord. (b) Three equally large radiculomedullary feeders (open arrowheads) accomplish blood supply to the entire anterior two thirds of the spinal cord (paucisegmental type). Posterior radiculomedullary and superficial arteries of less size (small arrowhead in a and b) are connected to the anterior spinal artery by anastomotic circles around the cone. (c) Diagram showing an average number of radicular feeders between the extremes of 2–14 (a Reproduced from Thron 1988, c modified from Thron 2008)

## 2.4 Superficial Arteries of the Spinal Cord

The network of superficial arteries of the spinal pia mater includes two systems.

1.

The anterior and posterolateral/posterior spinal arteries as the primary longitudinal arterial chains and in addition

2.

The pial arterial networks of lower degree.

The so-called anterior spinal artery and the posterior/posterolateral spinal arteries are not arteries in a common sense. Instead, they are systems of longitudinal anastomoses, connecting the ascending and descending branches of neighbouring radiculomedullary arteries. Therefore, they are called longitudinal (arterial) tracts or trunks in many textbooks. Kadyi (1889) suggested the term Tractus arteriosus medulla spinalis for these longitudinal arterial chains (Additionally, he stated that spinal artery is an inappropriate term for an artery supplying the medulla and not the spine.)

Nevertheless, we suggest keeping the terms anterior, posterolateral and posterior spinal artery and we will concurrently use them in this treatise, as they are commonly used in clinical practice.

The course and branching pattern of the anterior radiculomedullary arteries on the ventral surface of the spinal cord show characteristic features. Before reaching the midline, the ascending branch is issued (from the radiculomedullary artery) and diverges cranially in a slight curve to the anterior median fissure. The main artery continues on an ascending course, before it bends in a hairpin curve into the descending branch. At low thoracolumbar levels of origin the ascending branch of the radiculomedullary artery is usually considerably larger than the ascending branch (Figs. 2.12, 2.15, 2.51, and 2.52).

In cases in which branching occurs distinctly apart from the midline, the unconcealed segment of the anterior fissure is penetrated by multiple steeply ascending sulcal (central) arteries, issuing from the hairpin curve (Figs. 2.14 and 2.57).

This mode of branching and the appearance of a hairpin course are similarly found in the posterior radiculomedullary arteries (Fig. 2.16c) and are typical for all radiculomedullary blood vessels, including veins (Fig. 4.2), which have a steep, cranially directed course to the spinal cord (as a result of the ascension of the cord). Consequently, branching in the upper thoracic region is more often T-shaped. The difference in calibre between the ascending and descending branches in the lumbar region is quite variable and, according to our observations, also independent of the entrance level, frequency or calibre of the thoracic feeders.

The anterior spinal artery may be very thin or even interrupted as a continuous tract in the upper thoracic and upper cervical regions of the spinal cord (Figs. 2.12, 2.35, and 2.36). At the lower end of the spinal cord the small artery of the filum terminale constitutes the direct continuation of the anterior spinal artery. Additionally, lateral branches form anastomotic circles between the anterior with the posterolateral longitudinal trunks (Figs. 2.31, 2.51, and 2.52).

Nevertheless, the main source of arterial supply to the cord is the anterior spinal artery (ventral axis), with a multisegmental distribution of blood and a distinct territory of supply. It gives rise to the hemodynamically important central (centrifugal) system, which supplies the major part of the grey matter. Additionally, the anterior longitudinal trunk provides branches to the ventral two-thirds of the pial arterial network of lower degree on the anterior and lateral surface (Figs. 2.13 and 2.19).

Both systems supply a superficial network of smaller pial arteries that covers the spinal cord and from which the peripheral arteries of the centripetal system originate (Figs. 2.13, 2.14, 2.15, and 2.16).

The posterior/posterolateral arteries do not have such a distinct territory of supply as the anterior spinal artery, which means that they predominantly reinforce the rope-ladder-like network of posterior pial arteries.

The posterolateral tracts are located laterally and the posterior tracts medially to the posterior root entry zone. These longitudinally oriented vessels may not be continuous over the whole length of the spinal cord and they may replace each other. The posterior/posterolateral spinal arteries distribute blood to the dorsal one-third of this pial network, and in this way they share with central artery branches in the supply of the posterior horn and marginal parts of the central grey matter (Fig. 2.13).

However, there is a significant anastomotic interconnection between anterior and posterior longitudinal trunks formed by two anastomotic semicircles around the cone. It is called the arcade of the cone. The calibre and symmetry of the two sides are rather variable (Figs. 2.7, 2.31, 2.51, and 2.58).

Fig. 2.10

Superficial spinal cord arteries of the cervicothoracic region on the anterior (a) and posterior (b) surface. The anatomical illustration of the relationship between arteries and the basal cranial and spinal nerves at the craniocervical junction is very informative. Compare Section 2.1. (Reproduced from Kadyi's monograph, 1889; Upper half of Tafel I Fig. 1 (a), 2 (b). The unsurpassed realistic and instructive anatomical drawings were designed by himself and realized together with the painter Heinrich Dyrdon)

Fig. 2.11

Superficial spinal cord arteries of the lower thoracic and lumbosacral region on the anterior (a) and posterior (b) surface. (Reproduced from Kadyi's monograph, 1889; Lower half of Tafel I Figs. 1 (a), 2 (b). The unsurpassed realistic and instructive anatomical drawings were designed by himself and realized together with the painter Heinrich Dyrdon)

Fig. 2.12

X-rays of contrast-filled spinal cord specimens of the cervicothoracic (a) and thoracolumbosacral (b) region in a.p. view. It is difficult to define localization and contiguity of blood vessels on these plain films in a.p. view because many structures superimpose each other. Therefore sectioning of the specimens was performed in axial, coronal (frontal) and sagittal planes, as demonstrated on the diagrams. The results are comparable to tomographic imaging techniques and provide images from different parts of the volume without superimposition. In this way the three-dimensional course of intrinsic spinal cord blood vessels can be followed

Fig. 2.13

Diagram demonstrating the position of the superficial arteries. The longitudinal tracts are reinforced at certain levels from radiculomedullary arteries, which accompany an anterior or posterior nerve root to the surface of the spinal cord. The central arteries and the pial arterial plexus (vasocorona) on the ventral and lateral surface receive blood from the anterior spinal artery. The pial arterial network on the dorsal aspect of the cord is supplied by posterior longitudinal tracts. They differ in their position to the posterior root entry. The posterolateral artery is running lateral to it

Fig. 2.14

Superficial spinal cord arteries. Details of pial arteries at the entrance of the great anterior radiculomedullary artery. (a) X-ray film of the injected specimen. The division of the anterior radicular feeder (large arrow) into the ascending and descending part to the anterior longitudinal tract may be lateral from the midline. Note the asymmetrically developed arcade of the cone and the varying development of posterior longitudinal tracts in either posterior (small arrow) or posterolateral position (median sized arrow). (b) Microangiogram of the anterior surface (section S1). The paramedian position of the ascending and descending anterior tract results in a prolongation of central arteries to reach the entrance of the anterior fissure. Numerous branches derived from the anterior spinal artery form a dense superficial pial network on the anterior surface and on the nerve roots. (c) Microangiogram of the posterior surface (section S3). Posterior longitudinal tracts in changing positions and calibres (arrows)

Fig. 2.15

Superficial arteries of the anterior and the posterior surface above and below the entry of the great radiculomedullary artery. (a) X-ray film of the injected specimen in a.p. view. The vertical lines indicate the position and vertical extension of the anterior and posterior sections shown in (b–e). (b, c) Low thoracic level. Almost equal size of anterior and posterior longitudinal tracts. (d, e) Lumbar level. Clearly dominating anterior spinal artery (d) with numerous branches in oblique or horizontal direction to supply the anterior two-thirds of the superficial pial network (vasocorona). Posteriorly (e), rope-ladder-like linked tracts with a stronger posterolateral component (Reproduced from Thron 1988)

Fig. 2.16

Superficial arteries at the lower end of the spinal cord. (a) X-ray film of the injected specimen in a.p. view. In addition to the great anterior radiculomedullary artery of Adamkiewicz, entering the spinal canal at the T10 level, a posterior radiculomedullary artery (large arrowhead) reinforces two posterolateral longitudinal tracts of the posterior surface (small arrowheads). The anastomotic connection to the anterior spinal artery at both sides of the cone occurs at different levels. (b) and (c) are vertical reconstructions of frontal microangiograms. (b) Anteriorly, the superficial pial branches of the anterior spinal artery are outlined without superimposition. (c) On the posterior surface the rope ladder like network of pial arteries is reinforced from a posterior radiculomedullary feeder (large arrowhead). The longitudinal trunks in lateral position (small arrowheads) are the dominating arterial structures of the posterior pial plexus in this specimen. This figure is a good examples of the supreme information given by radiographic techniques which can be obtained following sectioning of the injected spinal cord in different planes (Reproduced from Thron 1988)

## 2.5 Intrinsic Arteries

Ever since the fundamental studies of Adamkiewicz (1881, 1882) and Kadyi (1889), the arteries directly supplying the spinal cord are divided into a central (centrifugal) and a peripheral (centripetal) system.

Fig. 2.17

Schematic illustration of intrinsic arterial blood vessel distribution in axial and sagittal plane. It should facilitate the understanding of blood vessel configurations shown on microangiograms of slices, cut in different planes. The central and the peripheral systems can easily be discerned in this drawing. Be aware that the central arteries go either to the right or to the left hemicord. Course of arterioarterial anastomoses between the central artery branches and the superficial systems is outlined in the axial plane on top

The central (sulcal) arteries constitute the centrifugal system. They approach from the anterior arterial tract and pass into the depth of the anterior median fissure. They, penetrate into the myelon on the left or right before the white commissure and branch tree-like (centrifugally) mainly in the grey matter of a hemicord (Figs. 2.17 and 2.18).

The peripheral arteries (perforating branches; rami perforantes) are derived from the pial network covering the surface of the spinal cord including the surface of the anterior fissure. They mainly consist of numerous small arteries and pass centripetally through the white matter in a radial course (Figs. 2.13, 2.17, 2.18, and 2.22). They are of different size and length and have to be regarded as end arteries like the central arteries. This entire centrifugal system was designated as the corona vasorum or vasocorona (Adamkiewicz 1881). Perforating branches do not keep to borders of different nervous tissue. They may end within the white matter or go deeper to the peripheral parts of the grey matter. Vice versa, centrifugal branches of the central arteries may pass the borders of grey matter and additionally supply white matter. The differences between the architecture of nervous tissue components in the spinal cord and the architecture of intrinsic blood vessels was repeatedly mentioned and stressed by Kadyi (1889). They can be confirmed by a big number of microangiograms in this book.

### 2.5.1 Central Arteries

The number, course, branching pattern and vascular territory of the central arteries can only be adequately viewed three-dimensionally. The X-ray visualization chosen here in axial (horizontal), coronal (frontal) or sagittal sections (Fig. 1.1) offers the additional possibility of eliminating superimposition of structures at various depths. In this manner, the deep, inner vessels of the myelon can be visualized separately from the superficial systems.

The number of central arteries is most easily determined in mediosagittal sections of the spinal cord. It varies substantially from individual to individual and in different spinal cord regions. The same applies to calibre. The data determined here in contiguous sagittal sections range from 170 to 210 central arteries per spinal cord and are somewhat lower than generally assumed until now. A false calculation from lateral projections could be due to superimposition of arteries going to left and right at the same level. However evaluation of consecutive frontal sections produced identical results. The observed discrepancy may be explained by the inclusion of very small arteries of the cone region and by inclusion of small arteries to the anterior white column next to the anterior fissure, which actually are branches of the vasocorona or of the central arteries within the anterior fissure.

The number of central arteries is 60–80 for the lumbosacral region (length 9–11 cm), 60–70 for the thoracic region (length 20–22 cm) and 50–60 for the cervical cord (length 10–12 cm). As shown impressively by Fig. 2.26, the densest sequence of side-alternating central arteries is found in the region of the enlargements with 7–12 arteries per centimetre. In the thoracic region there are only 2–3/cm. This equals an average of 5–9 per segment.

Determining the angle between the sulcal arteries and the anterior spinal artery is not essential, because deviations are numerous and the course may change from cranial to caudal direction even among central arteries issued from the same ascending or descending branch.

The essential features established from evaluation of our material can be summarized by the following statements:

  * Spinal cords showing a straight course of the central arteries and those showing a very tortuous course in the sagittal plane are found with almost equal frequency (Figs. 2.58, 2.59, and 2.60). Whether the second type represents a primary condition or a secondary vessel elongation cannot be discerned because of the high average age of our patients.

  * In relation to the longitudinal axis of the cord (or the anterior spinal artery), the central arteries can have an ascending, horizontal or descending course. Their course in the region of the enlargements is predominantly horizontal (more likely ascending). The mid- and upper thoracic regions mainly exhibit clearly ascending vessels (Figs. 2.24 and 2.25) while descending vessels are found sporadically scattered in all segments (Fig. 2.47). A high entrance level of the great radiculomedullary artery was observed in some specimens showing long descending vessels and vice versa (Figs. 2.59 and 2.60).

  * Steeply ascending and very long central arteries, which parallel the course of the anterior spinal artery, can be found at the paramedian bifurcations of large anterior radiculomedullary feeders (Fig. 2.57). Similar features are displayed by the central arteries in the entire thoracic region, where they can ascend parallel to the anterior spinal artery up to 1 cm, before they bend horizontally into the anterior median fissure (Figs. 2.46 and 2.47).

  * The vessel calibre of the central arteries varies considerably intra- and interindividually (Fig. 2.48), e.g. between 0.1 and 0.2 mm in the region of the lumbar enlargement (Table 1.2).

As mentioned above, the central arteries bend either to the right or to the left into the medulla and do not ramify in the depths of the fissure into bilateral branches as described at one time. This false impression is produced in axial sections when neighbouring central arteries overlap or become projected upon one another (Figs. 2.18 and 2.53). The true situation can be easily assessed in oblique sections of the central artery's origin and in frontal views: a short, common trunk may be found; however, a course alternating from side to side predominates (Figs. 2.19 and 2.21). This fact, too, reflects the originally bilateral, symmetrical arrangement.

The horizontal and vertical arborization of the central arteries within the spinal cord can be readily recognized in microradiographic sections. Horizontal branches of close succession are predominant in the enlargements while thoracically the steeply ascending and descending branches of large calibre prevail (Fig. 2.25). Inspections of our early cord preparations led to the impression that the ascending and descending branches could join to form an inner longitudinal anastomosis, which Adamkiewicz (1881) assumed to be the paracentral artery. In the course of this study, however, careful analysis of vascular branching in frontal and sagittal sections corroborated Kadyi's findings (1889) of a close intertwining and overlapping of the terminal branches. As shown by the microradiographs of all spinal cord segments, a continuous inner longitudinal anastomosis does not exist, the same is true for significant anastomoses between two neighbouring central arteries on the arterial or arteriolar level (Figs. 2.20, 2.23 and 2.26).

The horizontal distribution of central arterial branches is demonstrated best in axial sections (Figs. 2.18, 2.22, and 2.37). After issuing smaller branches to the anterior white column, located next to the anterior fissure, and to the ventral marginal zones of the anterior horn, and after entering the grey matter, the main stem branches out fascicularly into the anterior horn, the lateral column, the central gelatinous matter and the central components of the posterior horn.

In view of their great variability, denomination of the individual branches or branch groups is not essential. Isolated branches of this ramification also reach neighbouring fibre tracts, yet locally and individually to a very variable extent.

Whereas consecutive, approximately 2-mm-thick axial sections of the enlargements each contain at least 1–2 central arteries whose horizontal branching can be examined, many thoracic sections show none or only a short vessel transection in the ventral fissure (Figs. 2.37 and 2.45). This becomes clear when inspecting the vessel courses in sagittal sections (Figs. 2.46 and 2.47). A picture of the spatial distribution of these arteries, which are vital for the supply of the medullary grey matter, is provided by microradiography in different sectional planes (Figs. 2.23, 2.27, and 2.50).

Fig. 2.18

Superficial and intrinsic arteries of the spinal cord. Microangiogram of a transverse section at the L2/3 level. Three millimetre slice thickness. Several superimposed sulcal arteries pass to one side or the other of the cord and branch out mainly in the grey matter. Additional small vessels to the funiculus anterior and the cornu anterius originate in the anterior median fissure as branches of the central arteries or as branches from the pial plexus of lower degree (arrow). Note the variability of branches supplying the posterior horns. They may be derived from the central arteries (centrifugal system) or from the pial arterial network on the dorsal aspect of the cord (centripetal system), which is supplied from the posterior longitudinal tracts. The pial arterial plexus on the ventral and lateral surface receives blood from the anterior spinal artery (see section 2.6) (Microangiogram reproduced from Thron 1988)

Fig. 2.19

Superficial and intrinsic branches derived from the anterior spinal artery. (a) Coronal microangiography of the anterior surface. The anterior spinal artery has lost its previous content of contrast medium. The stems of the central arteries, running into the anterior fissure (arrows), are therefore not covered by the arterial midline tract. Extension of the superficial network of pial branches derived from the anterior spinal artery includes the depth of the anterior fissure. (b) Coronal microangiography of the midline section. Ramification of the central arteries in horizontal and vertical direction mainly within the grey matter of the anterior horns. The small arteries in the outer fibre tracts are penetrating branches derived from the lateral parts of the vasocorona

Fig. 2.20

Intrinsic arteries of the spinal cord. Microangiogram of a mid-sagittal section at the level of entry of the great anterior radiculomedullary artery (arrow). The central arteries take a horizontal or slightly ascending course (arrowheads). In this plane the vertical distribution of long central artery branches near the central canal can be demonstrated very well and the perforating arteries within the posterior columns can be appreciated in their typical tree-like configuration (Reproduced from Thron 1988)

Fig. 2.21

Intrinsic arteries of the spinal cord. Microangiogram of a median coronal section at the C4–C5 level. The central arteries (small arrowhead) show an irregular side-alternating distribution. In this median part of the cervical enlargement the number of central arteries is relatively high, the vertical ramification is therefore only moderate. The branches of neighbouring central arteries intertwine, but do not form inner anastomotic interconnections. Superficial arteries of the pial network (large arrowhead) provide blood supply through the centripetal system of small perforating arteries (Reproduced from Thron 1988)

Fig. 2.22

Superficial and intrinsic arteries in a specimen presenting with an optimal result of contrast filling. (a) X-ray film of the injected spinal cord specimen in a.p. view. The great anterior radiculomedullary artery and two posterior radiculomedullary feeders are connected to each other by the anastomotic arcades around the cone. (b, c) Axial microangiograms of mid-lumbar (b) and lower thoracic level (c). There is an equally good distribution of the contrast medium to all vascular territories. Even the very small precapillary arteries are opacified. Differentiation of vascular territories of supply is not possible. Posterior longitudinal tracts are situated medially, posterolateral ones laterally of the posterior root entry zone. These tracts are supplemented by smaller ones (arrowheads) in anterior, lateral, or posterior positions. They constitute together with additional smaller branches the pial arterial network of lower degree (b Reproduced from Thron 2002; c Reproduced from Thron 2008)

Fig. 2.23

Intrinsic arteries at thoracic level. Microangiograms of median coronal sections. (a) X-ray film of the injected spinal cord specimen in a.p. view. The vertical lines indicate the position of the sections shown in (b–e). There are small gaps, caused by axial slices, as indicated. (b–e) The number of central arteries is considerably smaller, the vertical extension of the central artery branches considerably larger compared to the blood supply in the enlargements. Arterioarterial anastomoses between central arteries and the superficial system (arrowheads in c and d) are frequent findings. But intrinsic longitudinal anastomoses between central artery branches are not verifiable. Supply from the posterior superficial system is much stronger than in other parts of the spinal cord (Reproduced from Thron 1988)

Fig. 2.24

Intrinsic arteries. Course of central arteries throughout the length of cervicothoracic spinal cord (Figs. 2.24 and 2.25). (a) X-ray film of the injected specimen in a.p. view. (b–e) Microangiograms of mid-sagittal sections at cervical and upper thoracic levels. The sections c and d are contiguous. The course of the central arteries is tortuous and slightly ascending in the cervical region (b, c) and becomes increasingly steeper in the upper thoracic levels (d, e). Solitary or interconnected central arteries run parallel to the anterior spinal artery over some distance before turning into the depth of the anterior fissure. Compare Fig. 2.25b

Fig. 2.25

Intrinsic arteries. Course of central arteries throughout the length of cervicothoracic spinal cord Continuation of Fig. 2.24. (a) X-ray film of the injected specimen in a.p. view. (b–e) Microangiograms of mid-sagittal sections at upper to mid-thoracic levels. The sections (c and d) are contiguous. In (b), the contrast medium has been lost in a part of the anterior spinal artery. This reveals the primarily ascending course of the small number of central arteries in the pial covering of the anterior fissure of the upper thoracic spinal cord (b, c). In the mid and lower thoracic cord central arteries may be more numerous but small in size, often matched by a large number of large perforating arteries from the vasocorona (d, e)

Fig. 2.26

Intrinsic arteries. Microangiograms from mid-coronal sections including the grey matter of the anterior horns. The sections were obtained from the cervical enlargement (cranial to C5), the upper thoracic region (cranial to T5) and the thoracolumbar enlargement (cranial to L3). Section length 2.5 cm, slice thickness 2–3 mm. Note the differences in the spatial distribution of central arteries and the preferential plane of their ramification. Furthermore, size course and degree of overlap of central arteries and their branches can be compared at these levels. The number of central arteries is about 16 per 2.5 cm in the cervical, 9 per 2.5 cm in the thoracic and 26 per 2.5 cm in the lumbar region. Anastomotic connection between the central system and the superficial pial network at the T5 level (Reproduced from Thron 1988)

### 2.5.2 Peripheral System

The posterior longitudinal anastomoses (posterolateral and/or posterior spinal arteries) function as a superficial pial supply system of first degree. Numerous superficial branches of the anterior spinal artery and the longitudinally directed network of posterolateral and/or posterior arteries feed a dense pial network of lower degree, from which the perforating branches of the peripheral system arise. This is very well demonstrated on microradiographs of frontal and sagittal sections (Figs. 2.14, 2.20, 2.55, and 2.58). The larger vessels of this pial network branch irregularly into ascending and descending vessels that can join the course of the roots (Figs. 2.14, 2.15, and 2.16). They, however, end after a few centimetres. These superficial vessels of second and third degree should not be specially designated as anterolateral or lateral arteries. Instead, they should be assigned to this part of the pial network, which supplies the peripheral system of penetrating branches. Especially above the enlargements, these smaller vessels form an impressive secondary anastomotic system between the anterior and posterior longitudinal anastomoses, although no significant anastomotic capacity can be attributed to the individual rami.

The penetrating branches appear angiographically as a largely uniform, radial vascular system. The almost exclusively thin arteries with calibres between 10 and 50 μm terminate in the external fibre tracts or in the marginal zone of the grey matter. Longer branches of larger calibre exist only on both sides of the posterior root's entry zone and as branches of the anterior system to the anterior column and anterior horn (Figs. 2.19, 2.37, and 2.53). Even oblique longitudinal sections, which follow the course of a posterolateral artery over several centimetres, do not display larger constant branches going directly to the cord. For this reason there is no need to develop such an extensive nomenclature for the vasocorona, as several anatomists have done, neither for its superficial nor its intramedullary components. From an angiographic-morphological standpoint, the superficial longitudinal and transverse connections attributed to the pial systems of lower degree do not suggest the function of supplying selective territories via larger branches. Rather, they guarantee a constant blood distribution from the periphery.

### 2.5.3 Capillaries of the Spinal Cord

Since only the diameter of injected vessels can be assessed in microradiographs, the exact transition of arterioles into capillaries and venules cannot be accurately determined. Nevertheless, evaluation of all specimens showing good, simultaneous filling of capillary vessels (Figs. 2.27 and 2.28) provides an impressive visualization of the difference in capillary density between grey and white matter, as has been shown by histological studies. The capillary networks are densest within the grey matter of the enlargements. In accordance with the microradiographical findings of Turnbull et al. (1966), no unequivocal difference between anterior and posterior horn was detectable here. In contrast, the capillarization of the fibre tracts is much more loosely meshed. The occurence of capillaries in the spinal pia mater was examined exhaustively by Kadji (1889). He denied the existence of own pial capillaries insistently.

Fig. 2.27

Capillary density (a) X-ray of the specimen in lateral view. Low entry of the great anterior radiculomedullary artery (arrow). Poor filling of the posterior superficial pial network. (b–d) Axial microangiograms at the levels, indicated in a. There is a striking difference in the density of small pre-capillaries and capillaries between gray and white matter, not only in the lumbosacral enlargement (b), but also at the T9 level (c, d). The artery of the posterior median septum, opacified in c and d (arrowhead), is filled from the anterior spinal artery. Abbreviation: asa, anterior spinal artery (as empty vessel in b–d)

Fig. 2.28

Capillary density and areas of supply. (a–c) Axial microangiograms from thoraric levels. Distinctly higher density of arterioles and capillaries in the grey matter of the spinal cord compared to the white matter. The contribution of the anterior spinal artery to the pial system in the anterior two thirds is very well shown. Due to the low proportion of gray matter, central arteries do not play a major role for the supply of the cross sectional area in this region. The artery of the posterior median septum (arrowhead in a and b) is filled from the anterior circulation. Pial branches to the anterior funiculus and anterior horn originate from the anterior fissure (arrowhead in c)

## 2.6 Arterial Territories of Supply

Demonstration of the intramedullary territories of arterial supply can be achieved by demarcating the central from the peripheral supply system. This can also include a separation of the area fed by the anterior or posterior spinal arteries (Fig. 2.30).

Figure 2.31 illustrates three axial sections of a cord at different levels, together with their microangiographic images. It is clearly shown that the cross-sectional areas differ considerably in size and that the proportion of grey matter is variable. Determining the distribution area of the intrinsic arteries allows a basic pattern to be observed. The ramification territory of the central arteries corresponds rather closely to the proportion of grey matter. In the region of the thoracolumbar enlargement the central artery branches cover a third to a half of the sectional area. Their contribution decreases thoracically to a fifth or a sixth and lies cervically between these extremes. However, this relates only to the intramedullary branching of the central arteries and not to the region of supply served by the anterior spinal artery, which also nutrifies more than the ventral half of the outer tracts by its contribution to the pial arterial networks of lower degree. Furthermore, a strict division between the supply of the grey columns solely from the centre and that of the white matter solely from the periphery is not justified. In fact, with complete filling of even very small vessels, both territories can hardly be distinguished from one another in the marginal zone of the grey matter (Figs. 2.22, 2.29, and 2.30). Moreover, considerable local and interindividual variations occur here. Yet at the apex of the posterior horn, supply via branches of the vasocorona dominates (Figs. 2.37 and 2.45). Also at the edge of the anterior horn, centripetal branches of the peripheral system almost always contribute to the supply.

In the cervical region, the amount of grey matter on the transactional surface is proportionately less in comparison to lumbar. This corresponds to a reduced dominance of the main ventral artery here as well as to a smaller proportion of the transactional surface that is supplied by central arteries (Fig. 2.30). If sagittal and coronal sections are also included in the evaluation of supply areas, it can be seen that a lesser volume of grey matter is accompanied by both a reduction in calibre and number of central arteries. This consequently causes greater axial vascular ramification. The supply region of neighbouring central arteries, "overlapping" longitudinally, correlates more closely to a cone-shaped intermeshing when viewed three-dimensionally. In the presence of vascular occlusion in a short segment, deficient compensation can be most likely expected in the territory of the central arteries, since they are end arteries like the perforating branches but with a more extensive territory of supply.

