Animal Study and Pre-clinical Trials of Biomaterials

  • Deni Noviana
  • Sri Estuningsih
  • Mokhamad Fakhrul Ulum
Chapter
Part of the Advanced Structured Materials book series (STRUCTMAT, volume 58)

Abstract

An in vivo study is one of the most important steps in the process of translating biomaterials to clinical applications. It is mostly conducted to confirm in vitro results before going further to clinical trials. Appropriate use of animal models in the in vivo studies of biomaterials and medical devices is mandatory and should meet the approved regulations and ethics as defined by both local and international regulatory bodies. These studies involve the use of various approaches and protocols in order to know the body responses both local and systemic and to find out the short- and long-term responses of the body toward the implanted biomaterials or devices. This chapter describes complete procedures and practices of in vivo studies starting from selection of appropriate animal model, pre-implantation, surgical procedure and post-implantation, and monitoring of material-host responses. Some experiences of in vivo studies done by Indonesian researchers and the development of new implants are also presented.

Keywords

Biomaterials Biocompatibility Animal testing 

Notes

Acknowledgements

The authors acknowledge the support of Indonesian Ministry of Education and Culture-DGHE No. 083/SP2H/PL/Dit.Litabmas/II/2015 and Indonesian-Australia Center Small Grant in the year of 2015.

