Publications in Integrative and Complementary Medicine: A Ten-Year Bibliometric Survey in the Field of ICM

Background This article aims to analyze the research status of integrative complementary medicine (ICM) and features of highly cited papers in the field to provide reference of the future development of ICM. Methods Publications in the field of ICM from 2009 to 2018 were retrieved from the Web of Science Core Collection. The top 20 countries/territories, institutions, journals, keywords of highly cited and noncited papers, and characteristics of essential science indicator (ESI) papers, as well as open access (OA) and non-OA papers, were analyzed. Results Mainland China had the largest number of ICM publications. The top 20 journals published a total of 31667 papers in 2009–2018, which represented 92.9% of all publications. Keywords of highly cited and noncited papers point to different research directions. 48 ESI highly cited/hot papers were identified, most of which are related to phytochemistry. Furthermore, the average citation rate (percentage of publications that have been cited one or more times) of OA papers was lower than that of total papers and non-OA papers. Conclusions China leads in number of publications; however, publication quality in ICM field requires improvement. A few journals accounted for more than half of number of publications and citations, which are important for the development of ICM. Many of the keywords in ICM noncited publications pointed towards broad meaning that poorly reflect the exact research content. Most highly cited ICM studies focused on the identification and evaluation of plant active components. OA may not be an effective approach to increase paper citations in the field of ICM.


Introduction
In 2015, the greatest news for scientists in the field of natural medicines, and particularly Chinese scientists, was that Professor Youyou Tu won the 2015 Nobel Prize for Physiology or Medicine, which is the first Nobel Prize in natural sciences awarded to a scientist based on the Chinese mainland. Professor Tu shared this prize (for discovery of avermectins) with Professors William C. Campbell and Satoshi � Omura, for her unprecedented contribution to medicine that has saved millions of lives worldwide. As declared in her Nobel Lecture on December 7, 2015, at Aula Medica, Karolinska Institutet in Stockholm, the discovery of artemisinin (Qinghaosu in Chinese) is regarded as a gift from traditional Chinese medicine (TCM) to the world. Notably, there is an increasing interest in investigating the biological activities and underlying mechanisms of action of TCM. e definitions of, and distinctions between, complementary, alternative, and traditional medicine and conventional medicine have been unclear and inconsistent across nations and cultures [1]. Integrative medicine in China always refers to the integration of TCM and Western medicine [2]. TCM is generally considered an important component of integrative and complementary medicine; thus, it is no surprise that scientists from western countries have also contributed considerably to TCM publications [3]. With the development of traditional medicine, combining traditional and modern medicines has been found to show great potential and integrative complementary medicine (ICM) has become an intense focus of new research. ICM has been used for treatment of cardiovascular diseases, cancer, and many other chronic diseases [4][5][6]. Correspondingly, scientific research output in the ICM field is increasing worldwide.
Moral-Munoz et al. analyzed the research in integrative and complementary oncology from production trends, country collaboration, and leading research topics. e field is led by China, and the primary topics attracting the attention are apoptosis, breast cancer, oxidative stress, chemotherapy, and NF-kappa-B [7]. ey also discovered the scientific evolution of cancer-related symptoms in complementary and alternative medicine (CAM) research area and identified the main research thematic by using the coword analysis. e coword analysis identified 12 main thematic areas including anxiety, survivors and palliative care, and meditation [8]. Jose's research studies can reflect the difference between CAM and ICM. Our research will focus on the field of ICM which includes traditional Chinese medicine.
Zhu et al. analyzed the integrated complementary medicine articles based on changes in publication years, geographical distribution, research institutes, and research fields. eir findings show that the development of research and application related to integrated complementary medicine can be divided into three periods. e first period is 2004-2010, which is the period of stable increase. e second one is 2010-2013, which is the period of rapid increase. In the third period, 2014-2015, the number of articles has slightly decreased [9]. We aim to analyze the recent research status of ICM. Considering the delay in the citation of the paper and referring to Zhu's research studies, we set the time as 2009-2018. Zyoud et al. evaluated the performance of research output published in international ICM journals, originating from Arab world. Scientific research output in the ICM field is increasing. Most of publications were driven by societal use of medicinal plants and herbs [6]. We will pay attention to the theme of the highly cited papers in China. Fu [11]. We will focus on the topics of highly cited papers in the field of ICM and analyze the phytochemistry-related publications in it.
Danell analyzed the reception of ICM research outside the ICM context such as in general or specialized medicine journals. A majority of the cited documents were acknowledged in journals and documents that could be related to research areas outside the ICM context, such as pharmacology and pharmacy and plant science. e related ICM research was related to basic preclinical research, in fields such as cell biology, plant pharmacology, and animal experiments [12]. We will pay attention to the journals of highly cited papers in the ICM field. Bibliometrics, first introduced by Pritchard, is an effective method that uses quantitative analysis and statistics to describe research trends in a specific field. Indeed, bibliometric approaches have been widely applied to analyze the development of various scientific fields [13][14][15]. In the present study, we conducted a bibliometric analysis of ICM research from 2009 to 2018. Our results provide a basis for better understanding of global ICM research development.