Fig. 2.29

Vascular territories of supply. Limited filling of the anterior spinal artery at the lumbar enlargement. (a) X-ray of a specimen in a.p. view. Exceptionally in this case, injection of contrast medium into the great anterior radiculomedullary artery did not proceed to the posterior longitudinal channels via the arcades of the cone. In other spinal cord regions, this is an expected and common observation. (b) X-ray of a specimen in a.p. view. Typically, injection of a single anterior or posterior radiculomedullary artery in this lumbosacral region results in filling of the complete network of superficial arteries. (c) Axial microangiogram taken from the specimen in a at the L1 level. The arterial territory of supply from the anterior spinal artery is restricted to the anterior parts of the cross-sectional area. However, completion of filling seems to be suboptimal in this case. (d) Axial microangiogram taken from the specimen in (b). Seperation of territories in this lumbosacral region, connected by the arcades of the cone is generally not possible. Contrary, at cervical and thoracic levels the anterior spinal artery territorry can easily be defined by injecting this artery (Figs. 2.30 and 2.42). At lumbar levels the large calibre of the anastomoses at the cone inevitably includes filling of the posterior longitudinal tracts and consequently contrasts the entire arterial system on the cross-sectional area (d Reproduced from Thron 2002)

Fig. 2.30

Territories of arterial supply. This composition offers a morphological and microangiographical comparison between the cervical, the thoracic and the lumbar region with regard to cross-sectional surface areas, relations between grey and white matter and the schematically defined territories of supply. (a) Paraffin-embedded sections, prepared for axial microangiograms, demonstrate the differences of cross-sectional surface areas of the same specimen at cervical, thoracic and lumbar levels. The different proportions of grey and white matter are obvious. The grey matter presents as a dark butterfly-shaped area in a bright surrounding of white matter. (b) The middle row of images present microangiogams of axial sections cut at the level of the cervical enlargement, the mid-thoracic region and the lumbar enlargement. Examples have been selected, separating the contrast-injected area of anterior supply from the non-contrasted posterior area of supply. (c) Diagrams of the approximate territories of arterial supply. The grey zone corresponds to the area specifically supplied by the anterior spinal artery through the central arteries and the branches to the anterior pial system of lower degree (about two-thirds of the whole cross-sectional area). The dorsal white zone is supplied by the peripheral system, fed from posterolateral and posterior spinal arteries. The central territory inside the hatched area is supplied by the central arteries. It is not distinctly seperated from the peripheral system. The hatched intermediate area is variably supplied by one system or the other. The cross-sectional extension of the central system corresponds approximately to the volume and relative amount of grey matter, which is quite different at various levels. The conclusion is that rough territories of supply exist but that there is no strict attribution between vascular supply and anatomical structures (a, c Reproduced from Thron 1988)

## 2.7 Arterioarterial Anastomoses

### 2.7.1 Superficial Anastomoses

1.

The spinal cord is covered in its entire length by a net-like anastomosing vascular system, in which the anterior spinal artery and the bilateral posterolateral and/or posterior spinal arteries can be regarded as the most constant longitudinal anastomotic trunks of greatest calibre. The anterior trunk is directly connected to the posterior ones by arterial circles at the conus medullaris (rami cruciantes) (Fig. 2.31).

2.

Even though these main trunks may occasionally exhibit short interruptions or at least narrow parts, it should be noted that the network is supplemented by a system of closely meshed longitudinal and transverse anastomoses of second and third degree.

3.

In the thoracic region longitudinal connections between central arteries can be observed that run parallel to the anterior spinal artery at the anterior median fissure (Figs. 2.49 and 2.50b).

### 2.7.2 Transparenchymal Anastomoses

Transparenchymal arterioarterial anastomoses between central artery branches and superficial arteries exist in the thoracic region (Figs. 2.26, 2.32, and 2.33). They are, however, rare and demonstration of their course requires a special sectional plane. Direct proof of their existence only succeeds if they can already be assumed on a standard X-ray survey. The calibre of these vessels does not taper from the central artery to the surface. The direct connection to superficial longitudinal trunks leaves no doubt as to their arterial character. Nevertheless, these findings were additionally checked against series of histological sections to eliminate arteriovenous anastomoses.

Fig. 2.31

X-ray films of specimens from cadavers that were contrast-injected after fixation through the great anterior radiculomedullary artery (arrowhead). There is non-filling of small vessels, but the anastomotic circles around the cone (at the S3–S5 level; arrow) and the transverse interconnections between the posterior longitudinal tracts are exhibited impressively. (a) and (b) specimen with high entry of the artery of the lumbar enlargement (arrowhead) and very symmetrically develloped "arterial basket" around the cone. (c) and (d) low entry of the artery of the lumbar enlargement (arrowhead). Compensating larger caliber of the ascending branch of the anterior radiculomedullary artery and of the posterior system. In such anatomically well develloped cases of the arcades around the cone an important collateral function, similar to that of the circle of Willis at the base of the brain, is obvious (Reproduced from Thron 1988)

Fig. 2.32

Arterioarterial anastomoses between the central artery branches and the superficial peripheral system. (a) Schematic illustration of the two typical courses. The vertical arrow marks an anterolateral anastomotic connection exemplified in (b). The horizontal arrow to a posterolateral anastomosis, exemplified in (c and d). (b) Axial microangiogram demonstrating a centro-anterolateral connection (Type 1). (c) X-ray film of the whole specimen in a.p. view. Undissected anastomosis from the central system to the posterolateral surface (Type 2) (arrow). (d) Microangiography of this specimen in an oblique section from the anterior midline to the posterolateral surface. Only a short part of this anastomotic channel could not be included in the slice of about 2 mm thickness (arrow). The majority of intrinsic anastomoses are disrupted by sectioning because of their irregular and variable courses (b–d Reproduced from Thron 1988)

Fig. 2.33

(a–c) The anastomoses demonstrated on these mid-coronal microangiograms at thoracic levels from different specimens are directed from central arteries to the lateral surface of the superficial pial network (arrows). (d) position of the mid-coronal sections of the microangiograms related to the cross-sectional area of the spinal cord

Depending on the direction of course, we can differentiate the following types:

1.

Centro-anterolateral anastomoses (Fig. 2.32b)

2.

Centro-posterolateral anastomoses (Figs. 2.32c, d and 2.33)

These directions do not correlate to the site of primary or secondary longitudinal anastomotic trunks. In no case are arterial interconnections found in anteroposterior directions as with the venous anastomoses. They form an additional collateral system between central and superficial in the thoracic region, thereby demonstrating the plasticity of the spinal blood supply.

### 2.7.3 Intrinsic Anastomoses

A longitudinal anastomosis within the parenchyma between the ascending and descending branches of the central arteries, as was assumed by Adamkiewicz (1881) and later on by Fazio and Agnoli (1970), could not been verified in our specimens.

## 2.8 Specific Patterns of Arterial Supply in the Cervical Spinal Cord

Fig. 2.34

Sources of spinal cord blood supply to the cervical region. The arteries from which segmental and medullary supply is derived (vertebral, deep cervical and ascending cervical arteries) and the anterior spinal artery are presented in red, the posterior superficial channels in light red. (Reproduced from Dafotakis et al. 2008 as modification of Thron 2008)

Variations of arterial supply are very pronounced in this region (Figs. 2.35 and 2.36).

Furthermore, various collaterals connect the arteries, which are extramedullary sources of supply in the cervical region (see Fig. 2.34). This can be demonstrated using superselective in vivo angiography of the vertebral, deep cervical and ascending cervical arteries (Fig. 2.4). Neglecting this knowledge makes embolization procedures in the regions of the neck and skull base hazardeous.

The most important arterial feeders for the anterior medullary supply of the cervical region may be the descending branches from the intracranial section of the vertebral arteries like in Figs. 2.35a, b and 2.36a. But these arteries may also have a relatively small calibre like in Figs. 2.35c and 2.36b, c. More relevant radiculomedullary vessels for the cervical enlargement may enter between C4 and C7. These segmental branches originating from the extracranial part of the vertebral arteries or from the neck arteries may exhibit calibres of 0.4–0.6 mm. The largest feeder was named the artery of the cervical enlargement by Lazorthes (1958) (Figs. 2.9, 2.34, and 2.36). It is more often derived from the deep and ascending cervical arteries than from the vertebral artery. The average number of anterior radicular feeders for the cervical medulla is 2–3, with no significant lateralization in this region. In the individual situation all the three mentioned potential sources have to be checked bilaterally.

Well-developed descending branches from the terminal intracranial part of the vertebral arteries, uniting to form the anterior spinal artery, are a rarely observed pattern of supply to the upper spinal cord. As outlined in Sect. 2.1 the terminal vertebral artery corresponds to the stem of the ascending branch of the anterior radiculomedullary artery of the first spinal nerve. The descending branch of this radiculomedullary artery represents the cephalad origin of the anterior spinal artery (Kadyi 1889).

Descending feeders of equal size forming this median arterial axis were the exception in our specimens (1/14). More often, the vessel on one side dominated (right/left = 1:1), the contralateral being small or even rudimentary (Figs. 2.35 and 2.36a).

Often, two branches run parallel over a number of segments. The major branch then continues in the midline as the typical median longitudinal vessel. The minor one may also reach the midline, yet upon closer inspection, it rather terminates as a large central artery (Fig. 2.35a).

The continuity of a median arterial trunk is less constant in the cervical region than in the thoracic or lumbar regions. Furthermore, dorsolateral spinal arteries of large calibre are not unusual here.

All of the additional details described in the following, such as vessel duplication, pseudo-islands and net-like vascular patterns, have to be regarded as a state more closely related to the embryonic (or ontogenetic) condition.

Sometimes a bilateral network extends as far as the mid-cervical region with decreasing vessel calibre (Fig. 2.35c).

Further branching of the cervical anterior spinal artery may also occur. True island formation is less frequent than duplication according to our experience. Again, the major branch continues as the anterior spinal artery, whereas the minor one ends in a central artery (Fig. 2.35b). Duplication over some distance was seen in 7 out of 14 filled cervical cords (Figs. 2.35b, 2.26a, b, and 2.41). Anterior radiculo-medullary arteries of larger calibre most often enter from segments C4 to C8 (8 out of 14 of our cases) (Figs. 2.36, 2.37, and 2.42). Discontinuities of the ventral longitudinal axis (3 out of 14 of our cases are usually found between two zones, the upper one being directly supplied by the vertebral artery and the lower two-thirds being supplied by segmental tributaries of the deep cervical or vertebral arteries (Fig. 2.35c). The posterior system of cervical supply is usually derived from the PICA or the vertebral artery. The descending branches further divide into the dorsal and dorsolateral spinal cord vessels of variable calibre. Lasjaunias et al. (1985) call this vessel the "lateral cervical artery". However, corresponding to conditions on the ventral aspect it must be an equivalent of the descending branch of a dorsal radiculomedullary artery. Kadji (1889) therefore termed it "Ramus descendens arteriae radicalis posterioris nervi primi".

The average number for the cervical posterior radicular arteries is approximately 3–4. They approach the dorsal cervical medulla with a calibre of 0.15–0.4 mm (Jellinger 1966a; Piscol 1972).

The posterior longitudinal systems form a network of concatenated fragments, only exhibiting more dominant individual tracts towards the thoracic region (Figs. 2.10 and 2.38).

Fig. 2.35

Embryologically defined patterns of arterial supply on the ventral surface of the medulla oblongata and the upper cervical spinal cord. Photographs of injected specimens. (a) The typical finding of blood supply to this area is a large descending branch from one vertebral artery (arrowheads) and a less developed, often rudimentary vessel on the other side (black arrow). They do not unite. The small one (small black arrow) is usually ending separately as a central artery. The longitudinal tracts of the posterior surface originate as a descending branch from the vertebral artery or from the posterior inferior cerebellar artery in a (postero-)lateral position (white arrow; cf. Fig. 2.10a). (b) In many cases only a single descending branch from one vertebral artery is present. A plexiform network of short superficial vessels supplies the contralateral part of the medulla oblongata. Concerning the cervical anterior spinal artery, non-fusion of the originally bilateral tracts ("duplication") is frequent in variable physical forms (white arrowheads). True "island formations" are at least rare. Reunion of the two tracts was not observed in our cases. The smaller descending branch generally enters the anterior fissure and terminates in a central artery (white arrow). (c) Plexiform pattern of supply from descending branches of the vertebral arteries and radiculomedullary feeders, but without formation of a significant unpaired anterior spinal artery (Reproduced from Thron 1988)

Fig. 2.36

X-ray films of three injected specimens in a.p. view. Variations of arterial supply to the anterior surface of the cervical spinal cord. (a) The strong unilateral descending branch from the left vertebral artery establishes the median anterior arterial tract (big arrow). A short duplication on the opposite left side below C1 with pseudo-island formation (small arrow) is small and terminates as a central artery in the median fissure. On the right side a plexiform pattern of short branches covers the medulla oblongata. The main radiculomedullary contribution enters the anastomotic tract at the C6 level. (b) "Duplication" (non-fusion) of the anterior spinal artery cranial to the C4 level with small radiculomedullary feeders entering at both sides. The artery of the cervical enlargement joins the anterior spinal axis at the C6 level. (c) The main feeder is a radiculomedullary artery entering at the C7 level. Additional anterior supply by several small arteries from higher cervical levels (a Reproduced from Thron 1988)

Fig. 2.37

Changing pattern of arterial supply at cervical and upper thoracic level. (a) X-ray of the injected specimen and localization of the axial sections in (b–d). Axial Microangiograms at the C5 (b) and C7/8 level (c) and, for comparison, at the T6 level (d). In the cervical region (b, c), arterial filling is equally well distributed in all territories of supply. Note the dense capillary network within the grey matter and the dominant role of the anterior spinal artery (arrow in c). The section at the thoracic level T6 (d) demonstrates incomplete filling in the posterior column area but the calibre of anterior and posterior longitudinal tracts (arrow and open arrowhead) has significantly changed in favour of the posterior system. (Reproduced from Thron 1988)

Fig. 2.38

Superficial arteries of the lower cervical spinal cord. Coronal microangiograms of the anterior and posterior superficial section taken from the specimen shown in Fig. 2.37a. (a) Anterior section S1. The main anterior radiculomedullary artery enters at the C7 level. The extensive network of arteries shown on this superficial frontal section are branches which constitute the anterior pial network of lower degree including supply of the nerve roots. The central artery branches, running posteriorly into the anterior fissure are not well shown because of superimposition of the anterior spinal artery. (b) Posterior section S3. The posterolateral and posterior longitudinal systems form an irregular pial network with fragmentary chains (Reproduced from Thron 1988)

Fig. 2.39

Vertical ramification of central arteries in the cervical spinal cord. (a) X-ray of the specimen in a.p. view. The vertical lines indicate the position and length of the median (S2) coronal slices which are contiguous between C2 and C5. (b, c) Upper and middle cervical levels. The irregular side-alternating distribution of the central arteries to the right or to the left side are best shown in this coronal sections in median position (S2). Each of them covers approximately 5 cm of length. The vertical ramification is intertwining but does not form an inner anastomotic tract. (d, e) Lower cervical and upper thoracic levels. The density of central arteries in the slim cervicothoracic spinal cord region is far less. The vertical ramification is more pronounced. The supply by perforating branches of the pial network is more important. This corresponds to the different proportions of grey and white matter in these regions (Reproduced from Thron 1988)

Fig. 2.40

Microangiograms of mid-sagittal sections from different levels of the cervical region (b–d). Their position is marked by vertical lines on the X-ray survey shown in (a). (b) The anterior spinal artery appears to be very thin at the high cervical level (arrow), but this false impression is caused by non-fusion of the two primary anterior tracts (compare with a). (c) In the region of the cervical enlargement which involves parts (b and c), the number of central arteries is high. The blood vessels take an almost horizontal course. Additionally, numerous small perforating arteries arise from the pial plexus, covering the outer surface and the anterior fissure. (d) The calibre of the anterior arterial tract very often decreases at high thoracic levels. Rather typical is the steeply ascending course of the central arteries at high thoracic levels. Solitary or sometimes interconnected central arteries run parallel to the anterior spinal artery over some distance before turning into the depth of the anterior fissure. As a result of the small calibre, central arteries of this region are difficult to distinguish from perforating vessels of the peripheral system on mid-sagittal sections. Compare the course and ramification of intrinsic arteries with the mid-coronal sections of this region, shown in Fig. 2.39 (b, d Reproduced from Thron 1988)

Fig. 2.41

Superficial and intrinsic cervical arteries. Non-fusion ("duplication") of the anterior spinal artery. (a) X-ray film in a.p. view. (b) Mid-sagittal microangiogram of upper cervical level. The calibre of the central arteries is equal to that of the separated longitudinal tracts (small arrows), supplying the corresponding semi-cord. (c, d) Mid-sagittal microangiograms of mid-cervical level. Short common stems of two central arteries frequently occur in unpaired anterior spinal arteries (arrowheads)

Fig. 2.42

Anterior (and right lateral) epidural spinal tumour (Hodgkin's disease) at the C7–C8 level. (a) X-ray film of the injected cord which is flattened and compressed from the right side (large arrow). The anterior spinal artery is narrowed, but there is extensive pial hypervascularization at the tumour level. (b) Photo of the macroscopic aspect of the epidural tumour position. (c) Mid-sagittal and (d) axial microangiograms show anterior indentation and flatting of the cord (large arrows). There is still no obstruction of the anterior spinal artery and the sulcal arteries are patent although they are considerably displaced posteriorly into the anterior median fissure. Histology revealed normal findings (Reproduced from Thron 1988)

## 2.9 Specific Patterns of Arterial Supply in the Upper- and Mid-Thoracic Spinal Cord

The upper- and mid-thoracic region is commonly supplied by small radiculomedullary arteries 0.2–0.4 mm. Therefore, angiographical demonstration of feeders may fail (Figs. 2.43b, 2.47, and 4.1). The average number of anterior radiculomedullary arteries in the thoracic region is 2–3 (Figs. 2.23, 2.37, and 2.43). In several of our specimens, we found the anterior longitudinal anastomosis in this region to be extremely narrow (Figs. 2.40, 2.43b, c, 2.46, and 2.47), or even interrupted (1 case). Usually, however, it took the form of a continuous trunk of small calibre (Figs. 2.43 and 2.46).

Corresponding to the smaller cross-sectional area of this region and the relatively smaller portion of grey matter, the number of central arteries is only 2–3 per cm for this region. This explains the prevalence of steeply ascending and descending central artery branches (Figs. 2.25, 2.40d, 2.46, and 2.47). As pointed out earlier, the impression of an intrinsic longitudinal anastomosis on sagittal images was not confirmed on coronal images of this spinal cord region where there is a preponderance of white matter tracts (Fig. 2.44).

On the posterior surface of the cord the longitudinal tracts may run in posterior or posterolateral directions, thus indicating the functional identity of these longitudinal anastomotic tracts (Fig. 2.44).

For the same reason, the arteries of the posterior longitudinal system can either uni- or bilaterally exceed the vessels of the posterolateral system in calibre or even completely substitute it at least for some segments (Figs. 2.37d and 2.44c). The relation of vessel diameters clearly shows that the posterior as well as the anterior vascular supply is adjusted to the thinner thoracic cord.

As could be demonstrated on the thoracic cord, a continuous posterior longitudinal system does not exist. The fragmentary trunks in posterior and/or posterolateral position mainly supply the superficial network of smaller branches and from this second-degree pial network the perforating rami emerge to the white matter.

Fig. 2.43

Variability of number and calibre of radiculomedullary feeders and longitudinal arterial tracts in the thoracic region. (a) One single feeder reinforces the strong anterior spinal artery in the entire length of the thoracic spinal cord. (b) Two small thoracic radiculomedullary feeders are obvious, the lower one nicely demonstrates additional supply of the corresponding spinal ganglion. The calibre of the anterior spinal artery is almost filiform and hardly exceeds that of the posterolateral tracts. (c) Two medium-sized segmental feeders constitute an equally sized anterior spinal artery (arrows). Again combined supply of a spinal ganglion from the radiculomedullary artery. (d) A large-sized radiculomedullary artery at high thoracic level merges with anterior spinal tracts which are doubled (not-fused) for a certain distance (arrowheads)

Fig. 2.44

Typical relationships of anterior and posterior patterns of supply in the upper thoracic region demonstrated on coronal microangiograms. (a) The anterior spinal artery is of medium size and contributes to the dense pial network with transverse and longitudinal interconnecting branches, also supplying the nerve roots. (b) The central arteries are less numerous compared to cervical or lumbar levels. The few arteries mainly branch in a vertical direction but they do not form inner longitudinal anastomoses. Instead, anastomoses between central artery branches and the superficial pial plexus can be observed (arrow) (see Sect. 2.7). (c) Posterior radicular arteries (arrowheads) reinforce a rope-ladder-like system of tracts. The longitudinal components may be situated in posterior or posterolateral position (small arrows). Both components, the vertical and the horizontal, distribute blood within the posterior pial network of lower degree (Reproduced from Thron 1988)

Fig. 2.45

Superficial and intrinsic arteries of the thoracic spinal cord on an X-ray of the injected specimen and at different levels of the thoracic spinal cord on axial microangiograms. Extension of the centrifugal and the centripetal supply system depending on grey/white matter relationship. (a) X-ray film of the injected specimen in a.p. view. (b–d) Axial sections from the thoracic levels indicated in (a). In between the enlargements the posterior tracts often match the anterior spinal artery in size. Supply of the fibre tracts through the superficial pial network gains increasing importance. The decreasing numbers and calibres of central arteries in the upper and mid-thoracic spinal cord correspond to the decreasing proportion of grey matter on the cross-sectional area in this region area (a Reproduced from Thron 1988)

Fig. 2.46

Course and vertical branching pattern of central arteries in the upper thoracic region. (a–c) Microangiograms of mid-sagittal sections extending from C8 to T5 in the same specimen. Narrow anterior spinal artery. Only few central arteries ascend steeply in the anterior fissure. They run parallel to the anterior spinal artery as a pial subsystem before they bend horizontally and give off branches to the central grey matter. During this course a significant contribution to the anterior pial network (vasocorona) is obvious, especially in this imaging plane

Fig. 2.47

Anterior spinal artery and distribution of central arteries in a specimen at mid-thoracic levels. (a) X-ray of the specimen and localization of the parts shown in (b–d). The great anterior radiculomedullary artery is joining the anterior trunk at T11. Its ascending branch is very thin. (b–d) Microangiograms of mid-sagittal sections extending from T5 to T7/8 in the same specimen. Each specimen part measures 2.5 cm in length and exhibits only four to eight central arteries (artificial interruptions of the anterior spinal artery in parts of (b and d). The central arteries ascend steeply in the anterior fissure, run parallel to the anterior spinal artery as a pial subsystem before they bend horizontally and give off branches to the central grey matter. During this course an additional significant contribution to the anterior pial network (vasocorona) is obvious in this imaging plane (c, d Reproduced from Thron 1988)

Fig. 2.48

"Duplication" (non-fusion) of the anterior spinal artery at T7–T8 level of a spinal cord. (a) X-ray in a.p. view. Entry of the great anterior radiculomedullary artery at T10 (large arrow) and of a posterior feeder at T11 (small arrow). Duplication is shown at T7/8 (small arrowheads), which is unusual at this location. (b) Microangiogram of the mid-sagittal section indicated in (a). Few but strong central arteries originate from the ascending branch of the anterior spinal artery above T10 and ramify vertically. (c) Bilateral anterior arterial channels each of which gives off the central arteries to the corresponding hemi-cord (arrowheads). They issue long branches in vertical direction (section length 2.0–2.5 cm) (b, c Reproduced from Thron 1988)

Fig. 2.49

Central artery courses at T6 in sagittal plane and at the entry of a radiculomedullary artery at T4. (a) X-ray of an injected thoracic spinal cord in a.p. view. (b) Microangiogram of an oblique section cut from the anterior midline to the surface posterolateral right. It roughly follows the ascending oblique course of a centro-dorsolateral anastomosis (vertical arrows in a and b). From the hairpin curve of the anterior spinal artery a steeply ascending central artery (short thick arrow) arises, running parallel to the ascending branch of the anterior spinal artery. Not only central artery branches arise from this stem but also strong superficial pial branches, running parallel to the anterior longitudinal tract. (c) Other central arteries may also arise from this secondary pial system, which can easily be seen on the mid-sagittal section of c (arrow). This is illustrated in the schematic drawing of Fig. 2.17 showing two or three central arteries arising from a common stem (Reproduced from Thron 1988)

Fig. 2.50

Anterolateral extradural spinal tumour (metastasis) at the T3–T4 level. (a) X-ray film of the contrast-filled spinal cord. At the upper extension of the tumour, which coincides with the upper margin of section (b), there is a narrow segment of the anterior spinal artery (diameter 100–200 μm). The posterolateral spinal artery on the side of the tumour is considerably dilated (300 μm) and receives blood from the anterior arterial axis from above. (b) Mid-sagittal microangiogram at the level of the upper tumour extension. Narrow anterior spinal artery (arrowhead). Interconnections between central arteries at the entrance into the anterior median fissure are very pronounced (arrows). (c) Axial microangiogram of the tumour and the highly deformed spinal cord. Histology revealed only demyelinization of the posterior columns, probably as a result of venous congestion (Reproduced from Thron 1988)

## 2.10 Specific Patterns of Arterial Supply in the Thoracolumbar Spinal Cord and Cauda Equina

One of the ventral feeders between T9 and L1 (exceptionally at L2 or L3) is distinctly dominant in calibre (800–1000 μm) and was therefore called the "artery of the lumbar enlargement" (Lazorthes) or the "great radicular artery" (Adamkiewicz). In 73 % of all cases it enters from the left side with its origin between T9 and 12 in 62 %, lower in the lumbar region in 26 % or higher between T6 and T8 in 12 % (Jellinger 1966a).

Additional significant ventral feeders are unusual below its level of entrance.

The average number of anterior radiculomedullary arteries to the lumbosacral medulla is 0–1 (Jellinger 1966a).

The predominant role of this great (anterior) radiculomedullary artery in supplying the thoracolumbar enlargement and the calibre and course of the anterior spinal artery, often deviating in a zigzag from the midline, are apparent in all the illustrations of this region. Complete filling of the low thoracic and lumbosacral spinal cord was easily achieved for almost all injections into this vessel, irrespective of whether the entrance level of this artery was located between T9 and T12, exceptionally high between T6 and T8, or low at L1 to L3 (Figs. 2.11, 2.14, 2.15, 2.16, 2.51, and 2.52).

Supply to the posterior system in this region often includes two almost equally large dorsal feeders (400–500 μm), which enter higher or lower than the great radiculomedullary artery (Figs. 2.8, 2.11, 2.51, and 2.52).

The existence of a great posterior radiculomedullary artery, corresponding to the anterior one and possessing a distinctly greater calibre than the other posterior radiculomedullary arteries, is affirmed by a few authors (Gillilan 1958; Lazorthes et al. 1958; Jellinger 1966a), but rejected by others (Corbin 1961; Piscol 1972). We found an especially large posterior radiculomedullary artery on only one side as an unusual observation.

The number of dorsal radiculomedullary arteries is reported with an average of 8 (Piscol 1972) to an average of 9–12 (Jellinger 1966a) for the total thoracolumbar region. No lateral preference is observed; the vessel calibres lie between 0.15–0.4 mm.

Posterior radiculomedullary arteries to the thoracolumbar region show a differently configured hairpin course compared to the anterior vessels and branch into ascending and descending vessels of mostly different calibre.

The transverse network is formed by external anastomoses between the anterior tract and the posterolateral spinal arteries yet even more by the intercommunication between them and the so-called posterior spinal arteries (Figs. 2.55 and 2.56). According to the description given by Piscol (1972), the tract of the posterolateral spinal arteries that runs in the "axilla" of the posterior roots is very constant in the lower half of the spinal cord. Its location and calibre in comparison to the posterior spinal arteries running medially and dorsally of the posterior roots can be easily recognized in the microradiographic reproductions of Figs. 2.13, 2.14, 2.15, 2.16, and 2.18. The numerous intercommunications of equal calibre produce a rope-ladder-like system.

The posterolateral longitudinal tracts clearly dominate above the posterior side of the lumbar enlargement, but they are only the largest components in a longitudinally oriented network that already becomes more irregular and fragmentary in the lower thoracic region.

The ventral and dorsal systems are connected to each other around the conus (arcade of the cone, rami anastomotici arcuati) (Kadyi 1889). This pattern may constitute a significant anastomosis, comparable to the circle of Willis (Fig. 2.31). It was seen in the vast majority of specimens, but with variable calibres and not necessarily at the same level on both sides (Figs. 2.14 and 2.16). Simultaneous filling of the posterolateral and posterior longitudinal tracts in the lumbar region occurred with regularity if the great anterior radiculomedullary artery was injected. Vice versa, filling of the anterior spinal artery was easily possible by injecting one of the neighbouring posterior radiculomedullary arteries. The filling was achieved primarily via these rami cruciantes (Adamkiewicz 1882), laterally surrounding the cone. These interconnecting vessels lie concealed between the sacral roots, but can be demonstrated well radiographically. They are usually of considerable calibre. Anastomotic function and supply of the cauda fibres might explain why the descending branch of the anterior spinal artery, but also that of the posterolateral tracts, maintains such a large calibre until the end of the conus even at low entrance (Figs. 2.52 and 2.60a).