References

  1. Alghamdi, H. S., Bosco, R., Both, S. K., Iafisco, M., Leeuwenburgh, S. C., Jansen, J. A., & van den Beucken, J. J. (2014). Synergistic effects of bisphosphonate and calcium phosphate nanoparticles on peri-implant bone responses in osteoporotic rats. Biomaterials, 35, 5482–5490.CrossRefGoogle Scholar
  2. Alper, T. (2008). Anesthetizing the public conscience: Lethal injection and animal euthanasia. Fordham Urban Law Journal, 35, 817.Google Scholar
  3. Alt, V., Thormann, U., Ray, S., Zahner, D., Durselen, L., Lips, K., et al. (2013). A new metaphyseal bone defect model in osteoporotic rats to study biomaterials for the enhancement of bone healing in osteoporotic fractures. Acta Biomaterialia, 9, 7035–7042.CrossRefGoogle Scholar
  4. Altman, G. H., Diaz, F., Jakuba, C., Calabro, T., Horan, R. L., Chen, J., et al. (2003). Silk-based biomaterials. Biomaterials, 24, 401–416.CrossRefGoogle Scholar
  5. Arts, J. W., Kramer, K., Arndt, S. S., & Ohl, F. (2012). The impact of transportation on physiological and behavioral parameters in Wistar rats: Implications for acclimatization periods. Institute for Laboratory Animal Research Journal, 53, E82–E98.CrossRefGoogle Scholar
  6. Baas, J. (2008). Adjuvant therapies of bone graft around non-cemented experimental orthopedic implants stereological methods and experiments in dogs. Acta Orthopaedica, Suppl 79, 1–43.Google Scholar
  7. Bădărău, D. (2013). Declaration of Helsinki. In S. Loue (Ed.), Mental health practitioner’s guide to HIV/AIDS (pp. 181–183). New York: Springer.Google Scholar
  8. Baena, R. Y., Lupi, S. M., Pastorino, R., Maiorana, C., Lucchese, A., & Rizzo, S. (2013). Radiographic evaluation of regenerated bone following poly(lactic-co-glycolic) acid/hydroxyapatite and deproteinized bovine bone graft in sinus lifting. Journal of Craniofacial Surgery, 24, 845–848.CrossRefGoogle Scholar
  9. Bancroft, J. D., & Gamble, M. (2008). Theory and practice of histological Techniques (6th ed.). Churchill Livingstone: Elsevier.Google Scholar
  10. Barckman, J. (2014). Bone allograft and implant fixation tested under influence of bio-burden reduction, periosteal augmentation and topical antibiotics. Animal experimental studies. Danish Medical Journal, 61, B4720.Google Scholar
  11. Baro, M., Sánchez, E., Delgado, A., Perera, A., & Évora, C. (2002). In vitro–in vivo characterization of gentamicin bone implants. Journal of Controlled Release, 83, 353–364.CrossRefGoogle Scholar
  12. Barrett, H. H., Myers, K. J., Hoeschen, C., Kupinski, M. A., & Little, M. P. (2015). Task-based measures of image quality and their relation to radiation dose and patient risk. Physics in Medicine & Biology, 60, R1–R75.CrossRefGoogle Scholar
  13. Beard, J. M., & Losh, D. P. (2006). Chapter 14: Selecting radiographic tests: Radiographs, computed tomography, magnetic resonance imaging, ultrasound, and nuclear imaging. In R. E. Rakel (Ed.), Essential family medicine (3rd ed.) (pp. 169–196). Philadelphia: W.B. Saunders.Google Scholar
  14. Beauchamp, T. L. (2008). The human use of animals: Case studies in ethical choice. New York: Oxford University Press.Google Scholar
  15. Beauchamp, T. L., & Childress, J. F. (2001). Principles of biomedical ethics (7th ed.). Oxford University Press.Google Scholar
  16. Beilin, B., Bessler, H., Mayburd, E., Smirnov, G., Dekel, A., Yardeni, I., & Shavit, Y. (2003). Effects of preemptive analgesia on pain and cytokine production in the postoperative period. Anesthesiology, 98, 151–155.CrossRefGoogle Scholar
  17. Bennett, R. G. (1988). Selection of wound closure materials. Journal of the American Academy of Dermatology, 18, 619–637.CrossRefGoogle Scholar
  18. Boerckel, J. D., Kolambkar, Y. M., Stevens, H. Y., Lin, A. S., Dupont, K. M., & Guldberg, R. E. (2012). Effects of in vivo mechanical loading on large bone defect regeneration. Journal of Orthopaedic Research, 30, 1067–1075.CrossRefGoogle Scholar
  19. Bosing, B., Tunsmeyer, J., Mischke, R., Beyerbach, M., & Kastner, S. B. (2012). Clinical usability and practicability of Alfaxalone for short-term anaesthesia in the cat after premedication with Buprenorphine. Tierarztl Prax Ausg K Kleintiere Heimtiere, 40, 17–25.Google Scholar