Search Strategy.
Using the search strategy: Web of Science (WoS) category, Integrative and Complementary Medicine, publication year 2009-2018, and publication type "article" and "review," publications in the field of ICM were retrieved from the WoS Core Collection; data were collected in November 2019. en, the data set is imported into the InCites database for analysis. According to the WoS classification criteria, journals classified in the ICM category were within the scope of the search. e WOS subject classification is many-to-many. A journal can belong to multiple WOS subject classifications at the same time.
A total of 34103 publications were identified. Publications in our research only referred to articles and reviews; other types of publications were not included in our research.

Statistical Analysis.
Statistical Product and Service Solutions (SPSS) software was used to analyze correlations among indicators. When analyzed the research topics of the top 500 highly cited and noncited papers (randomly selected by year), we extracted the author keyword and ID keyword plus standard in WoS for comparative analysis. Different words with identical meanings were grouped and considered as a single keyword.
An analysis flowchart is presented in Figure 1. We selected the top 20 countries/territories, institutions, and journals for detailed comparisons using multiple bibliometric indices.
An analysis flowchart is presented in Figure 1. We analyzed the top 20 countries/regions, institutions, and journals that contributed most to the quantity and quality of publications in the ICM field. Multiple bibliometric indices were used for detailed comparisons through keyword comparison and Essential Science Indicator (ESI) paper analysis to determine the characteristic of highly cited papers in ICM field. Finally, the impact of open access on the citation of papers in the ICM field was discussed. e mean number of citations per paper (CPP) is an indicator that is used to compare the scientific impact of publications among countries, institutions, and journals [16,17]. Although the number of publications from mainland China was highest (rank 1), the CPP (9.51) was somewhat lower than the global mean level (10.22). Among the top 20 countries/territories, 14 countries had higher CPP than the global mean, including the USA, Taiwan, Brazil, India, Germany, England, Hong Kong, Malaysia, Canada, Italy, South Africa, ailand, Spain, and Pakistan ( Figure 3(b)).

Results
Waltman and Schreiber introduced an approach to calculate percentile-based indicators. eir research shows the nice property of percentile-based indicators: a (small) change in the number of citations of one or more publications that are exactly at the top 10% threshold affects only research groups that have publications at the threshold.
Research groups without publications at the threshold are not affected [18].
Pakistan's top 10% indicator ranks first, accounting for 17.87%, far higher than Italy, which ranks second, accounting for 13.66%, and other countries account for about 10%. At the same time, considering the number of Pakistani publications is 431, ranking 20th, it is not difficult to conclude that most of the ICM publications in Pakistan have received more citations. We further analyzed the research area of the publications in Pakistan, we found that, in addition to being classified into the field of ICM, 162 publications were classified into Pharmacology & Pharmacy category. Chemistry, Medicinal, and Plant Sciences categories have 148 publications, respectively. At the same time, most of the top 50 highly cited publications in Pakistan are related to the pharmacological effects of plant extracts. e total number of publications in China is far ahead, but the top 10% indicator is not prominent, indicating that many publications published by China in ICM have not received enough citations (Figure 3(c)). e citation rates of the top 20 countries/territories were in the range of 85%-94%. e correlation between citation rate and CPP (r � 0.575) indicates that cited papers may greatly facilitate an increase in CPP (Figure 3(d)).      ICM publications are published in relatively concentrated journals. We analyzed the top 20 journals by number of publications. In 2009-2018, the top five journals published more than half of total publications, with the top ten journals accounting for more than 70%, and the top 20 journals accounting for more than 90%. Hence, a few journals hosted more than half of publications and citations in the field, which is important for the development of ICM.  Table 1 shows the impact factors of the top 20 journals. Comparing these impact factors over the past five years with current impact factors, we found that, as the volume of journal publications increased significantly, journal impact factors decreased. Only Phytomedicine (5), e American Journal of Chinese Medicine (9), and Acupuncture in Medicine (16)   e h-index (Hirsch index) [19] is an established indicator of the impact of an object (journal, author, topic, and institute) and is a parameter that synthesizes a researcher's output. It is defined as the maximum number, h, such that the researcher has h papers with at least h citations each [20]. It combines the effect of "quantity" (number of publications) and "quality" (citation rate) in a rather specific balanced way [21]. Analysis of the correlation between journal IF and h-index (r � 0.697) indicated that highly cited papers may contribute substantially to increases in journal IF ( Figure 5(c)). Similarly, there was a positive correlation between journal IF and citation rate (r � 0.913), indicating that top journals are less likely to publish papers with no citations ( Figure 5(d)).