The straight continuation of the anterior spinal artery to the filum terminale is an insignificant branch (Figs. 2.51b, c and 2.52c, d). The small arteries running with the fibres of the cauda equine (Fig. 2.54) are derived from the pial plexus (Fig. 2.11). Both crura of the conus arcade are usually relatively symmetrical, but at least one of both connecting branches may be missing (Fig. 2.51b, c).

The effective anastomotic function of this circle might also explain the difficulty in demonstrating different areas of supply in our specimen in this region. Injecting the solution of contrast medium in either anterior or posterior radiculomedullary arteries of the lumbar enlargement always resulted in immediate filling of the entire superficial longitudinal tracts and, furthermore, of the small arteries running with the fibres of the cauda equine.

Fig. 2.51

Frequent constellations in arterial supply of the lower third of the spinal cord. Selected examples of contrast-injected spinal cords, demonstrated on X-ray images in a.p. view. (a) Classical constellation: entry of the A. radicularis magna at the T11 level on the left. Bilaterally well-developed posterior radiculomedullary feeders at high lumbar levels and bilaterally well-constituted anastomotic circles around the cone. (b) Equally large-sized anterior feeders entering at the levels T10 and T12. Anterior spinal artery with a straight course. Asymmetrically formed anastomotic circle on the left and distinct artery of the filum terminale. (c) A radicularis magna entering at T10 level on the left side with convoluted course of the anterior spinal artery and an asymmetrical development of the anastomotic circle around the cone. (d) Similar to (a) with a very symmetrical supply situation, stronger posterior tracts, but only small-sized anastomotic arterial basket around the cone (a Reproduced from Thron 1988)

Fig. 2.52

Variability of supply conditions in individual specimens. High or low entry of the artery of the lumbar enlargement, variable patterns of supply between anterior and posterior superficial systems and variable developments of anastomotic circles around the cone. X-ray films of specimens in a.p.view. (a) High entry of the great anterior radicular artery at the T9 level. Well developed posterolateral arterial tracts but only sparse anastomotic circles around the cone. (b) High entry of the artery of the thoracolumbar enlargement. The ascending branch to form a part of the anterior spinal artery is extremely narrow. Medium-sized posterolateral tracts including symmetrical arcades around the cone. (c) Low entry of the artery of Adamkiewicz at the L2 level. Narrow ascending branch and anterior spinal artery up to the T7 level. Compensating strong posterolateral tracts. Incomplete unilateral "anastomotic basket" at the cone. (d) "Textbook example" with average findings in every respect including the artery of the filum terminale

Fig. 2.53

Axial microangiograms at a thoracic and a lumbar level for comparison. (a) X-ray in a.p. view. The dotted lines indicate the position of the axial sections. (b) Thoracic region. The position of the posterolateral (arrows) and the posterior longitudinal tracts (arrowheads) in relation to the posterior root is clearly shown. The two central arteries included in this section have remarkably different calibres. Filling of intrinsic vessels in the posterior third is poor. (c) Lumbar region. Transverse interconnection between the posterior longitudinal tracts on the right side (sharp arrow). In this slice of 3 mm thickness 4 central arteries of different size are included, reflecting the high vascular density (c Reproduced from Thron 1988)

Fig. 2.54

Arteries of the thoracolumbar enlargement. (a) X-ray film of the injected specimen in a.p. view. The supply pattern and the calibre relations of anterior and posterior radiculomedullary feeders are not uncommon. Well-formed anastomotic circles around the cone bilaterally. Posterior longitudinal trunks of almost equal size. (b) Lumbar level as indicated in (a). The equal filling of the superficial and deep arteries is rarely achieved in post-mortem studies. (c) Lower thoracic level as indicated in (a). Strong posterior tracts exist only on the right side. The difference in the density of arteries within grey and white matter is impressive. (d) Poor filling of superficial and intrinsic arteries especially in the territory of the posterior systems (c Reproduced from Thron 2002)

Fig. 2.55

Arteries of the thoracolumbar spinal cord. (a) X-ray film of the injected specimen in a.p. view. The levels chosen for the coronal sections in (b and c) are marked by vertical arrows. (b) Microangiograms of four contiguous coronal sections in the middle of the lumbar enlargement. Arrangement and distribution of the superficial (S1and S4) and intrinsic spinal cord arteries (S2 and S3) at this level demonstrate the extremely dense vascularization of this region. (c) Microangiograms of four contiguous coronal sections cranial to the lumbar enlargement, above the entry of the great radiculomedullary artery. A more loosely meshed superficial arterial network is obvious, the number of central arteries is far smaller and their ramification mainly occurs in a vertical direction (Reproduced from Thron 1988)

Fig. 2.56

Arteries of the lumbosacral spinal cord. (a–c) Frontal microangiograms (S1, S2, S3) in vertical reconstruction images. The arteries of the anterior and posterior surface as well as the intrinsic vessels (S2) can be seen without superimposition of each other. The longitudinal arterial trunks on the posterior surface (S3) form a rope-ladder-like network, in which the posterolateral arteries dominate in size (Reproduced from Thron 1988)

Fig. 2.57

Configuration of central arteries at the hairpin curve of radiculomedullary arteries at thoracolumbar levels. (a) X-ray film in a.p. view with significant radiculomedullary feeders at thoracic and lumbar levels. (b) Microangiogram of an oblique antero-posterior section at high thoracic level. A single very elongated central artery ascends parallel to the ascending branch of the anterior spinal artery. There are longitudinal interconnections between pial arteries at the entrance into the anterior fissure, but not between the central artery branches. A transverse anastomosis between a central artey branch and the superficial system is dissected (compare Fig. 2.32) (c) Microangiogram of an anterior frontal section at the entry of the great anterior radiculomedullary artery. Division of these large feeders into an ascending and descending branch most often takes place lateral from the midline. A series of steeply ascending central arteries covers the gap of supply before the anterior anastomotic tract returns to the midline (arrows) (Reproduced from Thron 1988)

Fig. 2.58

Arteries of the lumbosacral spinal cord. (a) X-ray of the injected specimen in a.p. view. Small damaged area on the right side near the cone. Complete filling of superficial and intrinsic arteries. (b) Microangiogram of a mid-sagittal section at the level of entrance of the great anterior radiculomedullary artery as indicated in (a). Cranial of the hairpin curve, the number and calibre of central arteries decreases abruptly. (c–e) Microangiograms of the mid-sagittal section (d) and the two lateral parts of the cone. The anastomotic tracts, also known as "rami cruciantes", connect the anterior spinal artery with the posterior longitudinal system. In this specimen they are well developed at both sides. The branch to the filum terminale is small (Reproduced from Thron 1988)

Fig. 2.59

Vascularisation pattern of central and anterior peripheral arteries in the thoracolumbar enlargement. Mid-sagittal microangiograms from a sacral level (a) to a lower thoracic level (c). The great anterior radicular artery is entering high, cranially of these sections. This might explain the continuously strong calibre of the anterior spinal artery. Horizontal or slightly descending course of central arteries, some of them showing short common stems (arrows in (a and b). In some cases in the thoracic region long superficial interconnections exist between two central arteries (arrows in c)

Fig. 2.60

Microangiograms of mid-sagittal sections at lumbosacral levels demonstrating the variability of central artery courses. (a) Exceptionally low entrance of the great anterior radiculomedullary artery at the L3 level (large arrow; specimen shown in Fig. 2.9b). Ascending steeply from the hairpin curve, several central arteries have a long common stem running parallel to the anterior spinal tract before dividing into two or more central arteries (small arrows). This finding is more common in the thoracic cord and is therefore included in the schematic drawings of Figs. 2.17 and 2.49. (b) Elongated and dilated arteries with a tortuous course in a patient of about 80 years of age (Reproduced from Thron 1988)

## 2.11 Anatomical and Haemodynamical Aspects of Arterial Supply

### 2.11.1 Anastomotic Capacity of Longitudinal Trunks and Distribution of Supplying Arteries

In comparing the radiographic anatomy presented here with earlier anatomical investigations and later studies, it can be appropriately remarked that inaccuracies and dubious clinical conclusions could have been avoided had the careful, minutely conducted study by Kadyi from 1889 received more attention, rather than just being quoted. One of the main reasons for divergent and discrepant descriptions of spinal vascular anatomy is certainly the gross regional and interindividual variability of vascular conditions . Unless all spinal cord segments are studied in as many specimens as possible, the observed findings can differ considerably. This is why we tried to present the large variability of supply patterns in this book.

If one compares surveys and monographs, which statistically evaluate a large number of specimens (Lazorthes, 1958; Corbin 1961; Jellinger 1966a; Piscol 1972; Dommisse 1975; Tveten 1976b), no essential discrepancies in the number of anterior and posterior radicular feeders are found. Also the distinction between a paucisegmental type with 2–5 ventral feeders per cord in approx. 45 % of specimens and a plurisegmental type supplied by 6–14 anterior radicular arteries in approx. 55 % (Kadyi 1889; Jellinger 1966a; Piscol 1972) shows largely conforming results. To a certain extent, this also applies to the segmental distribution of radicular feeders in percent of cases, which shows no great deviations comparing the evaluations by Piscol (1972) or Domisse (1975) with those by Jellinger (1966a), who derived his results from several hundred spinal cords. From this it can be deduced that both the regions C5 to C8 and T9 to L2 show an increased incidence of medullary feeders and, at the same time, almost all larger vessels join the spinal cord in these regions (Piscol 1972). These conclusions are important for a basic understanding of spinal cord blood supply, though not applicable in each individual case (Domisse, 1975). The medullary segments with a high incidence of large tributaries correspond to the cervical or thoracolumbar enlargement, respectively, i.e. the regions with the greatest accumulation of nerve cells. Analogous to the large-calibre radicular feeders, the anterior spinal artery, which is viewed as their anastomotic connection on the surface of the cord, also has its greatest diameter in these regions. These areas contrast with the thoracic region, which is supplied by fewer, mainly smaller arteries, and whose anterior anastomotic tract can show an accordingly weak development. Main functional zones of medullary supply were deduced from these conditions.

Thus, Lazorthes (1958 to 1962) and Domisse (1975) differentiate three territories, yet with differing boundaries. Their division roughly separates the cervical region from the thoracolumbar enlargement and from a thoracic intermediate zone. Other authors distinguish between two regions: an oral, cervicodorsal (supplied by subclavian artery branches) and a caudal, thoracolumbar region (supplied by aortic segmental arteries), which they further subdivide into sections with a low or high incidence of feeders (Corbin 1961; Jellinger 1966a). Piscol (1972) distinguishes between four territories that result from segmental distribution curves of anterior radicular arteries and various proportions of very small to large arteries (vessel categories I–IV). From this he defines zones of characteristic supply situations in respect to the total blood supply of the spinal cord, namely:

  * Obligatory vasoafference regions: the regions C5 to C8 and T9 to L2 with the radicular arteries relevant for the enlargements and the entire myelon.

  * Facultative vasoafference regions: the regions C3 to C4 and T4 to T6 with radicular arteries in varying number and size, and consequently a modifying effect on the total supply.

  * Vasodeficiency regions: the segments T1 to T3 and L3 to the caudal end without relevant feeders.

  * Variable vasoafference region: C1/C2, which always receives feeders from the vertebral arteries, but has a very inconsistent contribution to the total supply.

This short summary of the statistical extramedullary supply situation is indispensable as a basis for the very controversial discussions on sufficiency or regional insufficiency of arterial spinal vascular supply, and on the importance of the anterior spinal artery as a ventral arterial anastomotic trunk.

The calibre of the anterior spinal artery and of its radicular tributaries is approximately proportionate to the volume of grey matter. Very few authors have referred to this fact, yet it is emphasized here in agreement with Gillilan (1958). She stated, "The blood supply to the thoracic spinal cord is entirely adequate for the volume of grey matter present and it is relatively as good as for any other cord segment".

The reduced density of central arteries in the thoracic region correlates on the one hand with the greater longitudinal magnitude of the thoracic segments (Kadyi 1889; Corbin 1961). On the other hand, it corresponds to the decreasing proportion of grey matter here, down to one-sixth of the sectional area according to our measurements (compared with approx. 1/2 to 1/3 in the lumbar and cervical region). Furthermore, there is a corresponding absolute reduction of the total cross-sectional area (Fig. 2.30). If the number of central arteries is seen in relation to the varying lengths of myelon segments rather than to centimetre lengths of myelon, not much less than the normal incidence of 6–7 central arteries per segment results for the thoracic region as well (Clemens 1966).

On the other hand, selective injections into single radicular arteries showed that in most cases the entire spinal cord arteries cannot be filled by this procedure (Adamkiewicz 1882; Bolton 1939; Suh and Alexander 1939; Noeske 1958; Roll 1958; Corbin 1961; Lazorthes et al. 1962), since the anterior longitudinal anastomosis can narrow noticeably or even be interrupted at different locations. This supports the concept of circulatory partial systems (Adamkiewicz 1882; Piscol 1972). Concerning the anastomotic capacity of the anterior median trunk it means that this vessel may be an insufficient anastomosis for highly perfused distant regions, at least as far as acute demands are concerned.

But this situation is not restricted to the upper thoracic cord. It also exists in the upper cervical region according to our observations that agree with the findings of Corbin (1961), Lazorthes et al. (1971) and Piscol (1972) and with animal in vivo studies by Fried et al. (1970). The descending feeders from the vertebral arteries (homologous to the descending branches of an anterior radicular artery at C0/C1 level) may not only run as bilateral vessels over several segments but may also fail to unite with the median longitudinal trunk. This is just one of many variations for a territory whose vascularization often corresponds to the more primitive embryonic pattern of a plexus-like anastomosis (Figs. 2.35 and 2.36). Therefore, the potential anastomotic capacity of the anterior arterial axis may be as insufficient above the cervical enlargement as it may be in segments of the thoracic cord.

According to concurring reports, the second area with facultative narrow segments of the anterior spinal artery is the mid to upper thoracic region, i.e. the region between the entrance of the great radicular artery and of the largest, cervical anterior radicular artery. Here, we measured calibres as low as 0.2–0.1 mm, corresponding to those of the central arteries, which is in agreement with other investigators (Romanes 1965; Jellinger 1966a). Even interruptions were sporadically observed (Corbin 1961; Hassler 1966). But there are no set rules for the appearance of small-calibre segments in the thoracic region. Rather, it depends solely on individual distribution patterns.

If one accepts the existence of circulatory partial systems in the spinal cord, as conceived by Adamkiewicz, experimentally substantiated by Piscol (1972), and in agreement with spinal angiographical experience, it follows that the anterior spinal artery as an anastomotic trunk has segments with very good anastomotic capacities, but others with poorer anastomotic capacities in regard to the more distant circulatory partial systems of the spinal cord.

According to our findings, the calibre, arrangement and distribution of the posterolateral and posterior spinal arteries indicate that they merely represent the largest, longitudinally oriented components of the posterior part of the anastomotic pial network. Gillilan (1958) reaches the same conclusion, but does not place special emphasis on these vessels pursuing constant courses over quite a distance. Microradiographs show that these anastomotic trunks have less to do with the direct supply of certain medullary structures. Instead, they serve to distribute a constant blood supply in the dorsal part of the vasocorona. Evidence for this fact is that the dorsal longitudinal anastomoses cannot only complement each other by varying calibre, but also completely replace one another in certain segments. This is one reason for conflicting opinions on their location. However, it must be noted that the dorsolateral trunk is normally more constant and has greater calibre. A pial arterial network mediates between the longitudinal trunks and the vessels that directly enter the spinal cord. Visualization of the perforating arteries was not obtained by filling the longitudinal anastomoses alone, but only by additionally filling this superficial plexus. Although the pial plexus, fed by the anterior spinal artery and the posterior longitudinal anastomoses, is extremely dense over the enlargements, the parts of the vasocorona filled from ventral or dorsal are largely independent of each other in post-mortem injections.

The pattern of arterial supply to the spinal cord, via a system of longitudinal anastomoses reinforced from various segmental levels, protects the neural tissue against ischemia. Primarily the conus arcade constitutes an anastomotic function comparable to that of the cerebral circle of Willis. The additional pial and intramedullary anastomoses may only be important for slower circulatory adjustments, since their calibres are inadequate for a sudden intake of larger volumes of blood. Other intramedullary anastomoses, e.g. longitudinally and/or transversely between the central arteries, as postulated at the arteriolar level by Adamkiewicz (1881), Suh and Alexander (1939) and Fazio and Agnoli (1970), were not detectable in our specimens.

The number, distribution and branching pattern of the central arteries should no longer be a matter of dispute since Kadyi (1889) recognized them as essentially unilateral arteries occasionally branching from a short common stem. Hassler (1966) observed by microradiographs that bifurcation of a short common trunk takes place in the vertical plane. This was corroborated in our material (Figs. 2.59 and 2.60a). Noteworthy is the observation also mentioned by Hassler (1966) that very elongated, tortuous courses of the central arteries can be observed in some specimens, especially in the lumbosacral region (Fig. 2.60b). Their possible pathological or age-dependent significance, however, remains to be clarified by corresponding histological studies. Alterations in the vessel walls or luminal narrowing, as seen in cases of arteriosclerosis, was not observed in any of our specimens.

Considering the practical experience with spinal angiography, doubts as to the validity of the "partial flow theory" (Adamkiewicz 1882) are no longer reasonable. Variability in vessel calibre of the ascending and descending branches of the anterior radicular arteries, however, demonstrates that the haemodynamics of these circulatory partial systems cannot be strictly classified, and that the proportions of blood running cranially or caudally vary.

Suh and Alexander (1939) and later Zuelch (1954; Zülch 1976) postulated their traditional hypothesis of a watershed zone of increased ischemic vulnerability near T4. This model was based on the relative hypovascularity of this region.

Cheshire et al. (1996) described 44 patients with spinal cord infarctions. Surprisingly, the mean sensory level of the deficits was observed at T8 and T9 in cases of global ischemia. A review of the clinical literature by Cheshire and colleagues (1996) suggested that the most commonly sensory level found after spinal cord infarction is centred at T12.

We avoided using terms such as "vulnerable zone" or "undersupplied zone" in respect to the "poor supply" of the upper thoracic region. Such designations can be traced back to Adamkiewicz (1882). Kadyi (1889) subsequently rejected them with good reasons, but Suh and Alexander adopted them again in 1939. These terms were particularly revaluated and extended in the 1950s by Zülch's introduction of a marginal zone hypothesis (Zülch 1954, 1976). Numerical disputes were the result, and the participating authors declared almost every thoracic segment and many of the cervical ones to be marginal zones or areas particularly vulnerable to impaired blood flow. Since spinal vascular supply has been clarified better by following studies, this hypothesis need not be discussed in detail. Stochdorph (1961) criticized its fundaments with good reasons and it never found definite, pathoanatomical proof (Jellinger 1966a, b). This is discussed thoroughly in Schneider's study and review (1980).

Our investigation also shows that no vascular anatomical evidence supports the assumption of undersupplied areas. Differences in calibre of the anterior spinal artery as well as varying calibre and number of anterior radicular feeders depend on locally variable blood requirements especially of the grey matter. The only potential limit of anastomotic capacity is a small-calibre segment or interruption in the anterior spinal artery. This can be regarded as the cause of spinal complications in aortic surgery and also in dissecting aortic aneurysms (Hogan and Romanul 1966). Operative complications only occur—according to Adams and Geertruyden (1956)—if the great radicular artery entering in the lower thoracic region is ligated upon serial elimination of the intercostal arteries and if there is simultaneous, temporary occlusion of the aorta below the subclavian artery. Then, the possible occurrence of medullary ischemia signals insufficient anastomotic capacity of the anterior spinal artery with its sole remaining cervical supply. Nevertheless, ischemia affects only the lower cord in these cases. On the other hand, the anterior spinal artery can even function as a collateral of the basilar artery, as shown in cases of occlusion of both vertebral arteries. Furthermore, occlusion of the anterior spinal artery without ensuing effects in cases of arteriovenous malformation (AVM) treatment is not an unusual observation (Decker et al. 1975; Riché et al. 1983). But this is not really comparable with an exclusively spinal cord–supplying anterior spinal artery occluded over a critical distance.

As a rule, the numerous extra- and intraspinal anastomoses guarantee collateral supply in the presence of extravertebral occlusion. According to animal experiments on rhesus monkeys (Fried and Aparicio 1973) this also applies to ligature of the great radicular artery, unless its descending branch is directly ligated. Experimental findings by Shimomura et al. (1968) show that only occlusion of the anterior spinal artery extending over 1–2 segments leads to ischemia. This correlates fairly well to the pial longitudinal connections, which we could demonstrate between several central arteries at the anterior fissure parallel to the anterior spinal artery (Figs. 2.17, 2.46, 2.49, 2.50, and 2.60a). They are frequent in the thoracic region, but not in the cervical or lumbar enlargements.

Deficits in the rare cases with proven occlusion of the anterior spinal artery (Garland et al. 1966) vary considerably. Only a part of these showed the expected lesions of the ventral two-thirds of the transverse sectional surface (Schneider 1980). This accords with the general principle that development of an infarct becomes more probable the more distal a vessel is obstructed. Collaterals may not compensate for embolic occlusion of a central artery, but obstruction of a single artery will probably lack functional consequences owing to an overlapping of neighbouring regions.

Piscol (1972) stressed the fact that a paucisegmental arterial supply may function well in situations demanding rapid anastomotic compensation, but can be deficient in haemodynamical crises. This explains the verified necroses of the anterior horn in the enlargements at autopsy following circulatory arrest, which are consequently the most vulnerable structures.

Displacement even of the central arteries by ventral-compressing masses (Ramsay and Doppman 1973) does not lead to early ischemia, since they have some room within the anterior fissure (Fig. 2.42). The experimental studies by Doppman and Girton (1976) on the effects of intraspinal masses support the opinion voiced by a neuropathologist (Schneider 1980) that disorders in microcirculation play the decisive role in the genesis of medullary vascular lesions.

### 2.11.2 Spinal Cord Ischemia and Infarct

Compared with brain ischemia, spinal cord strokes are caused by more diverse etiologies. Up to now there is no satisfactory and accepted classification of spinal infarcts. Etiologies include circulatory arterial and venous disorders (Thron et al. 1987; Mull and Thron 2006). From a clinical and pathoanatomical point of view it seems reasonable to differentiate between acute ischemic myelomalacia and subacute to chronic vascular myelopathy. In most cases MRI enables the differentiation of these two main etiologies. A deficient spinal arterial blood flow generally has various causes, ranging from the occlusion of intercostal or lumbar arteries to affection of the intrinsic arteries of the spinal cord.

Many causes of acute spinal cord infarction (of arterial and venous origin) have been reported. They include diseases of the aorta and aortic surgery, thromboembolic events and cartilaginous disc embolism, vasculitis, coagulopathy, radiation-induced vasculopathy, toxic effects of contrast medium, epidural anaesthesia, periradicular nerve root therapy with crystalline corticoids (Dafotakis et al. 2008), decompression illness, shock or cardiac arrest, lumbar artery compression and other etiologies (Schneider 1980).

Cartilaginous disc embolism is meanwhile a widely accepted cause of acute spinal cord ischemia mainly on the basis of post-mortem findings (Pfeiffer et al. 1976; Mikulis et al. 1992; Toro et al. 1994). Most reported post-mortem cases are cervical, but conus medullaris infarctions are also reported. The exact mechanism of disc embolism remains unclear and speculative. An increased intraosseous pressure within the vertebral body as a result of acute vertical disc herniations—often after axial trauma—may explain the initial step in a process, which ends up in spinal cord ischemia (Tosi et al. 1996). In the clinical course of the histologically established cases of fibrocartilaginous embolism three main characteristics could be identified: (1) the sudden severe pain at onset, (2) the free interval of neurological signs and symptoms ("spinal stroke in progress"), (3) no improvement of the neurological deficit. In our experience, there is a surprisingly high rate of disc herniations in close proximity to the vascular lesions of the cord (Mull et al. 1992).

Lumbar artery compression by the diaphragmatic crus has been described as a new aetiology for spinal cord ischemia (Rogopoulos et al. 2000). A prolonged hyperlordotic position may play a predisposing role in this new syndrome. The first right and left and the second right lumbar arteries course through an osteotendinous passage between the vertebral body and the diaphragmatic crus. If spinal cord–supplying arteries arise at the level of the first and second lumbar artery, compromise of the spinal cord arterial supply can result in spinal cord ischemia, especially if lordotic positions reduce the space within the vertebral canal and intervertebral foramen.

We had a young patient who could provoke weakness in both legs by performing press-ups in a hyperlordotic position. One day, repeating this exercise he experienced definite paraparesis. Spinal angiography revealed an origin of the great anterior radicular artery from the L2 level.

Additional information on acute spinal cord ischemia can be obtained from special literature on this subject (Mull et al. 1992, Mull and Thron 2006).

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© Springer International Publishing 2016

Armin K. ThronVascular Anatomy of the Spinal Cord10.1007/978-3-319-27440-9_3

# 3. Venous Drainage

Armin K. Thron1

(1)

Aachen, Germany

The pattern of venous drainage substantially deviates from that of the arteries (Figs. 3.1 and 3.2). It will be described in the direction of venous drainage from the spinal cord parenchyma to the epidural plexuses.

Fig. 3.1

Diagram of superficial veins, large anastomotic midline connections and intrinsic veins. Radially oriented peripheral (and central) veins within the spinal cord parenchyma are connected to a pial venous network of lower degree. Superficial pial tracts of drainage, the large longitudinal venous tracts, typically, but not exclusively in a midline position, collect the blood. The inconstantly developed superficial midline veins may be supplemented or replaced over some distance by superficial venous trunks in an antero- or posterolateral position. They merge with anterior or posterior radiculomedullary veins (r.m.v.) at different levels

Fig. 3.2

Course and distribution of intrinsic veins in axial and sagittal planes. The characteristic features of the system are radially symmetric, largely horizontally oriented veins of the peripheral system with different depths of penetration. Central veins play a minor role. Different transparenchymal anastomotic channels in an anteroposterior (a.p.) or centro-posterolateral direction (on top of the diagram) are outlined

Four compartments, representing four different levels of intercommunicating drainage from the spinal cord and from the spine, can be discerned:

  * The intrinsic veins of the spinal cord parenchyma.

  * The superficial pial system covering the surface of the cord, comprising a network of small collecting veins. It is complemented by large, longitudinally oriented channels carrying the blood to the dural border of the thecal sac. Additionally, numerous intra- and extramedullary anastomotic connections between all components guarantee flexible blood flow deviation.

  * The extradural but intraspinal internal venous vertebral plexus.

  * The extradural and extraspinal venous vertebral plexus communicating with the azygos and cava system.

Technical Remarks

In comparison to the spinal arteries, the variability of the draining venous system is even greater. Due to a restricted number of specimens (Table 1.1 and Sect. 1.3), the presented images in this chapter should be considered rather as illustrative examples than as statistically confimed results. For the veins, we re-evaluated the radicular drainage, which is easier on the opened vertebral canal in situ (Jacobs 1996). Concerning the intramedullary system of veins importance was attached to the most complete venous filling possible for large medullary segments, which requires even better preserved specimens and much practical experience to avoid extravasations. Filling defects in some of the specimens are probably a result of intraluminal coagulation. On the other hand, a loss of contrast medium from large superficial vessels upon sectioning must be expected. In certain illustrative microangiograms the empty lumen of a large superficial vessel was therefore marked with "ev" (empty vessel).

## 3.1 Intrinsic Veins

Radial symmetry and dominance of intrinsic peripheral veins is evident in many parts of the spinal cord (Figs. 3.1, 3.3, 3.6, and 3.23). Mainly in the lower thoracolumbar cord, including the conus medullaris, do veins of the anterior fissure play an accentuated role and may display vessel diameters of up to 0.3 mm (Figs. 3.4, 3.29, and 3.31).

Therefore it seems justified to maintain the differentiation of

  * central veins and

  * peripheral veins

similar to the classification of the arterial system.

However, compared with arterial supply, an essentially different orientation of intrinsic drainage paths is obvious. Generally, intrinsic veins running along with arteries (venae comitantes) only occur along the proximal stem of the central arteries.

