Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016 (2016), Article ID 5178640, 12 pages
http://dx.doi.org/10.1155/2016/5178640
Research Article

A Novel In Vitro System for Comparative Analyses of Bone Cells and Bacteria under Electrical Stimulation

1Research Laboratory for Biomechanics and Implant Technology, Department of Orthopedics, Rostock University Medical Center, 18057 Rostock, Germany
2Institute of Medical Microbiology, Virology and Hygiene, Rostock University Medical Center, 18057 Rostock, Germany

Received 25 May 2016; Revised 28 September 2016; Accepted 1 November 2016

Academic Editor: Mario U. Manto

Copyright © 2016 Thomas Josef Dauben et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. S. Perlmutter and J. W. Mink, “Deep brain stimulation,” Annual Review of Neuroscience, vol. 29, pp. 229–257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. F.-G. Zeng and R. R. Fay, Eds., Cochlear Implants: Auditory Prostheses and Electric Hearing, vol. 20, Springer Science & Business Media, 2013.
  3. P. J. Bradshaw, P. Stobie, M. W. Knuiman, T. G. Briffa, and M. S. Hobbs, “Trends in the incidence and prevalence of cardiac pacemaker insertions in an ageing population,” Open Heart, vol. 1, no. 1, article e000177, 2014. View at Publisher · View at Google Scholar
  4. L. C. Kloth, “Electrical stimulation for wound healing: a review of evidence from in vitro studies, animal experiments, and clinical trials,” International Journal of Lower Extremity Wounds, vol. 4, no. 1, pp. 23–44, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. A. K. Vafadar, J. N. Côté, and P. S. Archambault, “Effectiveness of functional electrical stimulation in improving clinical outcomes in the upper arm following stroke: a systematic review and meta-analysis,” BioMed Research International, vol. 2015, Article ID 729768, 14 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Zanotti, G. Felicetti, M. Maini, and C. Fracchia, “Peripheral muscle strength training in bed-bound patients with COPD receiving mechanical ventilation: effect of electrical stimulation,” Chest, vol. 124, no. 1, pp. 292–296, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Kern, S. Salmons, W. Mayr, K. Rossini, and U. Carraro, “Recovery of long-term denervated human muscles induced by electrical stimulation,” Muscle & Nerve, vol. 31, no. 1, pp. 98–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. D. N. Rushton, “Electrical stimulation in the treatment of pain,” Disability and Rehabilitation, vol. 24, no. 8, pp. 407–415, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Fu, A. C. Y. Lo, J. S. M. Lai, and K. C. Shih, “The role of electrical stimulation therapy in ophthalmic diseases,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 253, no. 2, pp. 171–176, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Schatz, T. Röck, L. Naycheva et al., “Transcorneal electrical stimulation for patients with retinitis pigmentosa: a prospective, randomized, sham-controlled exploratory study,” Investigative Ophthalmology & Visual Science, vol. 52, no. 7, pp. 4485–4496, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. J. D. Dolbow, D. R. Dolbow, A. S. Gorgey, R. A. Adler, and D. R. Gater, “The effects of aging and electrical stimulation exercise on bone after spinal cord injury,” Aging and Disease, vol. 4, no. 3, pp. 141–153, 2014. View at Google Scholar · View at Scopus
  12. C. L. Sadowsky, E. R. Hammond, A. B. Strohl et al., “Lower extremity functional electrical stimulation cycling promotes physical and functional recovery in chronic spinal cord injury,” Journal of Spinal Cord Medicine, vol. 36, no. 6, pp. 623–631, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Kohata, S. Itoh, S. Takeda et al., “Enhancement of fracture healing by electrical stimulation in the comminuted intraarticular fracture of distal radius,” Bio-Medical Materials and Engineering, vol. 23, no. 6, pp. 485–493, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. W. Latham and J. T. C. Lau, “Bone stimulation: a review of its use as an adjunct,” Techniques in Orthopaedics, vol. 26, no. 1, pp. 14–21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Griffin and A. Bayat, “Electrical stimulation in bone healing: critical analysis by evaluating levels of evidence,” ePlasty: Open Access Journal of Plastic Surgery, vol. 11, article e34, 2011. View at Google Scholar