Comparison of Keywords between the Top 500 Highly Cited and Noncited Papers.
Keywords are the most condensed scientific components of a paper and can thus be used to trace hot topics and frontiers in specific research fields. As papers contributing to hot topic research and cutting-edge research are more likely to be highly cited,it is a reasonable hypothesis that keywords could differ markedly between highly cited and noncited papers. Keywords were retrieved from the top 500 highly cited and noncited papers in the field of ICM. Subsequent analysis showed that, from the top 500 highly cited papers, "in vitro," "oxidative stress," "mice," and"antibacterial activity" were the most frequently used keywords plus, and "medicinal plants," "antioxidant," "antiinflammatory," "apoptosis," and "ethnobotany" were the most frequently used author keywords.
ere were some differences between the two groups, but they were not   substantial. Because in noncited papers, "expression," "care," "disease," "prevalence," "apoptosis," "health," "cancer," "treatment," "oxidative stress," and "acupuncture" were the most frequently used keywords. From a scientific perspective, many of the keywords used in noncited papers pointed towards broad meaning that poorly reflect the exact research content. At the same time, comparing the keywords of highly cited and noncited papers, it can be seen that the keywords of highly cited papers directed to the pharmacological effects of medicinal plants.

Analysis of ESI Papers.
Highly cited papers: selected from the most recent 10 years of data, highly cited papers reflect the top 1% of papers by field and publication year. Hot papers: hot papers are selected by virtue of being cited among the top one-tenth of one percent (0.1%) in a current bimonthly period. ESI categorizes papers into 22 broad fields of research. Papers are selected in each of 22 fields of science and must be published within the last two years. Highly cited papers help identify breakthrough research within a research field and are used within Web of Science to identify and refine the most influential research papers. ESI highly cited/ hot papers are indicators of cutting-edge research. Notably, ICM is not an independent field in ESI, but rather is included into other ESI fields, according to the scientific characteristics of papers. Among the total of 34102 publications in ICM between 2009 and 2018, there were only 48 ESI highly cited/hot papers: 37 in Pharmacology and Pharmacy, 39 in Plant Sciences, 39 in Chemistry Medicinal, and 1 in Oncology (these papers were interdisciplinary). e 48 papers included 37 reviews and 11 research articles, with 15 OA and 33 non-OA papers. 15 of them belonged to international cooperation publications. 47 were highly cited papers, and 1 was hot paper (search in November 2019). e proportion of international cooperation papers in the top 500 papers was 21.6% and was 18.68% in all papers. e proportion of international cooperation papers in ESI highly cited/hot papers was 31.25%. It is not difficult to infer that international cooperation will help publications get more citations.
e African Journal of Traditional Complementary and Alternative Medicines and Alternative Medicine Review each had a highly cited article but were eliminated from SCI in 2018. Table 2 lists the top 20 highly cited publications. Analysis of these highly cited publications demonstrated that, except for one industry standard, all others were related to the antioxidant and anti-inflammatory effects of plant extracts. Most reviews were related to the effects of natural plant extracts, while several were about ethnopharmacology and meta-analysis of integrative medicine data. Notably, four of the 37 reviews were related to ginsenosides. Given the important role of ginseng in Chinese medicine, scientists in the field of Chinese medicine are exploring its potential from a modern perspective. e countries have the ESI papers were mainland China (15), South Korea (8), Italy (5), Switzerland (4), and the United Kingdom (4).