Peripheral veins tend to take a separate course, starting deep in the grey matter. In comparison with the numerous perforating branches of the arterial pial network, the radial veins are fewer in number but exhibit larger calibres. Their territory of drainage covers not only the outer rim of the fibre tracts. They also collect blood from the central grey matter area (Figs. 3.3, 3.15, and 3.25). Therefore their calibre equals or exceeds that of central veins (Figs. 3.4 and 3.26), at least in the cervical and thoracic regions (Kadyi 1889).

This basic radial drainage pattern becomes evident in axial as well as sagittal and frontal sections from most specimens of these regions (Figs. 3.4, 3.5, 3.6, 3.7, and 3.8). In the higher medullary segments, central veins may be more numerous, but more often they are of smaller calibre than the corresponding arteries. If veins of large calibre are observed in the anterior fissure at greater intervals, they are usually the anterior part of an anastomosis of large calibre to the dorsal or dorsolateral surface (Figs. 3.16, 3.17, 3.18, and 3.25; Sect. 3.3). Tortuous central veins that drain the white commissure and anterior central parts of the grey matter often join to a common stem deep in the anterior fissure. A common trunk is at least more frequent than for the arteries (Figs. 3.28, 3.29, and 3.30). Longitudinal anastomoses of central veins occur only at the entrance into the fissure, that is, directly under the main anterior median vein (Fig. 3.30b).

Small peripheral veins (so-called marginal branches) that originate in the white matter take a short course to the surface of the spinal cord. Other peripheral veins with diameters of 0.1 mm to more than 0.2 mm are larger and longer than the perforating arteries of the vasocorona and extend deep into the grey matter. They are morphologically equivalent to the central veins. This is clearly indicated not only by their almost equal calibres but also by the frequent anastomotic connections between both of them (Figs. 3.16, 3.20, 3.24b, and 3.26). However, this does not refer to even larger transmedullary connections between the anterior and posterior main venous trunks (Sect. 3.3).

As shown in X-rays of axial sections, a nomenclatural classification of the veins draining the medullary transverse sectional area is no less problematic than that of the perforating arteries, since an almost arbitrary number of venous trunks of approximately the same calibre can be found. Owing to the constancy of their occurrence, location in the anterior fissure and dominant calibre in the lumbosacral region, the central veins are of special importance that deserves mention. Furthermore, of the peripheral veins, only those of the posterior median septum should receive special attention because of their length (Figs. 3.3, 3.5, 3.6, and 3.8). Despite their inconsistent yet very remarkable calibres in certain sections, they were nevertheless hard to fill in our injection specimens.

Since the medullary territories drained by the central veins and the peripheral veins do not coincide with the supply regions of the central and peripheral arterial systems, an analogous classification should not falsely suggest an equal hemodynamical significance. The major impact for the drainage of the whole cross-sectional area has to be attributed to the peripheral system because the long radial vessels drain from the central grey matter and along their passage to the surface receive branches from the white matter, including veins of the posterior white columns.

All larger veins extending through the white matter into the medullary grey matter show a typical form of branching that Kadyi correctly characterized as a "compact, profusely ramified, small tree trunk" (Figs. 3.5, 3.6a, and 3.8b). By contrast, the central veins do not branch until they reach the white commissure and the central grey matter (Figs. 3.3, 3.4, and 3.29). Another difference between the intrinsic arterial and venous system with respect to the extent of the longitudinal territories is found in the thoracic region. There, larger veins may sometimes ascend obliquely, yet show no significant branching into long ascending or descending vessels (Fig. 3.27).

In summary, the intrinsic medullary drainage pattern can be characterized as a radially symmetric, largely horizontally oriented system. Mainly in the section of the thoracolumbar enlargement it exhibits a slight dominance towards the anterior or posterior midline veins yet drains mainly via radial peripheral veins and numerous oblique and transverse anastomoses almost uniformly to the surface. Not until the level of the spinal pia mater is blood accumulated in larger longitudinal trunks, of which the anterior and posterior median spinal veins are the most constant vessels with the greatest calibre.

Fig. 3.3

Characteristic features of intrinsic venous drainage. Microangiograms of axial sections from various levels of the mid and lower thoracic region. (a, b) Symmetrically oriented peripheral veins of different length drain the deep central parts of the spinal cord as well as the parts near to the surface on almost the complete cross-sectional area. (c, d) Veins of striking larger calibre running within the midline structures might be veins of the posterior septum (c, arrow) or central veins running in the anterior fissure (d, arrow). If they do not receive tributaries they might also be parts of dissected anastomotic connections between superficial (compare Fig. 3.25). The large superficial venous trunks of this specimen are in variant positions

Fig. 3.4

Comparison between peripheral and central veins at cervical (a), thoracic (b) and lumbar (c) levels. Central veins are generally less important in the pattern of venous drainage. The main part of the cross-sectional area is drained by the horizontally oriented peripheral veins (Reproduced from Thron 1988)

Fig. 3.5

Microangiograms of intrinsic and superficial veins of the cervical spinal cord (incomplete filling of small vessels in some circumscribed posterior areas of the posterior columns and septum). (a) Mediosagittal section at midcervical level. Course and ramification of the central veins anteriorly (small arrows) differ very much from that of the larger veins of the posterior septum and columns (arrowheads). Typical mediosagittal a.p. anastomosis (large arrow). Anterior and posterior longitudinal venous trunks course in midline position. (b) Mediosagittal section of the lower cervical cord. The incomplete filling of the posterior column area offers a unique image of the tree-like branching pattern of these compact, straightly coursing veins in the posterior septum (arrowheads). Numerous smaller central veins descend in the CSF-space of the anterior fissure (arrow) (a Reproduced from Thron 1988)

Fig. 3.6

Intrinsic spinal cord veins. Microangiograms at the lower cervical level. (a) Mid-sagittal section at the C7–C8 level. Only contrast remnants are visible in the anterior and posterior median spinal veins. Central veins can be identified (arrows), but they seem to be of minor importance compared to the large number of peripheral veins and strong veins of the posterior septum penetrating deeply into white and grey matter. (b) Paramedian sagittal section. The predominant role of slightly descending peripheral veins of varying size is impressively demonstrated in this image

Fig. 3.7

Microangiograms of frontal sections from the upper thoracic spinal cord C8–T3. (a) Anterior frontal section. The large median and anterolateral pial veins on the anterior surface contain only little contrast medium (arrow). The intrinsic peripheral veins are symmetrically arranged and take a horizontal or slightly oblique course in the craniocaudal direction. (b) Mid-frontal section. There are only scant central veins. Midline vessels of larger calibre are supposed to be anastomotic channels. (c) Posterior frontal section. Serpentine superficial vein (arrow) (Reproduced from Thron 1988)

Fig. 3.8

Central veins and posterior column veins at lumbosacral levels. (a) Microangiogram of a mid-sagittal section in the region near the cone, obtained following injection of stronger diluted contrast medium. Central veins occur in higher number and larger calibre at lumbosacral levels compared to other spinal cord regions. Additionally, a high density of smaller peripheral veins is obvious in the nervous tissue of the lumbar enlargement. (b) Microangiogram of a mid-sagittal section of the posterior columns and the posterior septum at low thoracic levels of the same specimen. The high density and tree-like configuration of peripheral veins in this area is clearly demonstrated

## 3.2 Superficial Veins

As demonstrated by the dorsal aspect of a spinal cord in situ (Fig. 3.13b, c) and the radiographs in Figs. 3.9, 3.14, 3.29, 3.30, 3.31, 3.32, and 3.33 a reliable systematization of the superficial venous vessels is difficult. Kadyi's anatomical drawings (Figs. 3.10 and 3.11) are a perfect compromise to explain the principle and the margins of spinal cord venous architecture. Apparently, there is again no well-defined parallelism to the superficial arteries. This impression is generated mainly by thick, convoluted venous formations on the posterior side of the spinal cord and by two longitudinally directed vessels which merge with radicular veins at different levels, and whose sections of largest calibre run medially in some segments, in some paramedially. Despite the great variety, common characteristics can be observed, and basic differences in comparison to the pattern of arterial supply can be demonstrated. Moes and Maillot (1981) have presented a very thorough study on these superficial vessels with an essay of systematization.

Two main systems can be differentiated within the pia mater:

1.

The longitudinal venous trunks (Tractus venosus medianus anterior et posterior), also called the anterior and posterior median spinal veins as the most common longitudinally directed vessels of the spinal cord. Anterolateral and posterolateral venous tracts partially replace the median trunks at least for short distances.

2.

The pial venous networks of lower degree collecting blood from the intrinsic peripheral and less important central veins.

### 3.2.1 Longitudinal Venous Trunks

The anterior median vein receives the draining vessels from the ventral fissure and can be considered as the vena comitans of the anterior spinal artery.

This mostly continuous tract is located in the anterior fissure where it is running below the anterior spinal artery (Fig. 3.12a). It starts at the craniocervical junction, has its largest calibre lumbosacrally and proceeds as a sometimes very large terminal vein in 60–80 % of the cases (Kadyi 1889; v. Quast 1961; Thron 1988). It continues parallel with the filum terminale to the end of the dural sac and can actually be regarded as a coccygeal radicular vein. Occasionally, a sacral radicular vein of equally large calibre assumes this function. In this case, the terminal vein is then less well developed (Figs. 3.31 and 3.33e).

The remainder of the superficial veins exhibit courses independent of the arteries. The most important of these vessels is the posterior median spinal vein. It is significant in the cervical region, especially large and sometimes convoluted and dilated above the thoracolumbar enlargement and it ends at the level of the cone (Figs. 3.11, 3.31, 3.33, and 3.34). As a rule, this large-calibre, posterior drainage system is formed especially in the thoracic region by longitudinal vessels that cannot be schematically standardized. They are sometimes larger, sometimes smaller, now running more to the left, then more to the right at the dorsal circumference. Varicose convolutions are frequent and can also appear as extremely tortuous, radicular venous convolutions, as seen in Figs. 3.28 and 3.32.

Venous circles at the conus medullaris, connecting anterior and posterior channels are also found (Fig. 3.33c, d). However, they are often supplemented or replaced by intramedullary anastomoses and are much less constant than the arterial conus arcade. The contrast in calibres of the arteries and veins is striking. Even if one takes into consideration that veins can dilate unphysiologically under injection pressure, the figures obtained here are within the dimensions previously reported (Table 1.2). The veins of the thoracolumbar enlargement, with a diameter up to 1.5 mm, are undoubtedly the medullary vessels of largest calibre and are only rarely matched by superficial cervical veins (Figs. 3.19, 3.24, and 3.31).

### 3.2.2 Pial Venous Networks of Lower Degree

Ventrally as well as dorsally and laterally, short, secondary systems of smaller calibre exist. Of these, anterolateral veins show the greatest continuity, replacing the median vein in its function if it is interrupted (Figs. 3.11a, 3.12, 3.25, and 3.26). Superficial transverse vessels connect the longitudinal ones, although not as densely as in the case of the arteries. Moes and Maillot suggest to differentiate between a truncal and plexiform type of drainage especially in the cervical region (Fig. 3.10).

Fig. 3.9

Characteristics of superficial spinal cord veins. (a, b) X-ray films of an injected specimen in a.p. (a) and lateral view including a schematic illustration (b). The superficial longitudinal trunks anteriorly and posteriorly are typically located in the midline. They drain the pial venous networks of lower degree. In the lower half of the spinal cord the anterior median vein follows the filum terminale as terminal vein. The posterior median vein often exhibits a plexiform convolution of large veins on the posterior surface at low thoracic levels. It is called the posterior venous plexus. In certain regions of the cord frequent anastomotic channels of large calibre exist. They interconnect the main longitudinal trunks through the midline of the spinal cord parenchyma as shown on the diagram and on the lateral X-ray, some of them marked with arrowheads (b) (X-rays reproduced from Thron 1988)

Fig. 3.10

Superficial veins of the anterior (a) and posterior (b) surface in the upper half of the spinal cord, including the craniocervical junction. Note the convoluted veins of the posterior venous plexus and conjoint radicular veins or radicular vein complexes on the posterior surface at level T4/5 and T5/6. (b) (Reduced reproduction from Kadyi's monograph, 1889; Tafel II Figs. 5 and 6; upper half. The unsurpassed realistic and instructive anatomical drawings were designed by himself and realized together with the painter Heinrich Dyrdon)

Fig. 3.11

Superficial veins of the anterior (a) and posterior (b) surface in the lower half of the spinal cord. In this anatomical illustration, large anterior and posterior midline veins drain the lumbar enlargement. (a) The anterior midline vein follows the filum terminale. Two large radiculomedullary veins accompany low lumber or sacral nerve roots to exit the dural sac (compare Fig. 3.33e). (b) The posterior veins are stronger and more convoluted in the lower thoracic area (posterior venous plexus). The posterior midline vein terminates at the level of the cone. (Reduced reproduction from Kadyi's monograph, 1889; Tafel II Figs. 5 and 6; lower half. The unsurpassed realistic and instructive anatomical drawings were designed by himself and realized together with the painter Heinrich Dyrdon)

Fig. 3.12

Superficial veins of the spinal cord. Photographs of injected spinal cord specimens. (a) Photograph of the anterior aspect at thoracic level. The hairpin configuration in the course of venous outflow, formed by the connection between anterior median vein (thick arrow) and radiculomedullary vein (slim arrow) is very similar to the arterial counterpart. The dark blood vessel (small arrowhead) is the non-filled anterior spinal artery, running beside or over the vein (large arrowhead) (Reproduced from Thron 2008). (b) Photograph of the large venous trunk at the posterior aspect at thoracic level. Cranial to the posterior radiculomedullary vein the median trunk is replaced by a secondary system of pial veins

Fig. 3.13

Superficial spinal cord veins on the posterior surface. (a) Simplified diagram. A more or less continuous posterior median vein, exhibiting plexiform parts especially on the posterior surface of the lower thoracic region, extends over the whole length of the spinal cord. It gets smaller at the cranial and caudal end of the medulla spinalis. In between, numerous radiculomedullary veins provide outflow to the epidural venous plexus (symbolized by the blue rectangular blocks). (b) Photograph of a specimen at cervical and thoracic levels. The posterior median spinal vein is continuous from the cervical to the lower thoracic region, but shows a variable size at different levels. Four large r.m.v. and some smaller ones can be seen. c Photograph of the dorsal aspect of a spinal cord in situ (post-mortem) at thoracic and lumbosacral level. There are discontinuous longitudinal veins of median and paramedian location. The vessels show tortuosities and varicose convolutions above the lumbar enlargement. One of the r.m.v. can be attributed to the "great radiculomedullary vein" (arrow). (b Reproduced from Jacobs 1996; c Courtesy of Prof. Dauber, Institute of Anatomy, University of Tuebingen, Germany)

Fig. 3.14

Superficial veins of the spinal cord. X-ray film of two injected specimens. (a) X-ray in a.p. view. The lower cervical and upper thoracic part of this specimen demonstrates typical drainage through a continuous longitudinal midline tract and several radiculomedullary veins. These veins follow a nerve root and empty into the internal vertebral venous plexus. The descending courses of radiculomedullary veins result in hairpin configurations, which are very similar to the narrow curve of radiculomedullary arteries. (b, c) A.p. and lateral view of the lower half of an injected spinal cord. Three anterior radiculomedullary veins and a small posterior one at lumbosacral level are exhibited in this specimen. The anterior midline tract is more pronounced than the posterior one and includes plexiform at the low thoracic level as well as a radicular vein complex at mid-thoracic level on the left side. Large anastomotic tracts at different sides and levels of the cone, comparable to the arterial arcades around the cone, are additional unusual findings (arrows) (a Reproduced from Jacobs 1996)

## 3.3 Transmedullary Venous Anastomoses

Venous channels within the spinal cord parenchyma connect the superficial venous tracts. Along their course they show a constant calibre, and the large ones do not receive intrinsic tributaries. They have preferential sites, different courses and vary considerably in diameter.

Two types of these venous anastomoses can be distinguished:

  * Type 1: Centro-dorsolateral anastomoses Frequent oblique anastomotic connections between peripheral or central and peripheral branches (0.1–0.2 mm) (Figs. 3.16, 3.18, 3.20, 3.21b, and 3.26).

  * Type 2: Midline anastomoses They connect the main superficial venous tracts without receiving intrinsic tributaries (0.3–0.7 mm) (Figs. 3.1, 3.2, 3.5, 3.9, 3.17, 3.22, and 3.27).

Kadyi (1889) as well as Herren and Alexander (1939) already described the variable vessels of 0.1–0.2 mm thickness connecting central and peripheral branches (Fig. 3.15).

In addition, anastomoses of much larger calibre run between the superficial longitudinal trunks through the spinal cord. To our knowledge Crock and Yoshizawa were the first to mention and illustrate this type of venous channel in their book from 1977.

Our radiological evaluation of a large number of contrast-injected human spinal cord specimens clearly shows that transmedullary venous anastomoses are an essential component for the venous return of the spinal cord and that they are not rare, occasional findings. Instead, they constitute an essential principle of superficial and intrinsic spinal cord drainage: anastomotic pathways and interconnections.

The diameters of Type 2 anastomoses approach those of the superficial main channels (0.3–0.7 mm). These veins receive few if any veins draining directly from the spinal cord. Their assumed function could be to provide collateral pathways for the venous return of blood from the spinal cord.

Their sinuously oscillating, mostly anteroposterior courses visible in thicker mediosagittal sections make it clear why they are missed in thin, axial as well as coronary sections (Figs. 3.17, 3.18, 3.19, 3.20, 3.21, and 3.28). They can show varicose enlargement and elongation similar to the superficial veins (Fig. 3.19), or just run straight, or ascend and descend in wide arcs or peaks (Figs. 3.22 and 3.41). In axial sections, lateral bending around the central canal is typical (Fig. 3.17). Guided by these characteristic courses, the large, transmedullary venous anastomoses can be distinguished from superficial transverse anastomoses on X-rays of injected spinal cords.

They are not distributed uniformly over the length of a spinal cord. Their greatest incidence is found in the high thoracic region, where up to two such anastomoses per centimetre can be detected (Fig. 3.9).

This will be described in detail in the Sects. 3.4–3.6 about specific patterns of drainage in the different spinal cord regions.

In the mid and lower thoracic regions, internal venous anastomoses of large calibre occur at greater distances. As of yet, none were found to have any significant calibre in the lumbar enlargement, although in one case we detected an abnormally large anastomosis near the conus, replacing superficial anastomoses or running next to these (Fig. 3.22d).

Fig. 3.15

Intrinsic venous anastomosis type 1 at high cervical level (arrowhead). Anastomoses of 0.1–0.2 mm between different peripheral veins or branches of central and radial veins are frequent findings. They often course central areas to the dorsolateral surface. They receive intramedullary tributaries (Reproduced from Thron 1988)

Fig. 3.16

Intrinsic venous anastomoses type 1 demonstrated on sagittal microangiograms at thoracic level. (a) Right paramedian section. (b) Mid-sagittal section. (c) Left paramedian section. Several dissected venous anastomoses between radial veins can be identified. The small and large arrowheads point to the vessel segments, belonging to two continuous anastomotic veins. These vessels take different ascending and descending oblique courses through the spinal cord substance and receive smaller tributaries. Peripheral veins in anterolateral or posterolateral location (large and small arrow in c) may exhibit very different configurations. The unique tree-like ramification of the veins of the posterior septum and columns, demonstrated on the midsagittal section in (b) is again very different (b Reproduced from Thron 1988)

Fig. 3.17

Large transmedullary anteroposterior venous anastomosis type 2 demonstrated on a series of axial microangiograms (a–d) and outlined in a diagram (e). (a–c) The anastomotic venous channels through the midline of the cord show ascending and descending courses. Therefore, several contiguous axial sections are needed to reconstruct the vessel through the spinal cord substance between the two midline veins (arrowheads in a, b and c). (d) Image obtained by superimposing a and c. The short parts of the anastomosis included in b have to be added (arrowheads). The deviation of the anastomotic midline veins type 1 around the central canal is best demonstrated in the axial view (c). (e) Illustrative diagram of the different courses of anastomotic vessels type 1 (on Top) and type 2 (in the sagittal plane) (a, c Reproduced from Thron 1988)

Fig. 3.18

Frequency of occurrence and variability of anastomotic channels type 2 in the thoracic spinal cord. (a, b) X-ray in a.p. and lateral view. A few of the many anastomoses type 2 exhibited in the lateral view of the X-ray (b) were marked with an arrow. Number and distribution of type 2 intrinsic venous anastomoses can best be estimated on the lateral view of X-rays. The often steeply ascending and descending courses near the central canal make it clear that the vessels are regularly dissected on axial sections of 2–4 mm thickness and that they are very difficult to follow on coronal sections. (c, d) Two axial microangiograms at the mid-thoracic levels indicated in a, b. At least two contiguous slices are needed to follow the anastomotic vessel course (arrowheads in c and d). More dissected anastomotic connections can be supposed in view of additional venous segments of large calibre between the smaller peripheral veins

Fig. 3.19

Varicosity of intrinsic venous midline anastomoses type 2 at upper thoracic level. (a, b) X-ray in a.p. and enlarged in lateral view. (c) Microangiogram of the mid-sagittal section at the T3 level. A large-sized tortuous midline anastomosis connects the superficial midline veins (vertical arrow in b and c). A similarly large and tortuous anastomotic vein can be identified on the lateral view of an X-ray of the contrast-injected specimen shown in b, based on the typical course and calibre (oblique arrow) (Reproduced from Thron 1988)

Fig. 3.20

Different types of intrinsic venous anastomoses at thoracic level. (a) X-ray of an injected specimen in a.p. view. (b, c) Mid-sagittal microangiograms at upper thoracic level, contiguous in vertical direction, as outlined by the vertical bar in a. Courses, calibres and drainage functions of different types of anastomotic veins through the midline of the spinal cord parenchyma are obvious on these slices. The large channels type 2 do not receive tributaries from the parenchyma, whereas smaller anastomoses between central and radial veins do. Posterior peripheral veins (at the side of the included diagram) at this thoracic level deeply penetrate into the medullary parenchyma and take a descending course (c)

Fig. 3.21

Intrinsic venous anastomoses demonstrated in coronal sections. (a) X-ray in a.p. view. (b–d) Three microangiograms of coronal sections corresponding to the section positions S2–S3 of the schema. The anterior and posterior superficial sections are not shown. The large midline anastomotic channel type 2 can be followed, but it is cut into short pieces (arrows). The arrowhead in b points to an interesting vertical connection between two large radial veins in the border zone of the anterior horn

Fig. 3.22

Microangiograms of large midline anastomoses at different levels of the spinal cord. (a–d) Mid-sagittal sections of injected specimens. The large channels connect the superficial longitudinal midline veins and do not receive from intramedullary tributaries. They show different courses but a similar deviation around the central canal (cf. Figs. 3.1 and 3.17), often combined with an up- and downward movement at this point. Even varicose dilatation and elongations were observed in some specimens (Fig. 3.19) (Reproduced from Thron 1988)

## 3.4 Specific Patterns of Venous Drainage in the Cervical Spinal Cord

Radial symmetry and horizontal distribution of intrinsic veins are very pronounced in the cervical spinal cord (Fig. 3.23).

Transmedullary midline anastomoses are frequent in the upper and mid-cervical regions, but they are of smaller calibre than those in the lower cervical and upper thoracic regions (Figs. 3.5, 3.15, and 3.24).

The anterior median vein is frequently larger than the posterior median vein. Radicular outflow to the epidural plexus occurs at many levels (Figs. 3.10, 3.13, and 3.14a).

Additionally, both veins connect to the brainstem veins (Fig. 3.10) and basal sinuses around the foramen magnum (Fig. 3.36). On the posterior aspect of the upper spinal cord and medulla oblongata differentiation between a truncular type of drainage in 80 % and a plexiform venous drainage pattern in 20 % of cases was described by Moes and Maillot (1981).

Fig. 3.23

Microangiograms of transverse sections at various levels of the cervical spinal cord. The intrinsic drainage pattern is characterized by radially and horizontally oriented peripheral veins draining the central as well as the peripheral nervous tissue. The central veins play a minor role compared to central arterial supply (Reproduced from Thron 1988)

Fig. 3.24

Intrinsic radial veins at a high cervical level (C2–C3). (a) X-ray in lateral view. The superficial anterior midline vein has a large calibre. (b) Microangiogram of a mid-sagittal section at the C2–C3 level as indicated in a. Apart from peripheral veins some central veins running in the anterior fissure with and without anastomotic connections to posterior veins can be discriminated (arrows). (c) Microangiogram of a parasagittal section. The main drainage occurs through horizontally oriented peripheral veins

## 3.5 Specific Patterns of Venous Drainage in the Thoracic Spinal Cord

Anterior and posterior median veins are commonly of equal size in the upper thoracic region. At lower thoracic levels the longitudinal venous trunks on the posterior surface show variable positions and courses, which deviate from the midline and may form plexiform convolutions, also called the posterior venous plexus (Figs. 3.9, 3.10, 3.11, and 3.13).

In the thoracic cord the course of peripheral and central veins as well as of small anastomotic veins is much more vertically oriented, compared to the mainly horizontal distribution of intrinsic veins in the enlargements. The greatest incidence of type 1 and type 2 intrinsic anastomotic veins is found in the thoracic region.

Among the posterior radiculomedullary veins in the thoracic region non-functional vessels exist (Figs. 3.38 and 3.43a). Moes and Maillot (1981) mention fibrotic veins in this location in the majority of their specimens.

Fig. 3.25

Veins of the thoracic spinal cord. Variability of peripheral veins and intrinsic venous anastomoses. (a, b) X-ray film of an injected spinal cord in a.p. (a) and lateral view (b). The broken lines indicate the level of the cross sections in c–f. (c) Axial microangiogram at a mid-thoracic level. In this section, a vein of the left intermediate posterior septum is the most prominent and deepest penetrating venous blood vessel. (d–h) Series of axial microangiograms at mid-thoracic level, demonstrating the changing pattern of peripheral veins in nearby sections. Strong vein of the posterior septum in f. Parts of very large vessels in the anterior fissure like in e, f and h (arrow) or around the central canal like in g (arrow) are most likely dissected parts of intrinsic anastomoses between central and peripheral veins. (i, j) Axial microangiograms at low thoracic level. The very large vessel in the anterior median fissure is not a central vein, but certainly part of a large midline anastomosis type 2 (arrowhead) (Reproduced from Thron 1988)

Fig. 3.26

Superficial and deep thoracic spinal cord veins of unsystematic and irregular appearance due to a missing anterior midline trunk. (a) X-ray film of the specimen in a.p. view. (b) Mid-sagittal section at the T3 level as indicated by the vertical line in a. At the level of this section posterior veins are in midline position (arrowhead). But there is no significant venous trunk in anterior midline position. Numerous transparenchymal venous anastomoses of moderate calibre cross this midline section. Most of them take an oblique path with ascending and descending loops and are cut in this median section at one point or another (arrows). The smaller veins are irregularly distributed and linked to one another in a pattern, appearing unsystematic. (c) Axial section, contiguous to the lower end of b. Corresponding to b, the radial veins follow a horizontal course only for short distances. The arrow points to a dissected vessel of larger calibre situated at the posterior intermediate septum on the right. It should be the posterior part of the lowest transparenchymal anastomoses marked with an arrow in b (Reproduced from Thron 1988)

Fig. 3.27

Intrinsic veins in midline position between anterior and posterior midline trunks. Caudal continuation of Fig. 3.26. (a) X-ray in a.p. view. (b) Microangiograms of two consecutive mid-sagittal sections at the T4–T6 level. Numerous intrinsic anastomotic veins of different size (0.3–0.5 mm arrows and arrowheads) connect the median longitudinal trunks in the midline. Median or intermedian veins of the posterior columns start in the centre of the cord and take a long descending course. Small anastomotic connections (0.1 mm) with branches of central veins are numerous. Compare Fig. 3.20. The vertical component of the vessel courses is similar to Fig. 3.26b, but the pattern of drainage through peripheral and anastomotic veins follows a more systematic pattern (Reproduced from Thron 1988)

Fig. 3.28

Superficial and intrinsic thoracic cord veins at the level of the posterior venous plexus including large midline anastomoses type 2 in coronal microangiograms. (a) The anterior frontal section shows the anterior median vein (arrows) collecting numerous superficial branches from the parenchyma and the roots as well as some large veins emerging out of the anterior fissure (arrowheads). (b) The mid-frontal section demonstrates three disconnected and partly dislocated large-sized veins (arrowheads) in the location of the arrowhead-marked vessels in (a). Sporadic, small central veins (small arrows) and peripheral veins directed to the lateral surface. (c) On the posterior surface the superficial veins exhibit varicose convolutions corresponding to the posterior venous plexus (arrows). The numerous large-sized anastomotic midline channels, connecting the posterior venous plexus with the anterior median vein are disrupted by dissection and partly dislocated and are therefore not adequately demonstrated (Reproduced from Thron 1988)

## 3.6 Specific Patterns of Venous Drainage in the Thoracolumbar and Sacral Spinal Cord

At the thoracolumbar enlargement including medullary cone, intrinsic venous drainage differs from the rest of the spinal cord and is more similar to the arterial supply pattern. Hence, central veins may be considerably larger than peripheral veins (Figs. 3.29, 3.30, and 3.31).