  16. S. Klouche, E. Sariali, and P. Mamoudy, “Total hip arthroplasty revision due to infection: a cost analysis approach,” Orthopaedics and Traumatology: Surgery and Research, vol. 96, no. 2, pp. 124–132, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. S. M. Kurtz, E. Lau, H. Watson, J. K. Schmier, and J. Parvizi, “Economic burden of periprosthetic joint infection in the United States,” The Journal of Arthroplasty, vol. 27, no. 8, pp. 61–65.e1, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Vuong and M. Otto, “Staphylococcus epidermidis infections,” Microbes and Infection, vol. 4, no. 4, pp. 481–489, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Giladi, Y. Porat, A. Blatt et al., “Microbial growth inhibition by alternating electric fields,” Antimicrobial Agents and Chemotherapy, vol. 52, no. 10, pp. 3517–3522, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. J. L. Del Pozo, M. S. Rouse, J. N. Mandrekar, J. M. Steckelberg, and R. Patel, “The electricidal effect: reduction of Staphylococcus and Pseudomonas biofilms by prolonged exposure to low-intensity electrical current,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 1, pp. 41–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. J. L. Del Pozo, M. S. Rouse, J. N. Mandrekar, M. Fernandez Sampedro, J. M. Steckelberg, and R. Patel, “Effect of electrical current on the activities of antimicrobial agents against Pseudomonas aeruginosa, Staphylococcus aureus, and Staphylococcus epidermidis biofilms,” Antimicrobial Agents and Chemotherapy, vol. 53, no. 1, pp. 35–40, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. H. Maadi, M. Haghi, R. Delshad, H. Kangarloo, M. A. Mohammadnezhady, and G. R. Hemmatyar, “Effect of alternating direct currents on Pseudomonas aeruginosa growth in vitro,” African Journal of Biotechnology, vol. 9, no. 36, pp. 6373–6379, 2010. View at Google Scholar
  23. D. Zituni, H. Schütt-Gerowitt, M. Kopp et al., “The growth of Staphylococcus aureus and Escherichia coli in low-direct current electric fields,” International Journal of Oral Science, vol. 6, no. 1, pp. 7–14, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Obermeier, F. D. Matl, W. Friess, and A. Stemberger, “Growth inhibition of Staphylococcus aureus induced by low-frequency electric and electromagnetic fields,” Bioelectromagnetics, vol. 30, no. 4, pp. 270–279, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. F. D. Matl, A. Obermeier, J. Zlotnyk, W. Friess, A. Stemberger, and R. Burgkart, “Augmentation of antibiotic activity by low-frequency electric and electromagnetic fields examining Staphylococcus aureus in broth media,” Bioelectromagnetics, vol. 32, no. 5, pp. 367–377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Ercan, K. M. Kummer, K. M. Tarquinio, and T. J. Webster, “Decreased Staphylococcus aureus biofilm growth on anodized nanotubular titanium and the effect of electrical stimulation,” Acta Biomaterialia, vol. 7, no. 7, pp. 3003–3012, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. M. T. Ehrensberger, M. E. Tobias, S. R. Nodzo et al., “Cathodic voltage-controlled electrical stimulation of titanium implants as treatment for methicillin-resistant Staphylococcus aureus periprosthetic infections,” Biomaterials, vol. 41, pp. 97–105, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Nodzo, M. Tobias, L. Hansen et al., “Cathodic electrical stimulation combined with vancomycin enhances treatment of methicillin-resistant Staphylococcus aureus implant-associated infections,” Clinical Orthopaedics and Related Research, vol. 473, no. 9, pp. 2856–2864, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. M. R. Asadi and G. Torkaman, “Bacterial inhibition by electrical stimulation,” Advances in Wound Care, vol. 3, no. 2, pp. 91–97, 2014. View at Publisher · View at Google Scholar
  30. E. L. Sandvik, B. R. McLeod, A. E. Parker, and P. S. Stewart, “Direct electric current treatment under physiologic saline conditions kills Staphylococcus epidermidis biofilms via electrolytic generation of hypochlorous acid,” PLoS ONE, vol. 8, no. 2, Article ID e55118, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Cardarelli, Materials Handbook, Springer, London, UK, 2nd edition, 2008.