Analysis of OA Publications.
OA refers to online publications that are free of restrictions on access; hence, OA is expected to maximize the circulation and impact of research publications [22,23]. erefore, an increasing number of  Figure 6). is result indicates that OA may not be an effective approach to increase the citation of papers in the field of ICM.

China Is Active in ICM Research and Remains with the Tremendous Potential.
Our results demonstrate that Asia, and particularly mainland China, leads the world in ICM  Additionally, the identification of arsenic trioxide as an effective drug therapy for leukemia represents another great achievement of ICM research in China. In the 1980s, the Chinese government launched a long-term and extensive project, "modernization of TCM." Since that time, China has made substantial financial investment in this area. In addition to the successful development of artemisia and arsenic trioxide as internationally recognized drugs, the successful entrance of Danshen dripping pills and other herbal preparations, into USA Food and Drug Administration, approved clinical trials represent another landmark in the achievements of "Modernization of TCM." e present bibliometric analysis clearly demonstrates that China is the leader in publication of ICM research, indicating the leading role of China in this field; however, it is also important to note that, based on CPP data, China is not preeminent, suggesting that the ICM publications from China have not received enough attention. WoS has an English-language bias. e problem cannot be ignored because myriad research findings of Chinese medicine, Islamic medicine, and Kampo are written in their native languages, not in English. As ICM emphasizes non-Western conventional medicines, this English-language bias is an obstacle to the ability to reflect any developing trends in this field accurately [24]. At the same time, our research shows that the level of international cooperation of highly cited papers was relatively high. Improving the level of international cooperation in ICM may be an effective way to attract more attention.

Plant Medicine in the ICM Field Gets More Attention.
Our research shows that most of highly cited papers were related to the effects of natural plant extracts. As Tu said, artemisinin, with its unique sesquiterpene lactone created by phytochemical evolution, is a true gift from old Chinese medicine. e route to the discovery of artemisinin was short compared with those of many other phytochemical discoveries in drug development. But this is not the only instance in which the wisdom of Chinese medicine has borne fruit [25]. e development of omics technologies and network pharmacology in recent years has offered an opportunity to bridge the gap between western medicine and TCM [26]. Intensive and comprehensive research and validation of the pharmacological mechanisms, targets, and signaling pathways involved in ICM remain very scarce and may be an important component of future ICM research.
Moreover, alongside increasing recognition of the limitations of the "one gene, one drug, one disease" philosophy for therapy of chronic and complex diseases, western scientists have called for a renaissance of TCM research. us, it is reasonable to expect that research into ICM from western countries will expand. Worldwide attention will doubtless facilitate the development of ICM. In the spirit of the recent recognition of Professor Tu's outstanding contributions and the tremendous potential of natural productbased medicines, the scientific community should strengthen collaborative research in various areas of natural medicine, to enhance scientific research quality.