Compact sequences of central veins can possibly be seen, exhibiting calibres of 0.1–0.25 mm, which correspond to those of the arterial counterparts. But they exceed them in number, as should be expected. In 2.5-cm-long mid-sagittal sections of the lumbar enlargement, as shown in Figs. 3.29 and 3.31, approximately 25–40 sulcal veins are found, in contrast to 25 sulcal arteries, which would be expected in this location. (Compare arterial supply in Figs. 2.59 and 2.60 with venous drainage in Fig. 3.31.)

No midline anastomoses of significant calibre were found in the lumbar enlargement, although in one case, seen at the conus, a very large anastomotic tract type 2 apparently substituted superficial anastomoses (Figs. 3.22d and 3.30d).

The anterior midline vein reaches its maximum calibre in this region and it is important to note that the vein of the filum terminale is the continuation of this anterior median vein, which is very clearly shown in the anatomical drawing by Kadyi (Fig. 3.11a) and in many radio-anatomical images, e.g. Figs. 3.29, 3.30, and 3.32. Alternatively, the anterior midline vein on the enlargement or cone follows a lumbar or sacral nerve root to reach the sacral epidural space (Figs. 3.11, 3.31, and 3.33c–e).

The posterior median spinal vein is particularly large above the thoracolumbar enlargement (Figs. 3.10b, 3.11b, 3.13, 3.30, and 3.31), frequently forming varicose convolutions called posterior venous plexus. This trunk ends at the level of the cone and anastomoses with the anterior median spinal vein. The anterior and posterior venous tracts on the surface of the thoracolumbar enlargement and their radicular venous outlet(s) are the most prominent blood vessels of the spinal cord with diameters up to 2 mm (Figs. 3.30, 3.31, 3.32, and 3.33). When demonstrated by tomographic imaging techniques without adequate time resolution they should not be mistaken for spinal cord arteries.

Fig. 3.29

Predominant anterior median and terminal vein. (a, b) X-ray of the specimen in a.p. and lateral view. (c) Two mid-sagittal contiguous microangiograms from the region of the lumbar enlargement and cone demonstrate a predominant terminal vein (arrowhead) and intrinsic veins in which central veins play a substantial role. (d–f) Axial slices from the lumbar level indicated in c exhibit a radial symmetry of veins in the contrast-filled central and anterior parts of the cord (a–c Reproduced from Thron 1988)

Fig. 3.30

Veins of the thoracic and lumbosacral spinal cord. (a, b) X-ray films of an injected spinal cord in a.p. and lateral view. (c) Microangiogram of a mid-sagittal sections from the levels indicated in a. Central veins in the lower thoracic region are less numerous than the peripheral veins of the posterior columns, but they are somewhat larger in calibre (arrowheads). Several of them may join to form a common stem (anterior arrowhead). (d) The large transparenchymal anastomosis near the conus medullaris (arrow) has a calibre of about 1 mm (Reproduced from Thron 1988)

Fig. 3.31

Variations of lumbosacral vein patterns. (a, b) X-ray of the injected specimen in a.p. and lateral view. The thick and convoluted vein (arrowheads) belongs to the posterior venous plexus of the low thoracic region. It passes to the anterior surface using superficial branches around the cord (not midline anastomoses as might be suspected from b). Anteriorly, it divides into two radiculomedullary veins which follow different lumbar and sacral nerve filaments of the cauda equina (large and small arrow). Only a very small branch accompanies the filum terminale (small open arrow). (c) Two contiguous midline sections include the large radiculomedullary veins and the small filum terminale vein (arrows). The midline sections exhibit central and peripheral intrinsic veins in a distribution typical for this region without significant intrinsic anastomotic interconnections

Fig. 3.32

X-ray films of injected spinal cord specimens in a.p. view. Different patterns of superficial veins at the thoracolumbar enlargement and cauda equina. (a–d) The posterior venous plexus with varicose convolutions and a "great radiculomedullary vein" (arrows) are common findings as well as a distinct terminal vein (arrowhead). The large radiculomedullary vein in a is a conjoint vein from two superficial trunks. The specimen shown in d features an extreme varicosity of a sacral radicular vein on the right side (arrow) (c, d Reproduced from Thron 1988)

Fig. 3.33

X-ray films of injected spinal cord specimens. Variations of venous drainage at the lower end of the spinal cord. (a, b) A.p. and lateral view. There is a large "great anterior radicular vein" and a distinct terminal vein (arrowheads), but only a weakly developed posterior venous plexus. (c, d) A.p. and lateral view. In this specimen the terminal vein is replaced by two strong anterior thoracolumbar radicular veins. Furthermore, lateral anastomoses around the cone on both sides (but different levels) resemble the arterial arcades. Radiculomedullary vein complex at mid-thoracic level. (e) A.p. view. Pronounced varicosity of veins on the thoracolumbar enlargement. Two sacral veins on the right side (arrowheads) and a great radicular vein on the left side substitute the drainage function of a terminal vein (e Reproduced from Jacobs 1996)

Fig. 3.34

Basic pattern of anterior and posterior superficial veins at thoracolumbar level. (a) Diagram of anterior veins. Typical findings in the lower part of the lumbar enlargement are a large anterior midline vein, proceeding as vein of the filum terminale in variable size. Moreover, additional radiculomedullary veins of considerable size are frequent findings, some of them originating from very deep sacral levels (cf. Fig. 3.31). (b) Diagram of posterior veins. A plexiform pattern of veins is almost regularly observed in the upper part of the enlargement (posterior venous plexus), as well as large posterior radiculomedullary arteries

## 3.7 Radiculomedullary Veins and the Transdural Course

Venous blood collected in the large longitudinal venous trunks on the surface of the spinal cord issues into anterior or posterior radiculomedullary veins, which cross the dura and empty into the internal vertebral venous plexus (Fig. 3.35). A hairpin bend in the course of radiculomedullary blood vessels is not only typical for spinal cord supplying arteries. As a result of the rising of the spinal cord, the radiculomedullary veins take similar hairpin courses. Commonly, they follow a nerve root and descend to an intervertebral foramen where they pierce the wall of the dural sac close to the nerve root in about 70 %, but their exit may be completely independent from the nerve root in 30 % (Thron et al. 2015). After crossing the dura mater, the so far distinct vessels empty in about 95 % into the lacunae and irregular spaces of the internal vertebral venous plexus. Rarely, a direct continuation to the intervertebral veins can be seen (Fig. 3.42c).

Documented by the experience of selected spinal angiography, most of the venous return passes through radiculomedullary veins (Fig. 3.35). At the craniocervical junction, connection occurs between the superficial venous trunks and the intracranial dural sinuses at the base of the posterior cranial fossa. Figure 3.36 demonstrates the case of a dural arteriovenous fistula located at an upper thoracic level with ascending drainage. Apart from segmental radicular outflow in the cervical region the dilated anterior median spinal vein seems to join directly the basilar or marginal sinus and continue through petrosal inferior and superior sinuses bilaterally. Whether this occurs really directly or via passage of parts of the internal vertebral venous plexus is not apparent in our case. In a second example of increased descending flow, caused by a dural arteriovenous fistula, the anterior median spinal vein can be followed downwards to radicular veins of the cauda equina (Fig. 3.37b; small arrow) until these vessels empty in an extended sacral epidural plexus at the end of the dural sac.

The true number of radicular spinal cord draining veins faces a problem of anatomical nomenclature, similar to the one encountered with the arteries.

In an older nomenclature the terms "radicular artery" and "radicular vein" were both used for blood vessels running with a nerve root, irrespective of their area of supply or drainage. Radicular blood vessels with and without relevance for the spinal cord blood circulation were not clearly discerned by nomenclature. Only in the French literature, the specification "radiculo-médullaire" was commonly used to specify spinal cord–supplying radicular arteries (Lazorthes et al. 1973), but also spinal cord–draining veins (Tadié et al. 1979, 1985). In any case, for a well-defined attribution of spinal cord–draining veins this specification seems indispensable. The term "radiculospinal", introduced in the Anglo-American nomenclature for this purpose, is less correct from an anatomic or semantic point of view, because we are not dealing with the spine, but with the spinal cord. That is different.

We suggest to use a nomenclature adjusted to the one proposed for the arteries, despite the fact that the pattern of venous drainage is predominantly independent from the pattern of arterial supply. But the different anatomical regions and functional aspects make it necessary to discriminate

  * Radicular veins draining the metameric elements like bone, dura mater, nerve roots of a given metamere and

  * Anterior and posterior radiculomedullary veins, which have additional drainage function for the spinal cord.

The question of how many radiculomedullary veins are preserved after embryonic life for the venous outlet of the entire spinal cord has been a matter of dispute. The group of Tadié et al. had insisted on an average number of only nine to ten veins, definitely carrying the venous return.

According to the older literature data, the total number of morphologically countable spinal cord draining veins should add up to 30–70 (Kadyi 1889; Tureen 1938; v. Quast 1961; Jellinger 1966), with an average of over 50 per spinal cord. An equivocal numerical dominance of anterior or posterior radicular veins has not been reported. Jellinger (1966) calculated an average of 23 ventral and 25 dorsal outflows, whereas v. Quast (1961) calculated 30–26. This almost symmetrical anterior-posterior distribution was accompanied by a minimal fluctuation in the segmental distribution. A significant reduction should only occur in the uppermost cervical and sacral segments. Likewise, no obvious lateral preference was observed.

These data supported the widely accepted conclusion of a much more pronounced symmetry and metameric structure, preserved in the radicular drainage system.

The calibre of the anterior radiculomedullary veins lies between 0.25 and 1 mm, whereas some of the posterior radiculomedullary veins can reach calibres up to nearly 2.00 mm.

Compared with the great anterior radiculomedullary artery, an especially large anterior or posterior radiculomedullary vein can be demonstrated with less frequency. This vein drains the caudal intumescence and is located ventrally between T6 and S3. The dorsal vessel of maximal calibre is situated between T9 and S3 with a distribution maximum at L1 (Jellinger 1966). The radiculomedullary veins in this region are the largest blood vessels around the cord intradurally.

Differentiation of radicular and radiculomedullary veins solely on the basis of macroscopic inspection may be problematic, especially for the numerous small veins running with the nerve roots or the filaments of the cauda equina. Morphological criteria include that radiculomedullary veins can easily be separated from the nerve root or cauda filament and that purely radicular veins increase in size if they are followed towards the spinal cord surface (Moes and Maillot 1981).

Tadié et al. (1985) used radiographic and cinematographic films to define radiculomedullary veins "through which the contrast medium leaves the spinal veins and the intradural sector to reach the extradural sector and the periphery".

In the large numbers of radicular veins counted by previous investigators, purely radicular veins might have been included. But even if all small veins less than 0.25 mm are excluded, the number of at least medium-sized radiculomedullary veins draining the spinal cord (and not only the radix or small parts of the pial plexus) remains in the range of 6–11 for the anterior and 5–10 for the posterior systems. These numbers can be determined from the data of Kadyi (1889) and Suh and Alexander (1939), who listed and categorized the number, localization and calibre of the observed radicular veins meticulously. They are in agreement with a study performed at our department (Jacobs 1996). If one accepts the principle that the volume for venous return has to exceed the volume of arterial input by a factor of 2.5 because of the different flow characteristics of arteries and veins (Kadyi 1889), the large numbers are reasonable and necessary.

Similar to the arterial supply individual protocols of number, distribution and calibre of radiculomedullary veins in post-mortem studies reveal highly variable patterns of drainage. This justifies the differentiation between a pauci- and a plurisegmental type of drainage similar to the arterial supply.

Conjoint and non-functional radicular veins are special observations made at the final intradural vein segment. Two or more veins coming from the medullary surface can merge to form a single radiculomedullary vein just before reaching the dura mater. Then, together or independent from the root, they pass as a common trunk through the dura and drain into the internal vertebral venous plexus (Fig. 3.38). The arrangement of several veins of ascending, descending or horizontal course converging radially to form a single radiculomedullary vein, as demonstrated on Figs. 3.10b, 3.35, and 3.38, has been called a radiculomedullary vein complex (Kadyi 1889). These veins may cross the dura mater in very atypical locations between two nerve roots.

This configuration of surface veins conjoining to a single radicular vein can also be observed in a variation or pathologic finding, in which the singular terminal segment is occluded immediately behind the communication. Only a few authors have reported the occurrence of such blind ending radicular veins. Moes and Maillot (1981) called these more or less fibrotically occluded radiculomedullary veins "non-functional veins", occurring mainly among the posterior thoracic radicular veins. Crock et al. (1986) presented an image of this arrangement, which they described as "V-shaped anastomosis" or "arrow-tipped loop of the dorsal median longitudinal trunk".

Examples from our investigations are shown in Figs. 3.38b and 3.43a. The aetiology and clinical relevance of such fibrotic radicular veins are unclear (Thron et al. 2015) and in so far open for hypothetical considerations (Gailloud 2014). The fibrotic segment may represent a residue from the embryonic desegmentation process. Likewise, the occurrence mainly among posterior thoracic veins might be related to the high variability and sometimes poor development of the posterior part of the internal vertebral venous plexus as reported by Groen et al. (1997).

Figure 3.46, reproduced from a cadaver study using injection of a modern polymer (Araldite CY 221), illustrates this high segmental and interindividual variability, which is in contrast to the fairly constant anterior part. Poor development of this posterior plexus could be the cause of secondary fibrotic regression of initially patent posterior radicular veins. Other possible aetiologies like focal inflammation or thrombosis appear unlikely but cannot be ruled out. The clinical significance of non-functional radicular veins is so far unclear. Hypothetically, they could play a role in the noticeable delay of hindered spinal drainage, observed in many cases of spinal dural arteriovenous fistula (SDAVF) (Merland et al. 1980).

Varicose convolutions, more frequent on the posterior than on the anterior surface of the spinal cord, are not unusual (Figs. 3.31 and 3.33). Even extreme varicosities of radiculomedullary veins like in Fig. 3.32d may be observed as incidental findings. This is why the term "spinal varicosis" was frequently used in the older neuropathology literature and in the evaluation of myelograms. Even today, accentuation of plexiform veins on tomographic images may cause confusion with regard to the differentiation between a normal and a pathological finding. In cases of doubt, especially if combined with clinical suspicion, exclusion of an arteriovenous shunt disorder is necessary.

The dural segment of radiculomedullary veins connects the veins of the subarachnoid space with the internal vertebral venous plexus (Batson's plexus).

Many investigators found that filling of intrathecal spinal cord veins in a retrograde manner from the outside of the dura mater could not be achieved or only with bad results (Breschet 1828–1832; Kadyi 1889; Batson 1957; Clemens 1961; Dommisse 1975; Crock et al. 1986). This is why the presence of valves close to the dura mater was generally assumed. Another convincing clinical argument for the necessity of valves was seen in the prevention of reflux to the spinal cord veins in case of extraspinal venous hypertension. Oswald (1961) then reported the existence of bicuspid venous valves in the radiculomedullary veins, immediately after passage through the dura. But subsequent investigators (Tveten 1976; Tadié et al. 1979, 1985) did not confirm this observation. Instead, Tadié et al. suggested a different "anti-backflow control system" consisting in a high reduction of vessel calibre at the dural segment of radicular veins and an oblique zigzag course of the vessel.

To improve our understanding of the assumed reflux-impeding arrangement in the dural segment of spinal cord–draining veins, a microscopic and microangiographic investigation was performed in the late 1980s at our institution (Otto 1990; Thron et al. 1990; Schroeder et al. 1993). Secondly, the unknown vulnerability of venous return from the spinal cord in the absence of an arteriovenous shunt should be studied. Again, no valves could be detected (Fig. 3.41). Similar features as described by Tadié et al. (1985) were identified. An oblique and sometimes bending transdural course associated with narrowing of the vessel lumen was observed in about 60 % of the studied specimens. However, microscopic evaluation of a total of 102 radiculomedullary veins revealed a second arrangement, comprising 35 % of examined cases.

Exemplifying histological sections of these two main types, called "slit" type and "bulge or nodular" type by Otto (1996), are demonstrated in Fig. 3.39. A diagram of both types is presented in Fig. 3.40.

The slit type occurs mainly in the vicinity of nerve roots. The dural segment shows narrowing of the lumen. The vessel wall is mostly replaced by fibrous tissue of the dura. The vessel courses in an oblique direction, sometimes bending or kinking.

The bulge or nodular type mainly occurs with vessels crossing the dura at some distance from a nerve root. There is considerable broadening of dural collagen fibres at the site of dural penetration, which follows the blood vessel in the direction of the epidural compartment. Narrowing or splitting of the lumen occurs within the fibrous tissue formation, which eccentrically encapsulates the disintegrated blood vessel.

Why these different arrangements at the dural exit of veins exist is yet unclear.

A reflux-impeding or better flow-modulating effect might be attributed to both devices. To what extent both exit arrangements with narrowing of the lumen impede reflux from the outside of the dura mater or influence flow in either direction is again unclear. Out of 14 attempts to fill the intrathecal veins from the extradural space, two were successful in our specimens. Figure 3.44 shows the radiculomedullary vein and the beginning longitudinal tract contrasted via the lacunae of the epidural plexus.

Clinical situations in which these devices did not strictly prevent reflux are spinal phlebography (Fig. 3.45) with abdominal compression (Théron and Moret 1978; Meijenhorst 1977) or SDAVF shunts to the internal vertebral venous plexus and secondary, at another place, reflux to superficial spinal cord veins (Krings et al. 2006). Examples in this book are Figs. 4.34, 4.38 and 4.39. But in the meantime not only the presence of valves but generally the existence and necessity of anti-reflux arrangements are not undisputed (Groen 1997; van der Kuip et al. 1999).

In two post-mortem studies from the end of the 1990s, cadavers were thoroughly prepared including removal of clotted blood before a modern polymer (Araldite CY 221) was injected to demonstrate the internal vertebral venous plexuses (Groen et al. 1997) and the human radicular veins (van der Kuip et al. 1999). These procedures allowed retrograde filling of intradural radicular veins to be documented as a rather regular and not as an exceptional observation. Therefore the conclusion is justified that reflux into radiculomedullary veins might be a physiological phenomenon (van der Kuip et al. 1999). Our reconsiderations concerning anti-reflux arrangements have been published recently (Thron et al. 2015).

The X-rays of the specimens injected for microangiography (Figs. 3.42, 3.43, and 3.44) confirm oblique vessel courses through the dural sheet and narrowing of the lumen. Moreover, they confirm a connection between regularly composed veins and a system, which in the majority of our specimens comprises multitudinous communicating lacunar spaces. Most of the epidural venous plexus compartments in our specimens injected for microangiography have a similar sponge-like aspect. In only a few cases the epidural plexus was composed of defined venous blood vessels or a mixture of both.

The functional role of this probably predominant internal vertebral venous plexus for blood flow adjustments between the intra- and extradural compartments of the vertebral canal remains poorly understood.

Fig. 3.35

Superficial spinal cord veins and radiculomedullary veins. X-rays of contrast-injected human spinal cord specimens in a.p. view. (a) Upper thoracic region. The anterior median venous trunk communicates through radiculomedullary veins with the internal vertebral venous plexus (Pl.ep.) after crossing the dura mater (D; arrows) (Reproduced from Thron 2015). (b) Mid-thoracic region. Not only singular veins branch from the longitudinal midline trunks to join the epidural plexus (arrow). Two or more radicular and radiculomedullary veins from different parts of the surface can merge to a common stem just before penetrating the dura mater (D), thus forming a "radiculomedullary vein complex" (Kadyi 1889)

Fig. 3.36

Digital subtraction angiogram of the superficial spinal cord veins in case of a dural arteriovenous fistula at thoracic level. (a, b) Cervical region: lateral view (a) and a.p. view (b). The large anterior median spinal vein (arrow) joins the petrosal sinuses (white arrows) rather directly than via the basilar or marginal sinuses. The posterior median spinal vein and the cervical radicular outflow at the C2/3 level (arrowhead) are additionally opacified (Reproduced from Thron 2002)

Fig. 3.37

Unsubtracted and subtracted image of digital subtraction angiography in case of a spinal dural arteriovenous shunt. Drainage is observed along the veins of the cauda equina (small arrow) downwards to the sacral epidural plexus (large arrow) (Reproduced from Thron 2002)

Fig. 3.38

Photographs of conjoint radiculomedullary veins presenting a fibrotic common radicular stem in one of the two cases. (a) Posterior surface veins merge to a common radicular stem immediately before penetrating the dura mater at low thoracic level (arrow) (Reproduced from Jacobs 1996). (b) The median longitudinal venous trunk deviates from the midline to form a radicular vein. The point of junction to form a single radicular vein is halfway to the dura mater in this specimen. The communication between upper and lower part of the longitudinal channel is preserved, but the single radicular vein is a non-functional fibrotic vein (arrow)

Fig. 3.39

Structurally different types of blood vessel exit through the dura mater. Histological sections, H&E, original magnification ×60. (a) "Slit type" showing a vein accompanying a nerve root to the nerve root sheath before penetrating the dura mater. The vessel course is marked with arrows. The narrowing and oblique transdural course are evident, as are the alteration of the blood vessel into a fissure-like narrowed channel. (b) "Bulge or nodular type" refers to the bulge of collagen in which the vein loses its normal structural integrity (Reproduced from Thron et al. 2015)

Fig. 3.40

Schematic illustrations of the "slit type" of dural vein passage (a) and the "bulge or nodular type" (b) (Reproduced from Thron et al. 2015)

Fig. 3.41

Histological sections of the dural segment of a radiculomedullary vein at the T9 level. Even in this technique, providing semi-thin sections, valves could not be demonstrated. Moderate narrowing of the vessel calibre and an oblique course when crossing the dura mater seem to be the only specifications to provide anti-reflux properties in this example (Reproduced from Thron et al. 2015)

Fig. 3.42

Transition of radiculomedullary veins to the internal vertebral venous plexus. Different configurations as demonstrated by post-mortem X-ray microangiography following orthograde contrast injection. (a) Short transdural passage of a radiculomedullary vein running with the nerve root. The lacunar spaces of the epidural venous plexus surround the nerve root sheath (slit type, level T7). (b) Tidy narrowing of the dural vein segment and acute angle between the subarachnoid vein and the recipient epidural vein. In this case the internal vertebral venous plexus is composed of an irregular plexiform convolution of distinct veins (histologically, the type of dural transition could not be assigned to slit or bulge type, level T6). (c) Rare dural transit of a radicular vein which continues in the epidural space as an intervertebral vein of equal size. There is only circumscribed narrowing of the vessel lumen while crossing the dura mater in an oblique course (slit-type, level T7). (d) Two pairs of radiculomedullary veins of different size, merge directly before they cross the dura mater. Narrowing of the lumen and kinking or bending course are similar (arrows). The larger veins empty in a lacunar part of the epidural plexus distant from the nerve root, the smaller ones in an extensively contrasted epidural venous space surrounding the nerve root sleeve (bulging type, level T10) (Reproduced from Thron et al. 2015)

Fig. 3.43

Microangiograms of the dural segment of radicular veins. (a) Fibrotic, "non-functional" radicular vein. Specimen at the L1 level following injection of an X-ray contrast medium. Two radiculomedullary veins of the cauda equina conjoin to a common radicular stem very close to the wall of the dural sac. Whereas free communication between the two veins is preserved, only a filiform residual lumen of the common stem can be demonstrated radiographically. It can be followed to a tiny dural or epidural compartment (arrows) (Reproduced from Thron et al. 2015). (b) Microangiogram of a specimen containing two conjoining small radicular veins and two conjoining large radiculomedullary veins (T9 level). Oblique passage through the dura mater and narrowing of the lumen (arrow) are evident. Blood flow is carried forward into irregular lacunar spaces of the epidural plexus (Reproduced from Krings et al. 2006)

Fig. 3.44

Malfunction of the presumed anti-reflux arrangement at the transdural exit of radiculomedullary veins (arrow). X-ray of the specimen in a.p. view. Following contrast injection of the internal vertebral venous plexus surrounding the dural sac, retrograde filling of a r.m.v. (arrowhead) at the T5 level was observed (D dura mater; r.m.v. radiculomedullary vein) (Reproduced from Thron et al. 2015)

## 3.8 Extradural Intraspinal and Extraspinal Venous Systems

Drainage of blood from the spine (including spinal cord) occurs through the internal and external vertebral venous plexuses of Batson (1957), which are connected to each other through intervertebral veins. Both are valveless epidural systems with an anterior and posterior part. The internal vertebral venous plexus lies within the vertebral canal between the dural sac and the outer margins of the vertebral canal. This system is still controversial in nature; either plexal or venular (Lasjaunias and Berenstein 1990). It is the first compartment, which receives blood from the radiculomedullary veins draining the spinal cord. Most of the compartments of the internal vertebral venous plexus close to the dura, which were injected and opacified for microangiography in our specimens, have a similar aspect. It can best be described as a system of smaller and larger venous lakes, lacunae and fissures (Figs. 3.42, 3.43b, and 3.44). In only a few cases the epidural plexus was composed of defined venous blood vessels or a mixture of both (Fig. 3.42c). This sponge-like system of venous pools extends over the whole length of the vertebral column (Fig. 3.45) from the sacrum to the skull base and connects pelvic veins with the basal cranial sinuses.

An example of spinal angiography in case of an arteriovenous shunt disorder shown in Fig. 3.36 indicates that the anterior spinal vein communicates with the basal sinuses around the foramen magnum. As an important collateral pathway, the internal vertebral venous plexus bypasses extraspinal longitudinal systems like the cava or azygos system (Lasjaunias and Berenstein 1990). The external vertebral venous plexus, lying on the outer surface of the vertebral column, is connected to the inner one (Fig. 3.45).

The anterior internal vertebral plexus is larger and more constantly developed than the posterior one (Figs. 3.45 and 3.46). The reason for this is that it receives venous blood not only from the spinal cord but also from the basivertebral veins of the vertebral body.

The valveless system of the plexuses is connected to the azygos and hemiazygos systems by intercostal or segmental veins and in the cervical region to the vertebral and deep cervical veins (Fig. 3.47).

Fig. 3.45

Lumbar venograms demonstrate large parts of the internal vertebral venous plexuses. The anterior venous plexus as the longitudinal part (small open arrow) together with the retrocorporeal network including the basivertebral vein of the vertebral body (large open arrow) form the oval-shaped configurations at each level. They are preferentially demonstrated in these clinical venograms. The posterior internal vertebral venous plexus is of high interindividual variability, better shown in the schematic drawings of Fig. 3.46. Intervertebral and emissary radicular veins are lateral connections (small arrows) to longitudinal external efferents, which may not be continuously developed (arrowheads). (a) Normal findings. (b) Venogram in case of lateral disk herniation. The lack of the vein(s) accompanying the S1 nerve root on the right side to the foramen (small black arrow) substantiate the suspicion of lateral disk herniation (Courtesy of Professor H. Becker, image archive of Professor H. Vogelsang, Institute for Neuroradiology, Hannover Medical School, Germany)

Fig. 3.46

The posterior internal vertebral plexus exemplified in three schematic drawings obtained in an intravenous postmortem injection study. They outline and stress the prominent differences in the segmental and interindividual configurations (Sect. 3.8) (Reproduced from Groen et al. 1997 © 1997 WILEY-LISS, INC, artist's impression, C. Zondergeld)

Fig. 3.47

Diagram of drainage routes and anastomotic interconnections between spinal cord draining veins and systemic veins of thorax, abdomen and pelvis. The small blue blocks in the course of radiculomedullary veins indicate the exit of these vessels through the dura mater and the compartment of the internal vertebral venous plexus, interposed in the drainage route

## 3.9 Anatomical and Haemodynamical Aspects of Venous Drainage

### 3.9.1 Intrinsic Veins

The spinal veins, especially the intramedullary ones, have been mostly neglected in neuro-anatomical studies (Gillilan 1970). The fundamental structure of this drainage system is assessed very diversely. The division into central and peripheral systems proposed in several studies (Jellinger 1966; Tveten 1976; Lanz and Wachsmuth 1982) is modelled after the pattern of arterial supply. However, since the pattern of venous drainage deviates substantially from that of the arteries, the sense of an analogous classification is at least questionable.