  32. K. Lochner, A. Fritsche, A. Jonitz et al., “The potential role of human osteoblasts for periprosthetic osteolysis following exposure to wear particles,” International Journal of Molecular Medicine, vol. 28, no. 6, pp. 1055–1063, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. A. S. Stephens, S. R. Stephens, and N. A. Morrison, “Internal control genes for quantitative RT-PCR expression analysis in mouse osteoblasts, osteoclasts and macrophages,” BMC Research Notes, vol. 4, no. 1, article 410, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. P. R. Supronowicz, P. M. Ajayan, K. R. Ullmann, B. P. Arulanandam, D. W. Metzger, and R. Bizios, “Novel current-conducting composite substrates for exposing osteoblasts to alternating current stimulation,” Journal of Biomedical Materials Research, vol. 59, no. 3, pp. 499–506, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Windisch, W. Kolb, E. Röhner et al., “Invasive electromagnetic field treatment in osteonecrosis of the femoral head: a prospective cohort study,” The Open Orthopaedics Journal, vol. 8, no. 1, pp. 125–129, 2014. View at Publisher · View at Google Scholar
  36. P. C. Grunert, A. Jonitz-Heincke, Y. Su et al., “Establishment of a novel in vitro test setup for electric and magnetic stimulation of human osteoblasts,” Cell Biochemistry and Biophysics, vol. 70, no. 2, pp. 805–817, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Abdel-Hady Gepreel and M. Niinomi, “Biocompatibility of Ti-alloys for long-term implantation,” Journal of the Mechanical Behavior of Biomedical Materials, vol. 20, pp. 407–415, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Wang, “The use of titanium for medical applications in the USA,” Materials Science and Engineering A, vol. 213, no. 1-2, pp. 134–137, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Cornet, D. Muster, and J. H. Jaeger, “Fatigue: corrosion of endoprosthesis titanium alloys,” Biomaterials Medical Devices and Artificial Organs, vol. 7, no. 1, pp. 155–167, 1979. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Velasco-Ortega, A. Jos, A. M. Cameán, J. Pato-Mourelo, and J. J. Segura-Egea, “In vitro evaluation of cytotoxicity and genotoxicity of a commercial titanium alloy for dental implantology,” Mutation Research/Genetic Toxicology and Environmental Mutagenesis, vol. 702, no. 1, pp. 17–23, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Fleck and D. Eifler, “Corrosion, fatigue and corrosion fatigue behaviour of metal implant materials, especially titanium alloys,” International Journal of Fatigue, vol. 32, no. 6, pp. 929–935, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. D. L. Cochran, P. V. Nummikoski, F. L. Higginbottom, J. S. Hermann, S. R. Makins, and D. Buser, “Evaluation of an endosseous titanium implant with a sandblasted and acid-etched surface in the canine mandible: radiographic results,” Clinical Oral Implants Research, vol. 7, no. 3, pp. 240–252, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. A. F. Mavrogenis, R. Dimitriou, J. Parvizi, and G. C. Babis, “Biology of implant osseointegration,” Journal of Musculoskeletal Neuronal Interactions, vol. 9, no. 2, pp. 61–71, 2009. View at Google Scholar · View at Scopus
  44. R. K. Alla, K. Ginjupalli, N. Upadhya, M. Shammas, R. K. Ravi, and R. Sekhar, “Surface roughness of implants: a review,” Trends in Biomaterials and Artificial Organs, vol. 25, no. 3, pp. 112–118, 2011. View at Google Scholar · View at Scopus