  20. Botnar, R. M., Perez, A. S., Witte, S., Wiethoff, A. J., Laredo, J., Hamilton, J., et al. (2004). In vivo molecular imaging of acute and subacute thrombosis using a fibrin-binding magnetic resonance imaging contrast agent. Circulation, 109, 2023–2029.CrossRefGoogle Scholar
  21. Brantigan, J. W., Mcafee, P. C., Cunningham, B. W., Wang, H., & Orbegoso, C. M. (1994). Interbody lumbar fusion using a carbon fiber cage implant versus allograft bone: An investigational study in the Spanish goat. Spine (Phila Pa 1976), 19, 1436–1443.Google Scholar
  22. Bratzler, D. W., Houck, P. M., Richards, C., Steele, L., Dellinger, E. P., Fry, D. E., et al. (2005). Use of antimicrobial prophylaxis for major surgery: Baseline results from the national surgical infection prevention project. Archives of Surgery, 140, 174–182.CrossRefGoogle Scholar
  23. Buchanan-Smith, H. M., Rennie, A., Vitale, A., Pollo, S., Prescott, M. J., & Morton, D. B. (2005). Harmonising the definition of refinement. Animal Welfare, 14, 379–384.Google Scholar
  24. Buchwalow, I. B., & Böcker, W. (2010). Immunohistochemistry: Basics and methods. Berlin: Springer.CrossRefGoogle Scholar
  25. Bushnell, B. D., Horton, J. K., McDonald, M. F., & Robertson, P. G. (2008). Perioperative medical comorbidities in the orthopaedic patient. Journal of the American Academy of Orthopaedic Surgeons, 16, 216–227.Google Scholar
  26. Campbell, K. A., Stein, S., Looze, C., & Bosco, J. A. (2014). Antibiotic stewardship in orthopaedic surgery: Principles and practice. Journal of the American Academy of Orthopaedic Surgeons, 22, 772–781.CrossRefGoogle Scholar
  27. Carleton, H. M., & Drury, R. A. B. (1957). Histological technique for normal and pathological tissues and the identification of parasites. Oxford University Press.Google Scholar
  28. Castañeda, F., Ball-Kell, S. M., Young, K., & Li, R. (2000). Assessment of a polyester-covered nitinol stent in the canine aorta and iliac arteries. Cardiovascular and Interventional Radiology, 23, 375–383.CrossRefGoogle Scholar
  29. Cerri, P. S., & Sasso-Cerri, E. (2003). Staining methods applied to glycol methacrylate embedded tissue sections. Micron, 34, 365–372.CrossRefGoogle Scholar
  30. Cha, J. Y., Takano-Yamamoto, T., & Hwang, C. J. (2010). The effect of miniscrew taper morphology on insertion and removal torque in dogs. The International Journal of Oral & Maxillofacial Implants, 25, 777–783.Google Scholar
  31. Cheng, B. H., Chu, T. M., Chang, C., Kang, H. Y., & Huang, K. E. (2013a). Testosterone delivered with a scaffold is as effective as bone morphologic protein-2 in promoting the repair of critical-size segmental defect of femoral bone in mice. PLoS One, 8, e70234.CrossRefGoogle Scholar
  32. Cheng, L., Shi, Y., Ye, F., & Bu, H. (2013b). Osteoinduction of calcium phosphate biomaterials in small animals. Materials Science and Engineering C, 33, 1254–1260.CrossRefGoogle Scholar
  33. Cho, Y. C., Cha, J. Y., Hwang, C. J., Park, Y. C., Jung, H. S., & Yu, H. S. (2013). Biologic stability of plasma ion-implanted miniscrews. Korean Journal of Orthodontics, 43, 120–126.CrossRefGoogle Scholar
  34. Clarke, K. W., & Trim, C. M. (2013). Veterinary anaesthesia (11th ed.). Elsevier Health Sciences UK.Google Scholar
  35. Coan, P., Mollenhauer, J., Wagner, A., Muehleman, C., & Bravin, A. (2008). Analyzer-based imaging technique in tomography of cartilage and metal implants: A study at the ESRF. European Journal of Radiology, 68, S41–S48.CrossRefGoogle Scholar
  36. Crenshaw, J., Winslow, E. H., & Jacobson, A. F. (1999). New guidelines for preoperative fasting. AJN: The American Journal of Nursing, 99, 49.Google Scholar
  37. Dale, W. B., Peter, M. H., & Workgroup, F. T. S. I. P. G. W. (2004). Antimicrobial prophylaxis for surgery: An advisory statement from the national surgical infection prevention project. Clinical Infectious Diseases, 38, 1706–1715.Google Scholar
  38. Davis, M. A. (2008). Bioimaging of laboratory animals: The visual translation of molecular insights. Institute for Laboratory Animal Research Journal, 49, 1–3.CrossRefGoogle Scholar
  39. De Maria, E., Bonetti, L., Patrizi, G., Scrivener, J., Andraghetti, A., di Gregorio, F., et al. (2012). Implantation of a completely subcutaneous ICD system: Case report of a patient with Brugada syndrome and state of the art. Journal of Interventional Cardiac Electrophysiology, 34, 105–113.CrossRefGoogle Scholar