The radioanatomic images presented in this book visualize the intrinsic venous drainage of the spinal cord as a radially arranged vascular system. These mostly peripheral veins originate at different depths of the cross-sectional area and run directly to the periphery. Anteromedian and posteromedian vessels, including central veins, dominate to a certain extent in different regions. But basically, venous drainage more likely complements the arterial supply pattern. These findings are in agreement with the findings of other investigations (Tveten 1976e; Crock and Yoshizawa 1977). The conclusion that, in comparison to the arterial system, a very different venous drainage pattern exists can therefore be confirmed. As outlined above, the basic pattern described exhibits regional variations that are conducive to divergent descriptions. In the lumbosacral region of the human spinal and to a certain extent in the cervical enlargement, central veins are similar in calibre and number compared to the arteries. In other regions, posteromedian veins of the septum are the largest and longest veins of the medullary transverse section (Kadyi 1889).

To accomplish drainage of the richly vascularized grey matter, the numerous, deeply extending radial veins form a system with greater capacity. Calculating the number and calibre of central arteries and veins, Kadyi (1889) had already pointed out that only some of the blood entering via the central arteries can return via the veins of the anterior fissure as the capacity in the venous "low-pressure system" with slow flow of blood must be higher by a factor of more than 2 compared to that in the arterial system. This stresses once more the opposition of a centrally dominating supply and a peripherally dominating drainage system.

### 3.9.2 Intrinsic Venous Anastomoses

Radiographic imaging of vascular anatomy, combining X-rays with tomographic sections in three planes, offers significant advantages for new insights into the number, localization and course of different types of intrinsic venous anastomoses, which were described in detail. Although venous anastomoses have been mentioned in some reports (Kadyi 1889; Herren and Alexander 1939; Crock and Yoshizawa 1977), other authors disputed them (Gillilan 1970; Tadié et al. 1985). As Tveten (1976) could not detect them in rats, he considered them to be random findings. Consequently, their physiological and pathophysiological importance has not been appreciated until now.

Kadyi (1889) describes diverse anastomoses between the central and the peripheral veins that allow drainage along several routes, yet his examples merely show the connections of smaller and medium-sized calibre. Herren and Alexander (1939) interpreted these centro-dorsolateral anastomoses as an arrangement to equalize venous pressure. The findings of our investigations support this view. Crock and Yoshizawa (1977) first mentioned a large midline communication between the main median trunks (type I). We had the possibility to examine a large variety of cases and, thanks to a novel technique of specimen preparation and my personal experience in X-ray examinations, we were able to image, understand and demonstrate the principles of extrinsic and intrinsic spinal cord arterial supply and venous drainage.

We are able to demonstrate that these anastomotic channels are still underestimated. They are frequent, they serve different needs and are therefore not randomly distributed over the length of the spinal cord. Whereas one type receives tributaries from the spinal cord, the second type does not. The constant calibre, mostly equal to that of the veins to which they connect, suggests them to be arrangements for pressure and flow adaptation. A rapid exchange between both of the large blood reservoirs anteriorly and posteriorly can occur through them. Furthermore, it can be assumed that the density in which they occur in the upper thoracic and cervicothoracic regions is related to the particular mobility of the spinal column in these regions. In contrast to the brain, the spinal cord must tolerate inner deformation under movements of the spinal axis. The draining vessels running on the surface are submitted to ensuing variations in volume and pressure. As can be seen in myelographic studies with maximal flexion and extension of the head, compression effects occur ventrally or dorsally, depending on the curvature of the spine, which probably affect the more easily compressed veins first, and the arteries later. Thus, if the ventral venous longitudinal tract is compressed by extreme movements, blood can be diverted dorsally not only through circular, superficial anastomoses but even more quickly and efficiently through the transmedullary anastomoses.

By means of this blood-deviating system, regional pressure differences in the veins are quickly adjusted, even under extreme hyperflexion of hyperextension. Also pathological conditions are compensated over long periods. Only a circular, collar-like constriction seems to be appropriate for an effective obstruction of venous drainage.

Our systematic radio-tomographic investigation of many spinal cord specimens support the conclusion that the predominantly radial arrangement of the intrinsic veins and the high number and variation of different anastomotic connections near the mobile segments of the spinal cord are one of the most characterizing features of spinal cord drainage. The anastomoses are locally adjusted to different requirements and protect venous drainage against circumscribed space-occupying effects as well as parenchymal deformation through movement.

### 3.9.3 Superficial and Radiculomedullary Veins

The anterior and posterior median spinal veins are only the most common superficial venous channels. The large blood-collecting anastomotic trunks can extend over the entire length of the spinal cord or they can be replaced or accompanied by antero- and posterolaterally located blood vessel tracts. In fact, they only represent the most noticeable longitudinally oriented components within a pial vascular network that is termed the "venous plexus of the pia mater" (Tveten 1976), "coronal (pial) plexus" (Gillilan 1970) or "venous pial plexus" (Crock and Yoshizawa 1977). Moes and Maillot (1981) presented a meticulous study on the superficial veins of the human spinal cord and for good reasons they added the subtitle "Essay of a systematization". The main reason is that deviations from the basic pattern are almost a rule instead of an exception and the changes in calibre and position of these veins along the longitudinal axis show a high interindividual variability. Looking at the numerous X-rays and photographs of contrast-filled specimens in this book, this statement should be convincing.

The clinical significance of the frequent varicosities of the venous pial plexus, especially on the dorsal side of the thoracolumbar enlargement, or of the extreme varicosity of a radicular vein shown in Fig. 3.32 remains unclear and unexplained.

Drainage routes of the superficial system run towards the inner extradural vertebral venous plexus via the anterior and posterior radiculomedullary veins.

### 3.9.4 Circulatory Disturbances of Venous Origin

Acute venous infarcts caused by spinal venous thromboses are considered rare. As a result of the lack of clinical criteria for such a diagnosis and because of the difficulties of post-mortem documentation, the low number of venous thromboses and phlebitides that are confirmed by autopsy must be considered with caution (Kulenkampff and Matheis 1961; Gruner and Lapresle 1962; Neumayer 1966; Hughes 1971; Rao et al. 1982; Kim et al. 1984). Disturbances in the venous section can hardly be distinguished from microcirculatory disorders.

In cases with local masses, venous drainage is only effectively obstructed by a circular constriction of the spinal cord, since the internal venous anastomoses allow for a change in direction of drainage. This is the reason why Doppman et al. (1979) failed in their attempt to produce spinal cord lesions by ligating the dorsal veins in rhesus monkeys. It further explains the switch of drainage towards the ventral system, which these authors could not interpret. Since intradural venous blood channels as protected as the cerebral sinus do not exist in the spinal canal, intramedullary or circular extramedullary masses lead to a compression of the superficial medullary veins after the subarachnoid space is consumed. Venous stasis then becomes relevant in addition to the primary process (tumour, trauma, inflammation, ischemia).

In case of a SDAVF, arterialisation of one of these veins at the site of dural penetration with flow backwards towards the perimedullary veins causes massive venous hypertension and in the long term severe damage of the spinal cord parenchyma (Foix–Alajouanine disease). The experience that spinal cord–draining veins may play an important pathogenetic role in vascular diseases created the expectation that chronic impairment of spinal venous drainage alone, in the absence of an arteriovenous shunt, could be the cause of important myelopathic conditions (Tadié et al. 1985; Aboulker et al. 1977; Merland et al. 1980; Thron 1988).

One of the two main aetiological concepts was the idea that contrary to the reported high numbers of radicular veins only a small number of the anatomically counted radicular veins definitely carry the venous return from the spinal cord (Tadié et al. 1985). To support this idea Tadié et al. define the restricted role of pure radicular veins and conclude that these considerably smaller veins of generally 0.1–0.2 mm diameter "do not play an important role in spinal venous drainage". Moes and Maillot (1981) argue with good reasons that vessel diameter should neither be the only nor the crucial argument to discern radicular from radiculomedullary veins. But Tadié et al. (1985) insisted on an average number of only nine to ten radiculomedullary arteries for the venous return of the entire spinal cord, compared to an average of about 50 in the majority of other investigations. But this low number would not only demonstrate high vulnerability, its capacity would principally be far beyond that needed for venous return.

Non-functional veins and narrowing of the veins in the transdural segment have not been taken into account in this assessment.

Therefore, the idea that possible diseases might result from impairment of venous drainage alone, in the absence of dural arteriovenous shunts (Sect. 3.4) has not received greater attention during the past three decades. Arguments that a low number of veins effectively draining the spinal cord should be responsible for chronic vascular myelopathies (Tadié et al. 1985) have not been substantiated.

The same is true for the second aetiological concept that possible malfunction of an assumed reflux-impeding device at the dural transit of radicular veins might occur. We must admit that we cannot measure normal or abnormal venous return from the spinal cord and imaging of parenchymal damage beyond the level of "subacute necrotizing myelopathy" is also not possible at the moment. But on the other hand we are not confronted with significant clinical consequences. It may be that there is a causal co-relationship between the high number of varicosities in and around the spinal cords demonstrated in cadaver studies of an older population and chronic impairment of venous drainage.

Our assured knowledge about the impact of circulatory disturbances in venous drainage is mostly restricted to our knowledge about the clinical impact of disclosed or undisclosed dural arteriovenous shunts. This impact is very high. And in numerous cases of unexplained hyperintensity of the spinal cord and progressive symptoms, failure to disclose the site of the pathological arteriovenous shunt was the real reason for a misdiagnosis. Missing experience in the necessary examination procedure or technical limitations were the concrete obstacles.

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© Springer International Publishing 2016

Armin K. ThronVascular Anatomy of the Spinal Cord10.1007/978-3-319-27440-9_4

# 4. Clinical Applications

Armin K. Thron1

(1)

Aachen, Germany

Only selected clinical examples and case studies are presented in this book. Mainly for didactic purposes but also with respect to the clinical impact, we prefer to present cases of spinal arteriovenous disorders that are particularly suited for a mental training in vascular anatomy of spine and spinal cord. Spinal cord arterial ischemia is discussed in Sect. 2.11. Analysing rare cases of suspected acute infarction of the spinal cord is important but troublesome, and the diagnostic problems encountered with acute spinal stroke cannot be solved satisfactorily within the scope of this chapter on clinical applications.

Therefore, this chapter offers the opportunity to analyse exemplary cases that have been diagnosed (and mostly treated) at our institution (Huffman et al. 1995; Thron and Caplan 2003; Thron and Mull 2004; Krings et al. 2006a; Thron and Krings 2007; Krings 2010). The selected clinical applications are restricted to five topics, beginning with normal vascular anatomy and the interpretation of some normal but unusual findings observed on clinical tomographic images. The second part deals with spinal arteriovenous malformations (SAVMs), the third with spinal dural arteriovenous fistulas (SDAVFs) and the fourth vertebrospinal and medullary vascular tumours. The final fifth part gives advice about how some of the repeatedly observed pitfalls in procedure and evaluation of spinal angiography can be recognized and avoided.

## 4.1 Applications in Normal Spinal Digital Subtraction Angiography and Interpretation of Uncommon Blood Vessels on Tomographic Imaging

By selective catheterization of the segmental arteries, the anterior radicular feeders of larger calibre and their continuation into corresponding segments of the anterior spinal artery can be demonstrated in the normal spinal cord in a high spatial and contrast resolution. Visualization of the posterior radicular feeders is also occasionally possible (Fig. 4.1). Visualization of longer vessel courses in selective digital subtraction angiography (DSA) is hampered not only by technical limitations of radiology but also by inflow of non-contrasted blood from other supply territories above and below. This is also why demonstration of the draining veins is difficult using this technique as long as only small amounts of contrast medium (approx. 2 ml) are injected. The disadvantages of this selective technique are not encountered with global blood vessel–contrasting techniques such as contrast-enhanced magnetic resonance angiography (ce-MRA) (Fig. 4.31). Therefore, combining both techniques means combining the advantages and disadvantages of selective and non-selective procedures (Fig. 4.37).

In the thoracolumbar region the great radicular artery can always be visualized in normal cases provided that a complete, selective spinal angiography is performed. Visualization of smaller radiculomedullary feeders (<0.2 mm) in other spinal cord regions can be a problem. Some examples from actual angiographic equipment are given in Fig. 4.1. In addition to potential feeders of the spinal cord, small branches to the homolateral hemivertebra, to the dura and to the nerve roots always issue from the segmental arteries (Figs. 2.5 and 4.1f). Attention has to be paid to the fact that the ventral branches of two intercostal arteries can arise from a common segmental stem. But the stem of the second segmental artery with the ramus spinalis of the dorsal branch should then originate separately from the aorta (see Fig. 4.1f, as well as Sect. 2.4 and Fig. 2.5 ). When looking for the feeder(s) of a spinal arteriovenous disorder (SAVM or SDAVF) or of spinal cord blood supply, one must take this situation into consideration.

It is widely assumed that a radicular artery and its continuation into a descending branch of the anterior or posterolateral spinal artery are easily identified by the typical "hairpin" course. Figure 4.2 exhibits an instructive example from clinical angiography reminding that the radiculomedullary veins may have an identical configuration.

Figures 4.3, 4.4, and 4.5 demonstrate that the superficial longitudinal trunks, their intrinsic anastomotic connections through a midline section of the spinal cord and the continuation of the anterior median vein to the filum terminale or to a deep sacral root are the largest blood vessels within the dural sac (1.5–2.0 mm). Additionally they have slow flow and are therefore together with the veins of the posterior venous plexus the spinal cord blood vessels most easily depicted on contrast-enhanced tomographic images.

Fig. 4.1

Spinal cord–supplying arteries in digital subtraction angiography. (a) Typical anterior feeder to the cervicothoracic region originating from one of the branches of the supreme intercostal artery. The ascending and descending branches, which are parts of the longitudinal anastomotic tract, called the 'anterior spinal artery', have equal calibre. (b) Anterior radiculomedullary arteries to the upper thoracic region may be very small (<0.2 mm) and can easily be overlooked (arrows). (c) Films in the late arterial phase may be helpful (arrows). The continuity of the anterior spinal artery may even be interrupted in this region. In this case the blood vessel cannot serve as an anastomotic tract between the cervical and the thoracolumbar enlargement. (d) Great anterior radiculomedullary artery (Adamkiewicz artery, arrows) supplying the thoracolumbar enlargement (reproduced from Thron 2008). (e) The unsubtracted image of d allows a better topical attribution of the segmental arteries, the extra- and intraspinal anastomoses and the anterior radiculomedullary artery to the osseous elements of the spine. (f) Great anterior radiculomedullary artery originating from one of two posterior intercostal arteries that have a common trunk in their origin from the aorta. The posterior intercostal artery with radiculomeningeal and medullary supply (hemivertebral blush and radiculomedullary branch) is a true segmental artery (T11). The other one represents only the ventral branch of the posterior intercostal artery T10. The dorsal branch of this segmental artery T10 should have a separate origin from the aorta. It has to be looked for if complete demonstration of radiculomeningeal and radiculomedullary supply is required (Sect. 2.2.2, Fig. 2.5). (g) Posterior radiculomedullary artery originating from the 12th posterior intercostal artery in anteroposterior (a.p.) view (arrow). Normal posterior feeders are generally only depicted well at the levels of the thoracolumbar enlargement. (h) Lateral view of the subtracted angiographic image. (i) Lateral view of the unsubtracted image clearly demonstrating the posterior position of the artery in the dural sac and vertebral canal

Fig. 4.2

Digital subtraction angiography of radiculomedullary arteries and veins. (a) Arterial phase of an angiogram of the great radiculomedullary artery. (b) Venous phase. The radiculomedullary vein is coincidentally observed at the same level. The hairpin course configuration alone does not help in the differentiation between artery and vein. In the case of an arteriovenous shunt disorder with early appearing veins, the time resolution of a dynamic sequence (e.g. in magnetic resonance angiography or computed tomography angiography) remains important for the evaluation of the angiogram (Courtesy of Prof. G. Schroth, Bern, Switzerland)

Fig. 4.3

(a) Venous midline anastomosis in a midsagittal microangiogram (arrow) (Reproduced from Thron 1988). (b) Lateral view of clinical spinal angiography at thoracic levels in a case of dural arteriovenous fistula. The configuration is typical for this type of midline anastomosis (arrow) (Courtesy of Prof. G. Schroth, Bern Switzerland)

Fig. 4.4

Large transmedullary midline anastomoses depicted in a clinical and a post-mortem examination. (a) Midsagittal section of contrast-enhanced magnetic resonance imaging (T1-weighted) (arrow). (b) X-ray of a contrast-injected spinal cord specimen in lateral view, which allows no differentiation between a superficial or intrinsic venous midline anastomosis (arrow). (c) Microangiogram of a midsagittal section from the specimen shown in b (arrow) (a Courtesy of Prof. D. Petersen, Luebeck, Germany; b, c Reproduced from Thron 1988)

Fig. 4.5

Vein of the filum terminale as continuation of the anterior median spinal vein in a clinical and a post-mortem examination. (a) Midsagittal section of a T1-weighted contrast-enhanced magnetic resonance image showing the superficial anterior (arrow) and posterior midline veins. (b) Microangiogram of a midsagittal section demonstrating the anterior median and the terminal vein and intrinsic central veins (Reproduced from Thron 1988)

## 4.2 Applications in SAVMs

### 4.2.1 Definition and Classification

Arteriovenous malformations (AVMs) are direct or abnormal connections between arteries and veins without an interposed capillary bed. In the case of intradural SAVMs, they are supplied by arteries supplying the spinal cord parenchyma (radiculomedullary arteries) and drained by spinal cord veins. Localization can be within the medulla spinalis or perimedullary on the surface. The arteriovenous transit of blood is fast and the resulting shunt volume is high. They are regarded as inborn lesions.

Vascular malformations of the spinal canal and its meninges are rare diseases that lead to damage of the spinal cord if not treated. Haemorrhage and circulatory disorders are the most frequent causes of damage, depending on the type of vascular disease. Space-occupying effects play a minor role. Following initial MRI, spinal angiography has to be performed with an adequate technique to define the exact nature of the lesion. This is a critical point because the type of lesion and the anatomical vascular details for both the lesion and the spinal cord are fundamental to the decision about the most appropriate therapy, which may be endovascular, neurosurgical, combined or attentive (Thron and Caplan 2003; Thron and Mull 2004; Krings et al. 2004, 2006a).

Topographically, vascular malformations of the head and spine can be found in extra- and intradural compartments. The dura mater may be involved in rare cases of these inborn diseases. But the dura mater itself is a place in which acquired shunts between arteries and veins occur. Those from the cranial meninges have been known for a long time. There, the established shunts lead arterial flow from meningeal branches commonly into the cranial dural sinuses. This makes the diagnosis easy. In the spinal canal dural sinuses do not exist, and the "hidden" arteriovenous shunt directly into the pial spinal cord veins may look like a true arteriovenous malformation if important details of vascular anatomy are disregarded.

Classification schemes for vascular malformations can be based on many different criteria. Parameters from histopathology, angiography, endovascular accessibility or genetic predispositions (Rodesch et al. 2002) may be selected for classification purposes. A generally accepted classification does not exist.

From an anatomical and clinical point of view it seems reasonable to establish a classification of spinal vascular malformations, which is similar to that commonly used for the brain and which separates the inborn malformations from the acquired lesions (Thron and Caplan 2003; Krings et al. 2005a, 2006a).

A classification of inborn spinal vascular malformations comprises

  * Arteriovenous malformations (AVMs) and

  * Cavernomas.

Capillary telangiectases are another form of inborn lesions frequently encountered in the brain and brain stem, but to our knowledge they have not been reported to occur in the spinal cord parenchyma.

Depending on the size and angioarchitecture of the nidus (which means the area of histologically undefined blood vessels between supplying artery and draining vein) and haemodynamics of a spinal AVM, the following angiographically defined subtypes have been introduced:

  * Spinal AVM subtypes

    * Fistula type 1–3 (perimedullary f.; 1 = small, 2 = medium, 3 = giant)

    * Glomus type (or nidus type; conglomeration of abnormal blood vessels)

    * Juvenile type (spinal AV metameric syndrome (SAMS)/Cobb syndrome)

AVMs of perimedullary fistula type are simple direct transitions of a dilated superficial artery into an arterialized vein. A frequent effect of the shunt is a dilated venous pouch or aneurysm at the recipient venous side (Figs. 4.6, 4.7, 4.8, 4.9, and 4.10). It may be very small (Fig. 4.6, type 1) or large and space-occupying (Fig. 4.10, type 3).

Djindjian et al. in 1977 were the first to describe perimedullary fistulas. Merland and his group distinguished three types, according to the vessel size, the shunt volume and the drainage pattern (Riché et al. 1983; Gueguen et al. 1987 ).

A spinal AVM of fistula type 3 (giant or macro-fistula) is now known as a neurovascular disorder typically associated with hereditary haemorrhagic telangiectasia (HHT) (Mont'Alverne et al. 2003; Krings et al. 2005b, 2005c). The macro-fistula consists of several arterial feeders, entering a solitary large venous pouch through a single hole (Fig. 4.10). The shunt volume is high and the draining vein is correspondingly enlarged.

AVMs of glomus type represent a frequent type which is characterized by a conglomeration of greatly dilated vascular masses (nidus) like in most cerebral AVMs. It may be located superficially on the surface of the spinal cord or deep within the cord parenchyma or may extend to both compartments. Owing to the numerous anastomoses between the spinal cord arteries, the nidus is always supplied by several arteries or branches derived from the anterior or posterior spinal arteries (Figs. 4.11, 4.12, 4.13, 4.14, 4.15, 4.16, 4.17, and 4.18).

AVMs of juvenile type comprise extensive AVMs and especially the metameric AVMs, involving all the structures of a given metamere, soft tissue, bone, dura and spinal cord (SAMS, Cobb syndrome, Klippel–Trenaunay, Parks–Weber syndrome) (Fig. 4.20).

In clinical practice, many spinal AVMs are complex vascular malformations. Mixed composition of fistulous and plexiform parts within the nidus (Fig. 4.19) is a frequent observation of superselective angiography.

It is important to keep in mind that—corresponding to the intracranial situation—AVMs of the intradural compartment of the spinal canal are supplied by spinal cord–supplying anterior and/or posterior radiculomedullary arteries and drained by radiculomedullary veins. In cases of dural arteriovenous fistulas the spinal cord–supplying arteries are not involved in the arteriovenous shunt.

Extradural AVMs or vascular tumours with possible intraspinal epidural extension are supplied and drained exclusively by extradural vessels (Fig. 4.41).

Only in the different forms of metameric angiomatosis segmental extradural and meningeal branches as well as spinal cord supplying arteries are invoved.

### 4.2.2 Angiographical Findings

Cases with intradural AVMs of the spinal cord correspond in principle to those of the brain, exhibiting a high variability in size, supply, shunt volume and drainage of the malformations. Several feeding vessels are usually involved which can be recognized as medullary arteries by their typical course. As a result of the AV shunts, their calibre can be extremely enlarged (Figs. 4.15, 4.19, and 4.20). The convolution of abnormal vessels, continuing as draining veins with enlarged calibre and thickened walls, can form an intra- and/or extramedullary mass (Figs. 4.15 and 4.18). AVMs typically show a rapid and high shunt into the draining vessels. Low shunt volume and diffuse staining are more suggestive of vascular tumours (Di Chiro and Doppman 1969; Vogelsang 1983) (Figs. 4.42, 4.44, and 4.45).

In exceptional cases combinations of haemangioblastomas and AVMs may occur. Aneurysms of the angioma feeders are an extremely rare finding. Instead, aneurysmatic dilations of the veins are more frequent (Djindjian 1978a; Cogen and Stein 1983) (Figs. 4.8 and 4.9). Venous drainage can variably proceed via all longitudinal systems and radicular paths of drainage.

The angiographical appearance of purely extradural AVMs of the spinal canal is variable. These vertebral or soft tissue haemangiomas may or may not extend into the epidural space. Since the X-ray image of a vertebral haemangioma is rather characteristic (Figs. 4.20 and 4.41), yet the spinal angiographies are diversified, Djindjian et al. (1981) differentiated three groups (A–C). In the most frequent case (type A) the supplying segmental arteries are not markedly enlarged and there is a heterogeneous, intensive vascular blush that exceeds the area of the hemivertebra. This persists into the late venous phase; early draining veins are not observed. Similar to an epidural tumour, intraspinal extension of the malformation may exert a compression effect on the spinal cord and its vessels. The combination with previously mentioned forms of spinal vascular malformations rarely occurs, with a rate of 4 % (Djindjian et al. 1981). This also applies to the combination of segmental angioma of the skin, vertebra and spinal cord, also known as Cobb syndrome or metameric angiomatosis (Fig. 4.20). Characteristic of the other forms of vertebral haemangioma is a weak, very irregular blush (type B), or a total lack of enhancement (type C) in the angiogram. According to angiographical criteria, vertebral haemangiomas are therefore often of the capillary venous type. However, if there is dilation of supplying vessels, as seen in Fig. 4.41, or early venous drainage, at least arteriovenous components are present. Such forms are more appropriate for endovascular therapy.

### 4.2.3 Conclusions

Intradural and extradural AVMs should be clearly distinguished from the dural AVFs draining via intrathecal veins.

While the pathophysiology of neurological deficits in cases of intradural AVMs includes steal phenomena (Kaufman et al. 1970), dural AV anomalies are pathogenetically effective only on the basis of increased spinal venous pressure (Aminoff et al. 1974; Kendall and Logue 1977; Symon et al. 1984; Hassler et al. 1989; Hurst et al 1995), because no arteries supplying the spinal cord are involved.