ICM Journals Should Play an Active Role in Promoting the
Development of ICM. In our research, we retrieved journals classified in the ICM category by WoS. Importantly, a large number of papers in this field, particularly high-impact papers, are not published in "ICM" journals, but rather in mainstream medical journals; however, as a unique part of medicine, relevant scientists have always emphasized that we must have reliable scientific evidence and respect the characteristics of traditional medicine. ICM needs its own professional journal to improve the rate of publication of quality articles. Improving the influence of ICM professional journals is very important to promote the development of ICM.
In bibliometric analysis, the capture of keywords is a useful approach to identify the cutting edge in a specific field. A scan of the recent ICM articles showed that most were limited to analysis of compounds, identification, and assessment of active components or simple analyses of the pharmacological, pharmacokinetic, or toxicological performance of herbal extracts, while assessment of drug efficacy was primarily limited to antioxidant, anti-inflammatory, and cytotoxic properties, which lack specificity, resulting in a low likelihood of discovery of novel drugs from natural and traditional Chinese medicines. e methods used in integrative medicine encompass a wide range of therapeutic Evidence-Based Complementary and Alternative Medicine modalities, among which acupuncture and Chinese herbal medicine are commonly used. Owing to great interest among the general public, integrative medicine has frequently featured in the media recently, and the phrase "the medicine of the future" has been coined [27]. Adjuvant therapy using ICM is developing rapidly; however, from a bibliometrics perspective, the related literature has yet to attract sufficient attention. Tam et al. analyzed the top 50 publications in the ICM field and found that no articles used an observational study design [28]. Physicians who practice complementary and alternative medicine must recognize the need to support their methods with scientific evidence relating to their effectiveness [29]. e number of ICM publications has experienced a period of rapid growth. With the development of ICM, we are glad to see that a panel of important clinical trials of ICM had been published in highimpact journals. Our research selected the journals of ICM category, and the relevant literatures have not been discussed but cannot be ignored. omas Kuhn, a highly significant philosopher of science of the 20th century, argued that science does not progress via a linear accumulation of new knowledge but rather undergoes periodic revolutions, also referred to as "paradigm shifts" [30]. Appropriate changes are key to the further development of ICM.
Few ESI highly cited/hot papers were captured, further demonstrating the lack of innovative studies in ICM. Nevertheless, the keywords captured from previous publications may not represent the "real" research highlights, considering keywords such as "rats" and "in vitro" are too general to indicate specific scientific aspects of the published studies. Most high-impact journals clearly demand that such void keywords should not be used in their guidance to authors. For journals in the ICM field, it is important to guide authors use specific keywords to highlight their investigations.
e overall low impact of research in the field of ICM is also evidenced by the general low impact factor of journals in this field. e Journal of Ginseng Research has the highest impact factor, at only 3.898, among journals in the field of ICM. In contrast, the field of western medicine includes many high-impact journals; for example, e New England Journal of Medicine, JAMA, and e Lancet and its sister journals. Although it is well-acknowledged that journal impact factors exhibit biases across different scientific fields, because total publications vary dramatically, generally low impact factors of journals in a certain scientific field indicates that the research in this field is less active than those with higher impact factors. It is understandable that the research scale, intensity, and comprehensibility of ICM, as alternative medicine, are much lower than those of the western medicine. Ling et al. believed that TCM possesses advantages over Western medicine in specific aspects at a certain stage of cancer treatment [31]; however, to expand the influence of ICM research, it is important to gather sufficient scientific evidence to support the advantage of ICM over the typical western medicine for the therapy of chronic diseases.
We expected the further reform and development of professional ICM journals to better lead the field.

OA Publication Is Not a "
Passkey" to Improve the Impact of Papers Reporting Poor Science. OA, which is a product of the belief that free and wide access to publications may help to expand the scientific impact of publications, has greatly promoted journal publication. e emergence and rapid growth of mega journals are part of the result of this development; however, the impact of OA papers, as evidenced by the results of CPP analysis in our study, was lower than that of both total papers and non-OA papers, indicating that OA did not improve the impact of publications in the field ICM. For OA, the authors are required to pay article processing charges and have promised rapid peer review and immediate online publication after acceptance, which leads to the quality of peer review becoming an essential concern [32,33]. After OA becomes a common publication type, manuscript quality remains the key to competition among scientific and technical journals; therefore, improvement of academic quality and ensuring publications presents a rational perspective deserve top priority. OA is not an appropriate approach for journals to improve business by sacrificing the scientific quality of publications.

Conclusion
Worldwide attention will doubtlessly facilitate the development of ICM, which could represent a challenge for ICM scientists. e continuous efforts of Chinese scientists in the field of ICM have made China the leader in ICM research publications; however, the quality of publications requires improvement. Keyword analysis of ICM publications reflects the main research content in this field, while highly cited papers reflect the hot topics. e plant pharmacology part of ICM gets more attention. China has a leading advantage in the field of natural medicine in ICM and should continue to tap the potential in this area. e number of ICM journals is not large, with a few journals accounting for more than half of the publications and citations in this field. Excellent professional ICM journals play an important role in the development of ICM. e development of the ICM field and improvement of the impact of ICM professional journals should be mutually reinforcing. e number of ICM publications has experienced a period of rapid growth; however, its impact remains relatively weak. Related research on ICM requires more valid evidence, and appropriate changes will be key to the further development of ICM. OA has been a hot topic in recent years; however, in our analysis of articles in ICM field journals from the WoS Core Collection, we found that the OA approach is not effective in promoting paper citations.
Overall, although publications in the ICM field have received widespread attention, their influence is relatively low. e field of ICM has great potential and we are motivated by Professor Yoyo Tu and looking forward with great anticipation for the future development of ICM.

Data Availability
e data used to support the findings of this study are included within the supplementary information files. 10 Evidence-Based Complementary and Alternative Medicine