  45. K. Suzuki, K. Aoki, and K. Ohya, “Effects of surface roughness of titanium implants on bone remodeling activity of femur in rabbits,” Bone, vol. 21, no. 6, pp. 507–514, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Marinucci, S. Balloni, E. Becchetti et al., “Effect of titanium surface roughness on human osteoblast proliferation and gene expression in vitro,” International Journal of Oral & Maxillofacial Implants, vol. 21, no. 5, pp. 719–725, 2006. View at Google Scholar · View at Scopus
  47. K. Kieswetter, Z. Schwartz, T. W. Hummert et al., “Surface roughness modulates the local production of growth factors and cytokines by osteoblast-like MG-63 cells,” Journal of Biomedical Materials Research, vol. 32, no. 1, pp. 55–63, 1996. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Y. Martin, Z. Schwartz, T. W. Hummert et al., “Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63),” Journal of Biomedical Materials Research, vol. 29, no. 3, pp. 389–401, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Hronik-Tupaj, W. L. Rice, M. Cronin-Golomb, D. L. Kaplan, and I. Georgakoudi, “Osteoblastic differentiation and stress response of human mesenchymal stem cells exposed to alternating current electric fields,” BioMedical Engineering Online, vol. 10, article 9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Ercan and T. J. Webster, “The effect of biphasic electrical stimulation on osteoblast function at anodized nanotubular titanium surfaces,” Biomaterials, vol. 31, no. 13, pp. 3684–3693, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. R. A. Gittens, R. Olivares-Navarrete, R. Rettew et al., “Electrical polarization of titanium surfaces for the enhancement of osteoblast differentiation,” Bioelectromagnetics, vol. 34, no. 8, pp. 599–612, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Hiemer, J. Ziebart, A. Jonitz-Heincke et al., “Magnetically induced electrostimulation of human osteoblasts results in enhanced cell viability and osteogenic differentiation,” International Journal of Molecular Medicine, vol. 38, no. 1, pp. 57–64, 2016. View at Publisher · View at Google Scholar
{"cc_re__cc_re__cc_by_4_0": ["iversity Medical Center, 18057 Rostock, Germany<br /><sup>2</sup>Institute of Medical Microbiology, Virology and Hygiene, Rostock University Medical Center, 18057 Rostock, Germany<br /></p>\r\n           \r\n      \r\n\r\n\r\n\r\n\r\n<p>Received 25 May 2016; Revised 28 September 2016; Accepted 1 November 2016</p>                \r\n<p>Academic Editor: Mario U. Manto</p>    <div class=\"xml-content\">\r\n        <p>Copyright &#xa9; 2016 Thomas Josef Dauben et al. This is an open access article distributed under the <a rel=\"license\" href=\"http://creativecommons.org/licenses/by/4.0/\">  Creative Commons Attribution License</a>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.\r\n        </p>\r\n    </div>\r\n<div id=\"divXMLContent\" class=\"xml-content\">\r\n            <h4>Linked References</h4>\r\n\r\n    <ol>\r\n\r\n<li id=\"B1\">J. S. Perlmutter and J. W. Mink, \u201cDeep brain stimulation,\u201d <i>Annual Review of Neuroscience</i>, vol. 29, pp. 229\u2013257, 2006.<span class=\"reflinks\"> <a href=\"https://doi.org/10.1146%2fannu"], "copyright__copyright__copyright": ["ation of titanium surfaces for the enhancement of osteoblast differentiation,\u201d Bioelectromagnetics, vol. 34, no. 8, pp. 599\u2013612, 2013. View at Publisher \u00b7 View at Google Scholar \u00b7 View at Scopus\n  52. B. Hiemer, J. Ziebart, A. Jonitz-Heincke et al., \u201cMagnetically induced electrostimulation of human osteoblasts results in enhanced cell viability and osteogenic differentiation,\u201d International Journal of Molecular Medicine, vol. 38, no. 1, pp. 57\u201364, 2016. View at Publisher \u00b7 View at Google Scholar"]}