Fig. 4.6

SAVM of perimedullary fistula type 1 at the level of the medulla oblongata (C1/2). (a) DSA of the left vertebral artery. Descending branch of the V4 segment, non-fusion of bilateral tracts (arrow) with a small aneurysmatic formation at the fistula site. Draining vein (white arrowhead). (b, c) CTA with multidirectional view on the vascular malformation allows better evaluation of the anatomical architecture of the lesion. (d) T2w MRI, midsagittal section. Severe damage caused by haemorrhage in the region of the (venous) aneurysm at the fistula site and infarction of the cervical spinal cord

Fig. 4.7

SAVM of perimedullary fistula type 1 at low thoracic level (T12/L1). (a) Anterior radiculomedullary artery originating from the L2 level. Fistula point at T12/L1 level (black arrowhead) into irregular venous convolutions (white arrowhead) on the posterolateral surface. (b–e) Drainage is first directed downwards, finally upwards (c) without radicular outflow between L1 and T10. (f, g) T2w MRI in midsagittal (f) and axial sections (g) show remnants of haemorrhage at the fistula point (arrow). The pencil-shaped hyperintensity of the medulla corresponds to severe multisegmental myelopathic damage

Fig. 4.8

SAVM of perimedullary fistula type 2 at T12/ L1 level. (a) Great anterior radiculomedullary artery originating from L2 (small arrow). Venous ectasia or aneurysm at the fistula point (large arrow). (b) Drainage into a midline vein first downwards, then upwards (arrowheads) without radicular outflow between L1 and T9. With exception of the venous aneurysm at the fistula point, location, supply and flow direction of this SAVM are very similar to the case presented in Fig. 4.7 (Reproduced from Thron 1988)

Fig. 4.9

SAVM of fistula type 2 at T11 level. Radiculomedullary artery (upper small arrow) originating from the T11 posterior intercostal artery and anterior spinal artery which can be followed caudally to the AV shunt (lower small arrow). Venous aneurysm at the shunt site (large arrow) and irregularly dilated draining veins (arrowhead). Goal of therapy in all these cases is occlusion of the aneurysm and shunt with preservation of vessel patency in the course of the anterior spinal artery

Fig. 4.10

SAVM of fistula type 3 (giant), typically associated with hereditary haemorrhagic teleangiectasia (HHT). (a) DSA of the left vertebral artery in a.p. view depicts a large venous pouch. Several feeders from both sides (not shown) enter the pouch through a single hole (arrow). (b) Midsagittal section of T2w MRI shows the space-occupying pouch before treatment. High shunt volume results in enlarged draining veins. (c) Occlusion of the single hole with coils through the main feeder from the left vertebral artery. (d–f) DSA and MRI follow-up with controlled thrombotic occlusion of venous aneurysm and draining vein

Fig. 4.11

SAVM of glomus or nidus type located in the medulla oblongata. (a) Unsubtracted image of the right vertebral artery angiogram in lateral view. (b–d) DSA of both vertebral arteries in oblique projection. Supply of the AVM is derived from vertebral artery and mainly posterior inferior cerebellar artery (PICA) branches to the medulla oblongata on the right side (arrowhead). An additional anterior feeder to the AVM is the descending branch from the right V4 segment (arrow) (Courtesy of Prof. L. Solymosi, Wuerzburg, Germany)

Fig. 4.12

SAVM of glomus or nidus type in the upper cervical spinal cord parenchyma. (a, b) Anterior (open arrows) and posterior (small arrow) medullary feeders from the right vertebral artery share in the supply of the vascular lesion. Early draining vein (white arrowheads). (c) Intrinsic position of the AVM rather posterior than anterior. Anterior (open arrow) and posterior (small arrow) supply is better demonstrated on the lateral view. The early draining vein is the posterior midline vein (white arrowheads). (d) T2w MRI in a midsagittal section shows remnants of haemorrhage in the anterior part of the spinal cord at the C2 level (Courtesy of Prof. L. Solymosi, Wuerzburg, Germany)

Fig. 4.13

SAVM of glomus or nidus type in the cervical spinal cord parenchyma at the C5 level (large arrow). (a, b) DSA of the right vertebral artery, early arterial phase. Posterior supply from the radicular level C7 (small open arrow). Early opacification of the anterior median vein (white arrowhead). (c–f) DSA of the left thyrocervical trunk. Anterior supply from the radicular level C8 (small closed arrow). Early filling of the anterior median vein (white arrowhead) and drainage to the internal vertebral venous plexus. (g, h) DSA of the left vertebral artery. Posterior supply from the radicular C7 level (small open arrow), similar to the right side and early draining vein (white arrowhead). (i, j) T1w and T2w mediosagittal image with characteristic appearance of an intramedullary AVM and surrounding areas of oedema or gliosis. Concerning differential diagnosis of spinal haemangioblastomas please compare the inhomogeneous appearance of the AVM nidus with the tumour opacification shown in Figs. 4.43, 4.44, and 4.45

Fig. 4.14

SAVM of glomus type and low shunt volume at mid-cervical level. (a) DSA of the right vertebral artery. Exclusive supply through an anterior radiculomedullary artery. Faint and inhomogeneous opacification of the nidus (large arrow) via small branches of the anterior spinal artery (arrow). Apparently low shunt volume with no very early draining veins. Collaterals from the vertebral artery to the deep neck arteries depict a lower posterior radiculomedullary artery not involved in AVM supply (arrowhead). (b) The lateral view visualizes the very thin ascending branch (small arrow) not shown in (a). (c) Superselective injection near the nidus (large arrow) depicts the ascending branch (small arrow) and small veins draining to the epidural plexus (white arrowhead)

Fig. 4.15

SAVM of glomus or nidus type and high shunt volume at low cervical level. (a) DSA of the thyrocervical trunk in a non-subtracted image demonstrating the nidus at the medullary C6/7 level. (b, c) The anterior feeder is a radiculomedullary artery entering with the C8 root. The intense opacification of the nidus, early draining veins (white arrowheads) into the anterior venous system and immediate outflow to the epidural plexus (open arrow) indicate high shunt volume and possibly intranidal fistulous parts. (d) T2w mediosagittal section to facilitate topical orientation. (e–h) DSA of the left vertebral artery demonstrating essential posterior supply from the C7 radiculomedullary artery. A different posterior part of the nidus is filled and drainage is directed mainly to the posterior median vein (white arrowheads). Different arterial supply of parts of an AVM as shown by angiography does not imply that the nidus consists of separated compartments. It is often possible to occlude the complete AVM from a single source of supply

Fig. 4.16

SAVM of monocompartmental glomus type at the T3 level. (a) A posterior radiculomedullary artery at T4 on the right side is the main supply to the nidus (arrow). The anterior median vein is the main drainage route (arrowhead). (b) Contralateral injection at this level passes the nidus and visualizes posterior feeders from both sides (thin arrows). Only upon closer inspection can a third radiculomedullary artery be identified, originating from T4 on the left side (thick arrow). (c) In the course of embolization, performed from T4 on the right side, a left-sided control injection reveals the posterior feeder (thin arrow) and the anterior spinal artery, now clearly depicted above and below a not yet occluded part of the nidus (thick arrows). (d) T1w MRI demonstrating the thrombosed AVM at T3 level, but also (transiently symptomatic) thrombosis of the AVM-draining anterior median vein (see a), requiring intermittent anticoagulation

Fig. 4.17

Very similar case to Fig. 4.16 with the glomus type AVM suspended between two posterior spinal arteries from the T11 level (a) and only limited anterior spinal artery supply from T8 (b). This AVM again was monocompartimental and accessible through the main posterior feeder (T 11 on the right)

Fig. 4.18

SAVM of glomus type at the cone. (a) ce-MRA. (b–e) The great anterior radiculomedullary artery with the arcade around the cone (b, c) and posterior feeders originating from T11 on the left and L1 on the right (arrows, d, e) are the main feeders to the different parts of the nidus (white arrow). The arteries have typical configurations for anterior and posterior radiculomedullary feeders. f Improved visualization of the posterior superficial arterial network including transverse intercommunications in the course of embolization. Compare the demonstration of posterior tracts (black arrows), supplied from T11, in (e) and (f) (Reproduced from Thron 2008)

Fig. 4.19

SAVM at the T10 level without defined nidus. (a) ce-MRA. (b) T2w midsagittal MRI shows cord atrophy and numerous distended blood vessels, mainly arterialized veins all over the thoracic region. (c–h) The anterior (c, d) and posterior feeders (e–h) are only moderately enlarged compared to the massive dilatation of the superficial spinal cord veins. This suggests a rather fistulous composition of the malformation and possibly drainage obstruction

Fig. 4.20

Spinal arteriovenous metameric syndrome (SAMS) with predominant extradural manifestation. (a) X-ray film of the cervical spine in lateral view showing cystic lesions of the cervical vertebrae 3 to 5 and narrowing of intervertebral spaces. (b) Frontal (c) sagittal section of T1w MRI. A mass of flow-void structures (arrow) in extra- and intradural location involves several cervical segments with more infiltrating than space occupying effect. (d, g) Lateral view of both vertebral arteries in an early angiographic phase. Intense opacification of the AVM from vertebral artery branches of both sides. (e, f) AVM supply from segmental branches of the deep cervical and ascending cervical arteries (Reproduced from Thron 1988)

Fig. 4.21

Spinal AVM of the filum terminale presenting as a complex malformation. (a) Selective angiography of the 6th intercostal artery in a.p. and lateral view. The anterior spinal artery is unusually large for that spinal level (arrow, a). (b) The blood vessel can be followed downwards to the L5/S1 level. There, a second blood vessel returns the blood flow in cranial direction (open arrow). (c) Schematic drawing following evaluation of serial histological sections from the excised shunt area at L5/S1 as indicated in (b). (d–g) The complexity of the vascular AVM is much higher than could be expected from the limited spatial and contrast resolution of the angiogram performed in 1992. A large, abnormally thick-walled artery (a) and an arterialized dilated vein communicate just below the level of e. Below that level, the size of this artery drops drastically (c, f, g). A second abnormal artery and another small vein are present with continuous course (small A and B) and without change of calibre in this part. Below the shunt level, the large vein ends as a blind sac as demonstrated in c and g. The complex architecture with numerous involved blood vessels and the additional content of fat and fibrous tissue are in accordance with a true vascular midline hamartoma including an AVM (c–g Courtesy of Dr. Wilhelm Kueker, Institute of Neuropathology and Department of Neuroradiolgy, University Hospital Aachen)

Fig. 4.22

AVM of the filum terminale at the L4/5 level. Analysis of supply. (a) Great anterior radiculomedullary artery (arrows) originating from the T10 posterior intercostal artery. The enlarged and tortuous vessel can be followed downwards to the intersegmental L4/5 level as a dilated artery of the filum terminale. At this point reversal of flow through another blood vessel, the terminal vein, can be observed (curved arrow). (b) At the level of L2 on the left a posterior radicular artery can be demonstrated (arrowhead), which enforces the posterolateral spinal tract and contributes in this way to the opacification of the terminal vein (arrow). The anatomical connection is the arcade between anterior and posterior tracts around the cone. (c) At the L4 level on the right another source of AVM supply can be observed. Opacification of the terminal vein can again be demonstrated (open arrow). The anatomical connection must be a meningeal and nerve root–supplying radicular artery L4 (arrow) connected to the filum terminale and thus to the shunt area (curved arrow). (d) Lateral view of T10 DSA which shows only the haemodynamically dominating shunt supply from the anterior spinal artery (arrow) to the terminal vein (open arrow). (e) Unsubtracted angiographic image. (f) T2w MRI in a midsagittal section showing the abnormal vascular structures in the region of the cauda equina

## 4.3 Applications in Spinal Dural AV Fistulas

### 4.3.1 History and Definition

The studies on assumed SAVMs by Kendall and Logue (1977) followed by re-evaluations by Merland et al. (1980) had furnished evidence that one type of SAVM, the most frequent one (>70 %), had to be reconsidered. The vast majority of the malformations previously classified as dorsal retromedullary angiomas (Djindjian et al. 1963, 1975) had been shown to be pathological arteriovenous shunts with a fistulous arteriovenous communication lying on or within the meningeal coverings of the spinal cord (Fig. 4.24). Definition: SDAVFs are supplied by meningeal (dural) branches of segmental arteries and drained by spinal cord veins. Contrary to fistulous types of spinal intradural AV malformations, spinal cord–supplying medullary arteries do not participate in the supply of dural AVFs. There is a striking similarity in the angiographical characteristics of dural arteriovenous fistulas of the spinal dura mater and those of the cranial dura mater. But a widespread network of dilated meningeal arteries penetrating into the sinus, as for example in arteriovenous fistulas of the posterior cranial fossa, cannot occur spinally as no comparable dural blood conductors exist. It should be reminded that "one of the important differences between the meningeal coverings of brain and spinal cord is that the spinal dura mater is a single-layered membrane. It lacks the periostal component of the cranial dura mater. The inner layer of the cranial dura mater is continuous at the foramen magnum with the spinal dural sheath, which is seperated from the vertebral periostum by an epidural space", which is an actual and not only a potential space (Nolte 1999). In clinically symptomatic cases, the spinal dural AV shunt is located in a region where a radiculomedullary vein pierces the spinal dura, which forms their wall for a short stretch (Tadié et al. 1979, 1985; Thron et al. 2015). The primary venous recipient of the meningeal artery branch should either be a radiculomedullary vein or the internal vertebral venous plexus.

A radiculomeningeal arterial branch persists at every segmental level (Chap. ) but radiculomedullary arteries persist only at certain levels due to the embryonic desegmentation process. In the evaluation of symptomatic cases the arterial shunt volume is almost always directed to the superficial spinal cord veins, and not to the epidural internal vertebral venous plexus even though the two venous compartments are connected to each other (Sect. 3.7). With increasing experience we were able to realize a mixed involvement on the angiograms more often (Figs. 4.38 and 4.39). Explanations could be that drainage to the plexal epidural compartment as a primary drainage route is asymptomatic and tends to occlude. And in case it is a concomitant drainage route to radiculomed veins it might be found thrombotically occluded at the time of diagnosis. (Krings et al. 2006a, Thron et al. 2015).

Figure 4.27 demonstrates on histological serial sections direct transition of the dilated radiculomeningeal branch into an arterialized vein within the dura mater spinalis. In the histologically examined case of Fig. 4.26 the meningeal arterial feeder courses in the wall of the recipient radiculomedullary vein, before entering it's lumen. This type of AV shunt has been called a "fistula" because of the abrupt transition of a vein into an artery without interposition of a convolution of abnormal blood vessels. The recipient vein passes into normal paths of spinal drainage (Figs. 4.23 and 4.24).

From a therapeutic (endovascular or neurosurgical) point of view SDAVFs could be classified together with arteriovenous malformations as arteriovenous disorders of the spinal canal and its meninges. Indeed, they are the most frequent type of this disorder. But they should be classified as a separate entity. Like their cranial counterparts, SDAVFs are acquired lesions, although their aetiology and possible predisposing factors are not yet clear. They are pathogenetically different from AVMs and affect a different age and sex population. They are the clinically most serious type of spinal arteriovenous disorders characterized by progressive paraparesis and sphincter disturbances (Aminoff and Logue 1974; Koenig et al. 1989; Thron et al. 1987, 2003)

### 4.3.2 Localization

The localization of dural AV shunts corresponds to the dural exit of radiculomedullary veins. In 69 % of cases this is joint or near (<1 mm) the exit/entry of a nerve root in the dural sleeve lateral of the root (Otto 1990). In 31 % of cases radiculomedullary veins pass the dura at greater distance independently from the nerve roots. In 121 of our own clinical cases of SDAVF diagnosed until 2003 more than 75 % of fistulas were found in the thoracolumbar region (Thron et al. 2003). But all segments of the spinal axis including the pelvic region and the skull base are potential sources of dural AVFs with spinal drainage (Figs. 4.36 and 4.37). Nevertheless, it is surprising to note the rarity of published cases of cervically localized typical dural AVFs. In only one case from a series of 129 SDAVFs did we observe double spinal arteriovenous fistulas at the levels L1 on the right and L2 on the left side (Krings et al. 2004).

### 4.3.3 Aetiological and Pathophysiological Aspects

The term dural arteriovenous fistula is more appropriate for this most probably acquired disease than malformation or angioma, because these last two terms suggest inborn lesions. The epidural or dural vascular convolutions resemble arteriovenous malformations in histological sections (Fig. 4.27). The high age at manifestation suggests at least an acquired triggering mechanism like hypertension, inflammation, thrombosis or microtrauma. A possible morphological basis of these pathological shunts could be the AV anastomoses of the dura in the vicinity of the root sheaths, described by Vuia and Alexaniu (1969), or the "pelotons vasculaires", cluster-like vascular formations between arteries and veins mentioned by Manelfe et al. (1972) in their study on dural vascular supply.

The occurrence of physiological arteriovenous communications in the dura mater cranialis and spinalis is mentioned in old anatomical textbooks (Langer 1877) and in an anatomical study by Hammersen (1964). In our morphological and microscopic examinations of spinal dural AV shunts performed in the 1980s (Fig. 4.25), we observed a shunt-supplying artery running in the broadened wall of a radiculomedullary vein before opening into the lumen of the vein (Fig. 4.26). This could be assessed as an indication that the establishment of an abnormal arteriovenous shunt pathology might occur between a meningeal vasa vasorum and the blood vessel wall of the spinal cord drainig vein. In the transdural course of radicular spinal cord veins the regular layers of the venous blood vessels are replaced by meningeal tissue. This may be accompanied by unusually configured structural arrangements like in the bulge or nodular type in which the narrowed and sometimes split lumen is fibrotically encapsulated (Thron et al. 2015).

Aetiological concepts and pathophysiological considerations about impaired venous return from the spinal cord should revisit the anatomy and the haemodynamic role of the internal vertebral venous plexus, neglected in the past. Arteriovenous fistulous connections with these epidural venous spaces and secondary reflux into radiculomedullary veins are extremely rare observations (Krings et al. 2006b). But these observations may be important for aetiological and pathophysiological considerations, which differ from those which were discussed until now (Geibprasert et al. 2008; Krings and Geibprasert 2009).

### 4.3.4 Pathogenesis of Spinal Cord Damage

While the pathophysiology of neurological deficits in cases of intradural AVMs is complex and includes steal phenomena (Kaufman et al., 1979), dural AVFs are pathogenetically effective only on the basis of increased venous pressure, since arteries supplying the spinal cord are not involved (Aminoff et al. 1974; Kendall and Logue 1977; Symon et al. 1984; Thron et al. 1987; Hassler et al. 1989, 1994; Hurst et al. 1995). Mechanical factors such as compression of the cord by dilated, intrathecal veins are excluded by intraoperative findings.

In Fig. 4.24 intraoperative Doppler recordings and measurements of pressure in the spinal cord veins, close and more distant to the fistula site are presented. Measurements were performed before and after occlusion of the meningeal feeder. The results strongly support the pathogenetical concept that an increase in venous pressure and a diminished arteriovenous pressure gradient causes venous congestion, which means an intramedullary oedema due to impaired venous drainage (Hassler and Thron 1994). In the long-term chronic hypoxia leads to necrotizing myelopathy, a severe damage of the spinal cord, described by Foix and Alajouanine in 1926. The course of the disease is progressive. Irreversible paraplegia is the final stage, if the disease is not diagnosed and treated at an early stage (Koenig et al. 1989).

### 4.3.5 Angiographical Findings

Leptomeningeal branches of a segmental spinal artery empty abruptly into a radicular artery in the vessel segment crossing the dura mater. Flow is now reversed against the spinal cord and continues through superficial subarachnoid venous trunks (Fig. 4.28). Normally, these small radiculomeningeal rami only supply nerve roots and dura and are not displayed angiographically. Although they do not have significant calibres, the shunt leads to an arterialization and dilation of the recipient veins. These veins, which are the physiological superficial veins of the spinal cord, get dilated and elongated by reversed arterial flow and produce the impression of a true intradural AVM (Figs. 4.23 and 4.24). This explains initial radiological misinterpretations as a retromedullary angioma resulting in temporarily misguided treatment of this disorder.

Ascending or descending dural (leptomeningeal) branches of neighbouring segmental arteries can participate in the shunt, because anastomotic connections in the network of dura-supplying arteries are abundant. The localized character of the shunt is based on the fact that it usually connects to a single vessel on the inner side of the dura. This can be different if a short common stem of two or more radicular veins is affected (Figs. 3.35b and 3.38). The estimated shunt volume is extremely variable. The progressive filling of draining veins may exhibit a relatively slow flow even in cases with apparently large shunt volume. Drainage can be observed running cranially and/or caudally at the same time over quite a distance (Figs. 4.32 and 4.33). Even repeated changes in upwards/downwards flow direction can be seen associated with a change of the longitudinal trunks that were used (Fig. 4.35). In an initial evaluation of our first 20 cases (Thron 1988, p. 86) the shunted blood was received and transported more often by the dorsal veins. However, a switch to the ventral side (or vice versa), using the external and intrinsic venous anastomoses could also be observed (Figs. 4.34 and 4.35). There was a tendency of fistulas at low levels (S3–T11) to drain upwards and of high thoracic levels to go downwards. The fistulas at intermediate thoracic levels all drained in both directions. A fistula at the lumbosacral level primarily involves the terminal vein or a sacral radicular vein (Figs. 4.37 and 4.39).

Often, outflow to the extradural plexus is not apparent over a long distance and drainage can be observed from the lumbar region to the cervical or cranial area (Fig. 4.35). Merland et al. (1980) were the first who suspected a second angiographic characteristic of SDAVFs: outflow via radicular veins of neighbouring segments seemed to be impaired or missing, when compared with the large number of radiculomedullary veins which had been counted in normal anatomy.

The explanation might be an overload of the venous drainage capacity by the shunt volume. But this contrasts with the even larger shunt volume in cases of SAVMs. More likely is an individually restricted drainage capacity in the thoracic region, caused by a primary or secondary veno-occlusive disease.

### 4.3.6 Diagnostic Management

The dural fistulas are rare, but they are the most frequent and the most devastating form of a spinal arteriovenous disorder in an unselected population (Koenig et al. 1989; Thron and Caplan 2003). Therefore they have to be regarded as one of the greatest challenges for neuroradiologists.

Meanwhile, MRI has become an early screening method with reliable findings in case of clinical suspicion. The results of ce-MRA can serve as an indicator of the shunt site (Backes et al. 2004; Mull et al. 2007). This allows more localized, not necessarily complete angiography along the spinal axis, which is helpful considering that the average patient age is over 60 years. Should the angiograms be negative in the suspected region, completion must be attempted, since arterialization of the spinal veins can occur from the sacral end of the dural sac into the terminal vein (Merland et al. 1980; Burguet et al., 1985) (Fig. 4.37) or from fistulas localized at the skull base (Woimant et al. 1982; Reinges et al. 2001) (Fig. 4.36). In this context it should be reminded that the segmental (radicular und dural) supply to the fifth lumbar level is derived from the iliolumbar artery, a branch of the internal iliac artery. When indicated, it should be injected selectively. Even in case of complete but negative selective spinal and cranial angiography, repetition should be taken into account if the suspected diagnosis of a dural fistula is strongly supported by clinical data and imaging results. In our opinion, the serious clinical consequences of a missed diagnosis of SDAVF justify or even require this management. Following this strategy we were increasingly successful over the years in quite a lot of cases.

But with increasing sensitivity of screening methods, especially ce-MRA, the number of these cases will drop considerably and be restricted to singular cases of low volume shunts.

### 4.3.7 The Question of Chronic Myelopathies in the Absence of AV Shunt Disorders

The experiences gained by selective spinal angiography in the late 1970s and the 1980s have taught clinicians in the neuro-disciplines that the superficial spinal cord–draining veins may play an important pathogenetic role in vascular diseases of the spinal cord, like in SAVMs and different forms of spinal arteriovenous fistulae (SAVF), mainly the dural ones (SDAVFs). Aboulker et al. (1977) and others (Merland et al. 1980; Tadié et al. 1985; Thron 1988) attempted to explain a group of chronic myelopathies by venous intraspinal hypertension caused by deficient venous outflow or disturbed reflux control from potentially increased pressure in the epidural plexus (Sect. 3.7, 3.9.4). But clinical experience gained over the last 30 years has not provided new evidence for this assumption.

Among investigators of spinal cord blood vessels it was generally accepted that spinal cord veins cannot be filled with blood or any other fluid by injection from the outside of the dura mater. The nature of this reflux-impeding mechanism has been a matter of dispute. Studies by Tadie et al. (1979, 1985) excluded the presence of valves and demonstrated instead an anti-backflow system resulting from narrowing and zigzagging of the vein while crossing the dura mater. We confirmed these results and presented a second arrangement in the dural segment of radiculomedullary veins, which might be appropriate to modulate flow (Thron et al. 2015). van der Kuip et al. (1999) and Groen et al. (1997) had no problems to achieve retrograde filling of the radicular veins in a post-mortem study following thorough preparation of the cadavers with infusion of saline containing a thrombolytic agent. They concluded that reflux could be considered to be a physiological phenomenon.

### 4.3.8 Open Questions

One of the open questions in the probably acquired dural AV shunt, is the surprising fact that blood flow is almost always directed against the spinal cord and not into the compartments of the internal vertebral venous plexus.

But the predominant compartment structure of the blood pools of the internal vertebral venous plexus in the microangiograms (Figs. 3.42–3.44) underline the hypothesis that in the vast majority of SDAVFs an initially arterialized compartment of the epidural plexus becomes spontaneously occluded.

But in the meantime some clinical cases of all these variations have been reported (Krings et al. 2006b; Figs. 4.34, 4.38, and 4.39). To our knowledge, only a few reports exist about clinically symptomatic arteriovenous fistulas with the flow primarily directed to the epidural plexus (Chen et al. 1977; Cognard et al. 1995 and Pirouzmand et al. 1997). All of these cases, except one (Chen et al. 1977), had secondary obvious reflux from the epidural plexus to the superficial spinal cord veins, as demonstrated by angiography. This is a strong argument for the paramount impact of AV shunts to generate clinically significant impairment of venous outflow. The clinical impact of disturbed reflux control is uncertain. The functional role of the probably predominant epidural venous plexus for the spinal cord blood circulation remains poorly understood.

Fig. 4.23

Photographs of findings at surgery. (a) View on the posterior surface of the spinal cord. The elongated and very tortuous blood vessel is the regular posterior median spinal vein, secondarily enlarged as a result of arterialized flow. (b) Enlargement of the veins (open arrow) starts at the inner surface of the dura mater with a circumscribed dilatation at the point where the vein crosses the dura (arrow). In the short segment of transdural exit, the vein is entered by small radiculomeningeal arteries (Courtesy of Prof. Grote, Department of Neurosurgery, University of Tübingen, Germany) (b Reproduced from Thron 1988)

Fig. 4.24

Illustration of operative findings in a case of spinal dural AVF. Doppler recordings of leptomeningeal feeder and draining vein as well as measurements of venous pressure in the spinal cord veins at different distances from the fistula point are demonstrated before and after shunt occlusion (70 mmHg versus 45 mmHg) (Courtesy of Prof. Hassler, Department of Neurosurgery, University of Tübingen, Germany)

Fig. 4.25

Dural segment of an arterialized vein (aV). Histological section of the excised shunt area in case of spinal dural AVF. Oblique passage of the arterialized vein through the dura mater (D). Only marginal narrowing of the blood vessel in its transdural course (arrows). The entry of the artery into the vein is not shown on this section (van Gieson staining, original magnification ×40) (Courtesy of Prof. Roggendorf, Department of Neuropathology, University of Tübingen, Germany)

Fig. 4.26

SDAVF with an artery running in the broadened wall of the arterialized vein before entering it. Histological sections of an excised shunt area. (a) A small artery is enclosed in the broadened wall of an arterialized vein (arrow) (previous vasa vasorum?). (b) In the area before the shunting artery opens, the composition of the vessel wall becomes irregular with splitting of the internal elastic lamina and marked fibrosis of the tunica media (arrow). The arterialized vein (aV) shows a considerable increase in elastic fibres and smooth muscle cells. (c, d) The lumen of the artery has opened into that of the vein. Elastic fibres from the arterial wall now form the bottom of the resulting groove (arrow) (van Gieson staining) (Courtesy of Prof. Roggendorf, Department of Neuropathology, University of Tübingen, Germany)

Fig. 4.27

(a–c) Transition of a dural artery (A) in the dural segment of a radiculomedullary vein (V). Histology of an excised shunt in a case of spinal dural AVF. Series of histological sections with staining of the internal elastic lamina reveal the direct transition of a dural artery into the dural segment of an abnormal radicular vein (small arrow in b; large arrow in c). The artery is characterized by the internal elastic lamina (small arrow in c). The arterialized vein shows a thickened wall with scattered elastic fibres (open arrow in c). A glomus-like formation (G) is situated close to the communication point (small arrow in b, large arrow in c). E epidural space, I intradural space, D dura mater. Elastica van Gieson staining. (Courtesy of Prof. Roggendorf, Department of Neuropathology, University of Tübingen, Germany) (c Reproduced from Thron 1988)

Fig. 4.28

DSA of SDAVF at T7 level with high shunt volume. (a) A network of dilated radiculomeningeal arterial branches (arrow) supplies the arteriovenous shunt. (b) Drainage passes the radiculomedullary vein to the longitudinal midline trunk and is directed up- and downwards (white arrowheads). An intradural spinal AVM can be excluded because no spinal cord–supplying arteries are involved in this arteriovenous shunt disorder. The shunt site has to be looked for at dural level of T7. DSA digital subtraction angiography, SDAVF spinal dural arteriovenous fistula

Fig. 4.29

DSA of SDAVF at T5 level. In this case two different longitudinal veins are opacified simultaneously (white arrows) at the shunt site (black arrow). This is certainly caused by the presence of a short common stem before the radicular veins exit the dural sac, as shown in the morphological and radio-anatomical examples of Figs. 3.32a, 3.35b, and 3.38. The diagnosis of SDAVF (and not SAVM) is based on the fact that a spinal cord–supplying artery is obviously not involved. DSA digital subtraction angiography, SDAVF spinal dural arteriovenous fistula, SAVM spinal arteriovenous malformation (Reproduced from Thron 2008)

Fig. 4.30

DSA of SDAVF at the L3 level. (a, b) Subtracted images in a.p. view. (c) Unsubtracted in lateral view. (a) The blood vessel that is opacified first (white arrow, question mark) resembles a radiculomedullary artery. It runs upwards to the lumbar enlargement and shows a hairpin configuration. (b) On later images it branches into typical venous tracts (white arrows). Furthermore, a focal change of calibre in the course of the superficial vessels, indicating an arteriovenous shunt, does not exist. Therefore, the presence of a SAVM of perimedullary fistula type can be ruled out. All of intradural blood vessels are veins and the shunt has to be localized in the dura mater at L3 (black arrow). (c) Ventral position of this lumbar vein L3 on the surface of the spinal cord (white arrow). Compare with the anatomical examples given in Figs. 3.11a and 3.31. The configuration of a radiculomedullary vein can be very similar to that of an artery and in case of an AV shunt careful analysis and high time resolution of dynamic angiographic series are helpful. DSA digital subtraction angiography, SDAVF spinal dural arteriovenous fistula, SAVM spinal arteriovenous malformation (Reproduced from Thron 2008)

Fig. 4.31

Contrast-enhanced spinal magnetic resonance angiography (ce-MRA) (a, b) and selective spinal digital subtraction angiography (DSA) (c, d) in the screening and diagnostic evaluation of suspected spinal arteriovenous disorders, exemplified with a spinal dural arteriovenous fistula (SDAVF) at T10 level

SDAVFs can occur principally at each segmental level of the spine from the base of the skull down to the end of the spinal canal. ce-MRI has turned out to be an imaging technique not only helpful to support or exclude the suspected diagnosis of the presence of a spinal AV shunt but also to localize the lesion at least roughly, if not exactly, like in the presented example. The technique is very sensitive in depicting the early filling of veins and of venous flow in general. Thus, selective spinal DSA can be focused on the region of interest and complete the diagnostic evaluation with details concerning topographical and differential diagnostic aspects required for assured diagnosis and safe treatment. It offers the advantage of selectivity and of high temporal and spatial resolution, often necessary to differentiate the many forms of slow or fast flowing AV shunt lesions and of feeder identification. A questionable alternative to MRA may be offered by spinal CT techniques.

Fig. 4.32

Selective spinal angiography of a spinal dural AVF at the T12 level with abnormal drainage to cervical and cranial levels. (a) The dural AV shunt is located in the intervertebral foramen T12/L1 (arrow). Ascending drainage via a radiculomedullary vein (arrowheads) and the superficial veins of the spinal cord. (b) No significant radicular outflow in the thoracic region. (c) The draining veins can be followed up to the cervical and craniocervical region. Only at mid-cervical levels, the anteromedian vein (arrowhead) partly empties into the internal vertebral venous plexus (arrows) (Reproduced from Thron 1988)

Fig. 4.33

Selective spinal angiography of a spinal dural AVF with abnormal drainage preferentially in caudal direction. (a) Arterial shunt occurs through the radiculomeningeal branch of the fifth intercostal artery. (b, c) Drainage can be observed in the descending and to a lesser degree in the ascending direction. (d) The serial angiogram at 19 s visualizes opacification of the terminal vein in the lumbar region. (e) The most impressive finding on myelography is the dilated terminal vein (arrows) far below the shunt localization (Reproduced from Thron 1988)

Fig. 4.34

Digital subtraction angiography of SDAVF at the T12 level showing large anteroposterior venous anastomoses directing blood flow to different drainage routes. (a, b) Subtracted and unsubtracted image of the shunt region. The vertical circumscribed contrast accumulation between the meningeal feeder and the draining vein (white arrowhead) probably corresponds to a minimal involvement of parts of the epidural plexus (arrow). (c, d) Tortuous superficial longitudinal trunks (white arrowheads) interconnected by large presumably midsagittal anastomoses (arrows). Thus drainage can be directed to different routes

Fig. 4.35

SDAVF at the L2 level with repeating reversal of upward and downward flow direction and typical MRI appearance of "necrotizing myelopathy" as long-term damage of this disease. (a–f) Digital subtraction angiography in a.p. (a, b) and lateral view (c–f). The early flow direction is upwards (a, b). At the T11/12 level a proportion of this flow passes through an intramedullary anteroposterior anastomosis of typical configuration to go downwards (c–e). At the L1 level there is again reversal of flow direction of this flow component. Finally (e, f), blood is distributed to anterior and posterior superficial spinal cord veins draining cranially (white arrowheads). (g) T1w ce-MRI with typical enhancement of dilated, relatively slow flowing superficial spinal cord veins. The spinal cord volume may be increased in subacute cases. Intrinsic central enhancement of the spinal cord parenchyma indicates subacute–chronic hypoxic damage caused by disruption of the "blood–spinal cord barrier". Unfortunately, neoplasm is an occasional misdiagnosis resulting from these signs. (h) T2w MRI with flow-void vascular structures in the cerebrospinal fluid around the spinal cord and central parenchymal hyperintensity due to oedema and infarction

Fig. 4.36

Dural AVF at the skull base near to the foramen magnum with perimedullary drainage. (a) X-ray in lateral view, unsubtracted image. Injection of contrast medium into the left ascending pharyngeal artery and opacification of a vein at the posterior C0/C2 level are visible (white arrow). (b) Subtracted image in lateral view. Posterior meningeal branches of the artery communicate with a short segment of the marginal sinus (black arrow) before connection with the posteromedian spinal vein is evident (white arrowhead). (c) Downwards flow within the posterior subarachnoid space can be seen (white arrowheads) far below the cervical region. (d) T2 w mediosagittal MRI shows signs of parenchymal damage (hyperintensity) and abnormal blood vessels as dark flow-void dots within the bright cerebrospinal fluid

Fig. 4.37

Fistulous AV shunt at S1 level between a meningeal sacral branch from the internal iliac artery to the terminal vein. (a, b) T2w and ceT1w MRI. The MRI aspect is like in SDAVF with involvement of the terminal vein. (c) ce-MRA. The localization of the lesion at S1 (arrow) and the direction of flow in the terminal vein (white arrowhead) are not unambiguously clear on tomographic or angiographic MR images. The shunt might be localized everywhere between low thoracic and sacral levels and drainage could go downwards, upwards or in both directions. Therefore, the high resolution of conventional angiograms in space and time remains important. (d, e) The main feeder to the AV shunt (arrow) as demonstrated by selective DSA is a dural branch from the internal iliac artery (small arrow). Draining veins (white arrowheads). Additional small meningeal branches to the AV shunt are not shown

Fig. 4.38

SDAVF with involvement of the epidural internal vertebral venous plexus. (a) DSA image in the early arterial phase visualizes the AV communication (small black arrow) with draining vein (white arrowhead) but also a small accumulation of contrast medium in a vertical line (white arrow), presumably in epidural localization (cf. Figs. 4.3 and 4.10a). (b) In the late arterial phase progressive filling of the superficial spinal cord veins and the epidural compartment (white arrows) are clearly demonstrated. Filling of both venous systems seems to occur simultaneously, but with higher flow rate into the intrathecal veins than in the epidural venous compartment. (c, d) Subtracted and unsubtracted early image of DSA in lateral view showing the shunt localization at a posterior radiculomedullary vein (white arrowhead) and early opacification of the epidural component (white arrow)

Fig. 4.39

Spinal epidural AVF with secondary remote reflux into perimedullary veins. (a) DSA of the third lumbar artery on the right depicts a shunt to anterior parts of the internal vertebral venous plexus on the right side (white arrowhead). Collateral filling of L2 on the left shows the great anterior radiculomedullary artery originating from this level and side (arrow) as an incidental finding. (b) Progressive filling of other parts of the anterior internal vertebral venous plexus first downwards, then again upwards (white arrowheads) results in entering of a radiculomedullary vein on the opposite side (white arrow). (c) The lateral view of a late venous image demonstrates the extension of involvement of the anterior epidural plexus (arrowhead). The irregular lacunar spaces do not form a homogenous or completely symmetrical venous drainage system with transverse communications at each level. The perimedullary draining veins indicate that a postulated reflux-impeding mechanism is not effective or is non-existent in this case. (d, e) T1w and T2w MRI with typical signs of SDAVF with congestive and necrotizing vascular myelopathy. (f) ce-MRA shows epidural (arrowhead) and intrathecal abnormal findings (arrow) without context

Fig. 4.40

Anterior spinal artery and SDAVF originating from the same segmental artery (L1 on the left). Comparison of findings in ce-MRA (a, b, e) and DSA (c, d, f, g). The arrows point to the normal anterior spinal artery in a coronal (b) and oblique sagittal target MRA image (e). The arrowheads mark the arterialized posterior veins of the SDAVF in all figure parts. The corresponding DSA images in a.p. view are presented in c and d. DSA comparison in lateral view in an early and late angiographic phase is given in f and g (a, b, e–g Reproduced from Mull et al. 2007)

## 4.4 Applications in Vertebrospinal and Medullary Vascular Tumours

Purely extradural AVMs of the spine may have quite variable angiographic presentations. These vertebral or soft tissue haemangiomas may or may not extend into the epidural space. Similar to a progressively expanding epidural tumour, intraspinal extension of some of these malformations may exert a serious and clinically relevant compression effect on the spinal cord (Fig. 4.41). This may require endovascular devascularization combined with surgical decompression. The X-ray image of vertebral haemangiomas is rather characteristic (Figs. 4.20a and 4.41a), yet the spinal angiographies are diversified. Djindjian et al. (1981) differentiated three groups (A–C). In the most frequent case (type A) the supplying segmental arteries are not markedly enlarged and there is a heterogeneous, intensive vascular blush that exceeds the area of the hemivertebra. This persists into the late venous phase; early draining veins are not observed. The combination with previously mentioned forms of spinal vascular malformations rarely occurs, with a rate of 4 % (Djindjian et al. 1981). This also applies to the combination of segmental angioma of the skin, vertebra and spinal cord, also known as Cobb syndrome or metameric angiomatosis. Characteristic of the other forms of vertebral haemangioma is a weak, very irregular blush (type B), or a total lack of enhancement (type C) in the angiogram. According to angiographical criteria, vertebral haemangioma therefore often belong to the capillary venous type.

The non-expanding vertebral haemangiomas are a frequent incidental finding at autopsies and spinal MRI.

The angiographical appearance of the other intra- and extramedullary tumours (ependymomas, neurinomas, meningiomas) and of vertebrogenic tumours (sarcomas, chondromas, osteochondromas, aneurysmatic osseous cysts, giant cell tumours, metastases) does not facilitate the differential diagnosis of the tumour type in the majority of cases (Voigt et al. 1978; Djindjian et al. 1981). Nevertheless, indication of the benign or malignant nature of a lesion may be provided by demonstration of pathological vessels, arteriovenous shunts as well as by the extent and type of tumour blush (Fig. 4.42).

In addition, spinal angiography supplies preoperative information on the degree of vascularization and the source of arterial supply of the tumour, plus the very important indication as to origin and possible displacement of anterior radicular arteries supplying the spinal cord. The risk of a "vascular catastrophe" during surgery can be diminished and the feasibility of preoperative or palliative embolization can be estimated.

Although MRI and spinal CT have decisively improved the diagnostics of vertebrospinal masses, spinal angiography can be helpful and even mandatory as a supplementary diagnostic method. Compared to the glomerular types of AVMs, low shunt volume and diffuse staining are more suggestive of vascular tumours like haemangioblastoma. This is a vascular tumour characteristic as part of the inherited von Hippel–Lindau syndrome. These vascular tumours of intraparenchymal localization in the spinal cord (15 %), medulla oblongata (5 %) and cerebellum (80 %) are supplied by brain- or spinal cord–supplying arteries of the region in which they become manifest (Figs. 4.43, 4.44, and 4.45). Therefore, the potentials of preoperative embolization are limited if damage to the spinal cord prior to surgery should be avoided. Spinal cord–supplying arteries can be studied in angiographies of these tumours because they are prominent, but preoperative embolization carries a separate risk. The neurosurgeon at our hospital did not demand preoperative embolization. He surgically isolated the angiographically well-described lesion before taking it out and followed his own advice:" do not cut in it before!".

Fig. 4.41

Vertebral haemangioma with epidural extension. Significant progressive space-occupying effect on the spinal cord. (a) Myelography of the thoracic region. The X-ray demonstrates the typical honey comb appearance of the involved bony vertebral structures. Circular compression of the dural sac and its content with subtotal block is evident, but no signs of an intradural vascular malformation. (b) Selective angiography of the ninth intercostal artery on the right shows descending supply with multiple feeders and an early homogeneous blush. The left ninth intercostal artery participated in the supply to a lesser degree (not shown). (c) Selective angiography of the tenth intercostals artery with a more inhomogeneous blush, clearly exceeding the normal hemivertebral area of supply. Again, additional supply could be demonstrated from the contralateral segmental artery (not shown) (Reproduced from Thron 1988)

Fig. 4.42

Intraspinal neurinoma demonstrated by digital subtraction angiography. (a) A.p. view of the circular hypervascularized mass (large open arrow). It is supplied by an anterior and posterior radicular artery, both emerging from the tenth intercostal artery on the right. The posterolateral spinal artery (small arrow) carries the main tumour supply resulting in an increase of vessel lumen. Both arteries (small and large closed arrows) can be discriminated by the position of the top of the hairpin curve and the position of the descending branch above the mass. At tumour level both arteries are considerably displaced to the left border. (b) Late phase with tumour blush and draining veins (open arrow). Drainage is in time. (c) Lateral view. Better discrimination of position and calibre of anterior and posterior spinal arteries (large and small arrow)

Fig. 4.43

Solitary haemangioblastoma demonstrated by digital subtraction angiography. Several spinal cord arteries from different levels and both sides share in the supply of the vascular tumour at the T9 level. Posterior spinal arteries from T10 and T11 of the right and T10 of the left side contribute to the tumour blush (a, b, d) as well as the anterior spinal artery from T9 on the left side (c). The strongest and largest diffuse opacification of the mass is observed via the segmental feeder T10 on the left. The shunt volume is lower compared to AVMs (e)

Fig. 4.44

Multiple haemangioblastomas in von Hippel–Lindau syndrome. (a, b) Digital subtraction angiography at the levels T6 on the right and T3 on the left side. Together with the opacification of either posterior (a) or anterior (b) spinal cord–supplying arteries, the numerous vascular tumour nodules are distinctly visualized. (c) T1w ce-MRI in a midsagittal section shows the scattered bright tumour formations accompanied by extensive dark perinodular cystic formations

Fig. 4.45

Cervical haemangioblastoma demonstrated by digital subtraction angiography in early and late arterial phase. Differential diagnosis of a cervical arteriovenous malformation (AVM). (a, c) Intensive opacification of the vascular tumour supplied by an anterior feeder from the vertebral artery (black open arrow) appears very early. (b, d) In late arterial phase, an early draining anteromedian vein in the lateral view indicates a rather high shunt volume (d, white arrowheads) In a.p. view a short time later (b) advanced outflow of the anterior median vein (white arrowheads) to the internal vertebral venous plexus (white open arrows) has occurred. Differential diagnosis of glomerular types of AVMs on the basis of angiographic criteria alone can only refer to the diffuse, more or less homogeneous "tumour-like" opacification (cf. Fig. 4.15)

## 4.5 Potential Pitfalls in Spinal Angiographic Examinations and Evaluations

Standards of image acquisition in spinal DSA and potential pitfalls in the anatomical evaluation of blood vessel anatomy mainly in spinal arteriovenous disorders should be mentioned and critically commented on.

1.

Imaging of feeders in two planes. Correct image interpretation requires sufficient information from the provided images. This sounds self-evident. But in our experience spinal angiographies are often performed in only an a.p. view and sometimes even without presenting an unsubtracted image. If ever possible, one of additional planes from the diagnostically important series should be a definitely lateral one. Prior to a therapeutic intervention, but even for diagnostic purposes, it is essential to identify the feeders of a spinal AVM from both the anterior and posterior circulation. On the basis exclusively of an a.p. view this can be difficult because of space-occupying effects or scoliosis. Figures 4.15 and 4.42 illustrate the different configuration of the hairpin curve in anterior and posterior radiculomedullary arteries. This is additionally helpful. Nevertheless, it is essential to have a lateral projection for an assured identification. This also facilitates identification of a spinal cord–supplying artery originating from the same pedicle (Fig. 4.40).

2.

Selective injections with good intra-arterial placement of the catheter tip. Another technical aspect for not being able to localize the feeder and shunt site of a suspected SDAVF is missing selectivity of the angiographic vessel injections. An exemplifying case is the pelvic dural fistula shown in Fig. 4.37. In case of an SDAVF at the L5 level neither the global injection of the abdominal aorta nor the demonstration of the pelvic vessels from the injected internal iliac artery demonstrated the fistula. Only selective injection into the iliolumbar artery was successful. Today, in the majority of cases, ce-MRA is helpful in localizing at least the region of the AV shunt, so that selective or superselective injections can be restricted to this area. But selectivity is needed to identify the therapeutic target.

3.

The diagnostic challenge of "spinal varicosis". Varicose convolutions, more frequent on the posterior than on the anterior surface of the spinal cord, are not unusual (Figs. 3.31, 3.32, and 3.33). Even extreme varicosities of radiculomedullary veins like in Fig. 3.32d may be observed as incidental findings. The term "spinal varicosis" was frequently used in the older neuropathology literature and in the evaluation of myelograms. Even today, accentuation of plexiform veins on tomography images may cause confusion with regard to the differentiation between a normal and a pathological finding. In cases of doubt, especially if combined with clinical findings that substantiate suspicion of an AV shunt disorder additional adequate examinations are necessary.

4.

Distended vein of the filum terminale or of a sacral radicular vein (Figs. 4.5, 4.21, 4.22, 4.30, 4.33, and 4.37). As pointed out in Sect. 3.2.1 a sacral radicular vein may assume the function of the terminal vein, which may be an impressively strong normal blood vessel (Fig. 4.5). Enlargement of this important drainage at the lower end of the vertebral canal or increased flow is noticeable in modern MRI and ce-MRA examinations. But until now, the underlying disease of a suspected AV disorder has to be clarified by selective angiography. Flow can be directed downwards from an AVM on the myelon or from a dural shunt. Flow can be directed upwards from an AVM at the filum terminale or from a dural shunt at lumbosacral levels. Both situations have to be checked thoroughly. It is important to understand that the AV shunts of the filum terminale are true pial AVMs with main but not exclusive supply from spinal cord–supplying arteries. In contrast, DAVFs at sacral levels are exclusively supplied by leptomeningeal arteries. The feeders may be derived from different sources. Therefore, the contribution of the anterior spinal artery is the essential question. If the anterior spinal artery participates in supply, AVM of the filum terminale is the diagnosis and the concept of treatment is in favour of open surgery.

5.

The diagnostic challenge of a pseudo-bimetameric trunk. Selective spinal angiography is not complete as long as segmental supply to the spine at each level has not been achieved. (Figs. 2.5 and 4.1). A pseudo-bimetameric trunk is not a combination of two segmental arteries, but the interconnection of one segmental (posterior intercostal) artery and two neighbouring ventral branches of the posterior intercostal arteries. These ventral intercostal branches have nothing to do with supply of the spine and spinal cord. The situation is easily comprehensible after closer inspection of Fig. 2.2, which has been modified for that reason from earlier schemes (Thron 2008). Therefore one has to look for an independent dorsal branch of the posterior intercostal artery originating from the aorta, which is missing so far. The challenge is that catheterization of this small segmental branch from the aorta may be difficult. But otherwise, spinal, radiculomeningeal and radiculomedullary arterial branches will be missed in this situation.

6.

Demonstration of all potential feeders. For therapy planning the most appropriate feeder has to be selected for a safe and efficient treatment.

7.

Restricted field of view. If an anterior or posterior spinal artery seems to be too large for the region to be supplied or if it extends below the level of the cone it should be followed caudally. This is the only way not to miss the small AVMs of the filum terminale. A field of view covering the whole length of the vertebral column is important especially if abnormal findings are obvious (Fig. 4.19).

8.

Distinction artery vs vein. On the way from the spinal cord surface to the dural outlet, the radiculomedullary vein takes a hairpin course similar to the arterial configuration Figs. 3.10, 3.11, and 4.2. Therefore, it can be mistaken for an artery, particularly when an AVM with early venous filling is present.

9.

The risk of very small radiculomedullary arteries. Anterior radiculomedullary arteries may be very small in the upper and mid thoracic region (down to less than 0.2 mm, see Table 1.2), but nevertheless they may be indispensable for the regional supply (Fig. 4.1b, c). This makes embolizations in this region more hazardous. Small feeders may be hidden behind the nidus of an AVM (Fig. 4.16). Tiny feeders may easily be overlooked or not be demonstrated prior to an intended embolization. Reasons can be limited spatial and contrast resolution of the angiographic equipment or other factors leading to decreased image quality. High flow to an AV shunt from the same segmental source, as shown on Fig. 4.40, might be a cause of haemodynamic origin. One of our few serious complications from glue embolization of a fistula in the upper thoracic region in the early 1990s was most probably caused by this constellation.

10.

Differentiation of SDAVF vs SAVM? (Figs. 4.28 and 4.29) SDAVFs may look very similar to AVMs and have been misjudged as such for many years. This has remained a problem especially with large shunts entering the short common stem of two or more radiculomedullary veins (vein complexes) coming from different parts of the medullary surface as illustrated and described in Sect. 3.7. But as long as no typical radiculomedullary artery is involved, the AV shunt must be located at the level of the dura mater.

11.

Differentiation of SDAVF or SAVM by fistula type? (Fig. 4.30) Discrimination between a spinal dural AVF and the fistulous type of a perimedullary AVM may again be difficult if the recipient arterialized vein looks like an anterior radiculomedullary artery taking a hairpin curve on the ventral surface of the spinal cord as demonstrated in Fig. 4.30. This event is not rare in SDAVFs at lower lumbar levels when the arterialized vein is one of the large lumbar veins shown in Figs. 3.11, 3.33e, and 3.34. The sharp bending course does not discriminate between arteries and veins. Furthermore, the terminal vein or comparably large veins of the cauda equina are connected to the ventral midline vein of the lower spinal cord. To avoid misinterpretation, careful analysis of the vessel anatomy in the region of the intervertebral foramen is important as well as a look at the further course of the vessel on the spinal cord surface on later images (Fig. 4.30b). If you are unable to identify an AV shunt (fistula) in perimedullary veins on the spinal cord, ask yourself whether the intradural blood vessels as a whole could not be veins, exhibiting reversed flow from a dural shunt located at low lumbar or sacral level.

12.

Same pedicle for arteriovenous shunt disorder and spinal cord–supplying artery. Spinal cord–supplying arteries and the meningeal feeders of a dural shunt occasionally arise from the same pedicle as demonstrated in Fig. 4.40. They are better discriminated on lateral views, supporting the relevance of acquiring two perpendicular planes. In case of treatment the surgical approach might be the safer one.

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Index

A

Anatomical and haemodynamical aspects

of arterial blood supply

longitudinal trunks

spinal cord ischemia and infarct

of venous drainage

circulatory disturbances

intrinsic veins

intrinsic venous anastomoses

superficial and radiculomedullary veins

Angiograms

Angiographical appearance

Anterior and posterior radiculomedullary veins

Anterior radiculomedullary arteries

Anterior spinal artery

Anti-backflow control system

Arcade of cone

Arterial blood supply

anatomical and haemodynamical aspects

longitudinal trunks

spinal cord ischemia and infarct

arterioarterial anastomoses

intrinsic anastomoses

superficial anastomoses

cervical spinal cord

embryology

intrinsic arteries

arterial territories

capillaries

central arteries

peripheral system (vasocorona)

radicular and radiculomedullary arteries

spine and spinal cord

extra-and intraspinal extradural anastomoses

segmental spinal branch

spinal angiography

superficial arteries

thoracolumbar spinal cord and cauda equina

upper-and mid-thoracic spinal cord

Arterioarterial anastomoses

intrinsic anastomoses

superficial anastomoses

Arteriovenous disorders

Arteriovenous malformations (AVMs)

Artery of filum terminale

B

Batson's plexus

Blind ending radicular veins

Blood-deviating system

Blood vessels, anatomical description of

C

Capillaries

Capillary telangiectases

Caudal continuation

Cavernomas

C4–C5 level, microangiogram of

ce-MRA

Seecontrast-enhanced magnetic resonance angiography (ce-MRA)

Central (sulcal) arteries

Central grey matter

Centro-anterolateral anastomoses

Centro-dorsolateral anastomoses type 1

Centro-posterolateral anastomoses

Cervical haemangioblastoma

Cervical spinal cord

Conjoint and non-functional radicular veins

Conjoint radiculomedullary veins

Contrast-enhanced magnetic resonance angiography (ce-MRA)

Coronal microangiograms

Corona vasorum

D

Digital subtraction angiography (DSA)

Dura mater

E

Ependymomas

Extradural AVMs

Extradural intraspinal and extraspinal venous systems

F

Facultative vasoafference regions

Fibrocartilaginous embolism

Filum terminale

Fistula type, spinal AVM subtypes

Foix–Alajouanine disease

G

Glomus type, spinal AVM subtypes

Great radicular artery

H

Hodgkin's disease

I

Inborn spinal vascular malformations

Internal vertebral venous plexus

Intradural compartment, AVMs of

Intraspinal neurinoma

Intrinsic anastomoses

Intrinsic arteries

Intrinsic veins

Intrinsic venous anastomoses

J

Juvenile type, spinal AVM subtypes

L

Large transmedullary midline anastomoses

L2/3 level, microangiogram of transverse section

Longitudinal venous trunks

Lumbar artery compression

Lumbosacral spinal cord

Lumbosacral vein patterns

M

Marginal branches

Meningiomas

Microangiograms

cervical spinal cord

of intrinsic and superficial veins

of large midline anastomoses

lumbar level

of median (S2) coronal slices

radicular veins, dural segment of

thoracic level

upper thoracic spinal cord C8–T3

Midline anastomoses type 2

Monocompartmental glomus type

Multiple haemangioblastomas

Myelon

N

Neurinomas

Neurological deficits, pathophysiology of

Non-functional radicular veins

O

Obligatory vasoafference regions

P

Paucisegmental type

Perimedullary fistula type, AVMs

Peripheral arteries

Peripheral system

Pial venous networks of lower degree

Pia mater

Plurisegmental type

Posterior inferior cerebellar artery (PICA)

Posterior median spinal veins

Posterior radiculomedullary arteries

Posterior radiculomedullary veins

Posterior spinal artery

Posterior venous plexus

Predominant terminal vein

Pseudo-bimetameric supply of T9 and T8

R

Radial and central veins

Radial (peripheral) veins

Radicular veins

Radiculomedullary vein(s)

complex

dural segment of

and transdural course

Radio-anatomical images

S

SAVF

SeeSpinal arteriovenous fistulae (SAVF)

SAVMs

SeeSpinal arteriovenous malformations (SAVMs)

SDAVFs

SeeSpinal dural arteriovenous fistulas (SDAVFs)

Small peripheral veins

Solitary haemangioblastoma

Spinal angiographic examinations, pitfalls in

Spinal arteriovenous fistulae (SAVF)

Spinal arteriovenous malformations (SAVMs)

applications in

angiographical findings

definition and classification

complex malformation

with predominant extradural manifestation

Spinal cord parenchyma

Spinal digital subtraction angiography

Spinal dural arteriovenous fistulas (SDAVFs)

aetiological and pathophysiological aspects of

angiographical findings in

chronic myelopathies

diagnostic management

digital subtraction angiography of

histological sections of

histology

history and definition

internal vertebral venous plexus

localization

spinal cord damage, pathogenesis of

spinal cord–supplying artery and radiculomeningeal supply

Spinal radicular arteries

Spinal varicosis

Spinal vascular system

anatomical methods and materials

contrast medium and injection technique

injection techniques

microangiography

preservation

radiological examination techniques

clinical spinal angiography

CT and magnetic resonance angiography

post-mortem macro-and microangiography

X-ray techniques

Sulcal (central) arteries

Superficial anastomoses

Superficial arteries

Superficial veins

longitudinal venous trunks

pial venous networks

T

Terminal vein

Territories, arterial supply

Thoracolumbar levels

Thoracolumbar region

Tractus arteriosus medulla spinalis

Transmedullary midline anastomoses

Transmedullary venous anastomoses

Transparenchymal anastomoses

T3–T4 level, anterolateral extradural spinal tumour

V

Variable vasoafference region

Varicose convolutions

Vascular malformations, classification schemes for

Vascular territories

Vasocorona

See alsoPeripheral system

Vasodeficiency regions

Venous drainage

anatomical and haemodynamical aspects

circulatory disturbances

intrinsic veins

intrinsic venous anastomoses

superficial and radiculomedullary veins

cervical spinal cord

direction of

extradural intraspinal and extraspinal venous systems

intrinsic veins

radiculomedullary veins and transdural course

superficial veins

longitudinal venous trunks

pial venous networks

thoracolumbar and sacral spinal cord

transmedullary venous anastomoses

Venous midline anastomosis

Ventral fissure

Vertebral haemangioma

Vertebrospinal vascular tumours

von Hippel–Lindau syndrome

redpajama_set_name: RedPajamaBook