  40. Deleo, J. A. (2006). Basic science of pain. Journal of Bone and Joint Surgery, 88(Suppl 2), 58–62.CrossRefGoogle Scholar
  41. Diederich, C. J., & Hynynen, K. (1999). Ultrasound technology for hyperthermia. Ultrasound in Medicine and Biology, 25, 871–887.CrossRefGoogle Scholar
  42. Dincer, Y., & Sezgin, Z. (2014). Medical radiation exposure and human carcinogenesis-genetic and epigenetic mechanisms. Biomedical and Environmental Sciences, 27, 718–728.Google Scholar
  43. Donaldson, A. J., Thomson, H. E., Harper, N. J., & Kenny, N. W. (2009). Bone cement implantation syndrome. British Journal of Anaesthesia, 102, 12–22.CrossRefGoogle Scholar
  44. Driehuys, B., Nouls, J., Badea, A., Bucholz, E., Ghaghada, K., Petiet, A., & Hedlund, L. W. (2008). Small animal imaging with magnetic resonance microscopy. Institute for Laboratory Animal Research Journal, 49, 35–53.CrossRefGoogle Scholar
  45. Ferrari, E., Benhamou, M., Cerboni, P., & Marcel, B. (2005). Coronary syndromes following aspirin withdrawal: A special risk for late stent thrombosis. Journal of the American College of Cardiology, 45, 456–459.CrossRefGoogle Scholar
  46. Fish, R., Danneman, P. J., Brown, M., & Karas, A. (2011). Anesthesia and analgesia in laboratory animals (2011th ed.). New York: Academic Press, Elsevier Science.Google Scholar
  47. Fitzpatrick, J., Scott, M., & Nolan, A. (2006). Assessment of pain and welfare in sheep. Small Ruminant Research, 62, 55–61.CrossRefGoogle Scholar
  48. Fonseca, R., Branco, C., Soares, P., Correr-Sobrinho, L., Haiter-Neto, F., Fernandes-Neto, A., & Soares, C. (2006). Radiodensity of base, liner and luting dental materials. Clinical Oral Investigations, 10, 114–118.CrossRefGoogle Scholar
  49. Fossum, T. W. (2013). Small animal surgery textbook (4th ed.). Elsevier Health Sciences.Google Scholar
  50. Fowler, M. E. (2011). Restraint and handling of wild and domestic animals (3rd ed.). Wiley.Google Scholar
  51. Fox, J. G., Anderson, L. C., Loew, F. M., & Quimby, F. W. (2002). Laboratory animal medicine (2nd ed.). Elsevier Science.Google Scholar
  52. Freilich, M., C, M. P., Wei, M., Shafer, D., Schleier, P., Hortschansky, P., kompali, R., & Kuhn, L. (2008). Growth of new bone guided by implants in a murine calvarial model. Bone, 43, 781–788.Google Scholar
  53. Garber, J. C., Barbee, R. W., Bielitzki, J. T., Clayton, L. A., Donovan, J. C., Kohn, D. F., Lipman, N. S., Wood, G. A., & Wurbel, H. (2010). Guide for the care and use of laboratory animals (8th ed.). National Academies Press.Google Scholar
  54. Garcia, M. A. (2013). Laboratory animal anesthesia and analgesia. UC Santa Barbara: The Regents of the University of California.Google Scholar
  55. Gardel, L. S., Serra, L. A., Reis, R. L., & Gomes, M. E. (2013). Use of perfusion bioreactors and large animal models for long bone tissue engineering. Tissue Engineering Part B: Reviews, 20, 126–146.CrossRefGoogle Scholar
  56. Gavet, O., & Pines, J. (2010). Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Developmental Cell, 18, 533–543.CrossRefGoogle Scholar
  57. Giavaresi, G., Fini, M., Cigada, A., Chiesa, R., Rondelli, G., Rimondini, L., et al. (2003). Mechanical and histomorphometric evaluations of titanium implants with different surface treatments inserted in sheep cortical bone. Biomaterials, 24, 1583–1594.CrossRefGoogle Scholar
  58. Gibbon, W. W., Long, G., Barron, D. A., & O’Connor, P. J. (2002). Complications of orthopedic implants: Sonographic evaluation. Journal of Clinical Ultrasound, 30, 288–299.CrossRefGoogle Scholar
  59. Grimm, H. (2014). Ethics in laboratory animal science. In E. Jensen-Jarolim (Ed.), Comp Med (pp. 281–300). Vienna: Springer.Google Scholar
  60. Grimm, K. A., Tranquilli, W. J., & Lamont, L. A. (2011). Essentials of small animal anesthesia and analgesia (2nd ed.). Wiley.Google Scholar
  61. Guhad, F. (2005). Introduction to the 3Rs (Refinement, Reduction and Replacement). Journal of the American Association for Laboratory Animal Science, 44, 58–59.Google Scholar
  62. Haenle, M., Zietz, C., Lindner, T., Arndt, K., Vetter, A., Mittelmeier, W., Podbielski, A., & Bader, R. (2013). A model of implant-associated infection in the tibial metaphysis of rats. Scientific World Journal, 481975.Google Scholar
  63. Harkness, J. E., Turner, P. V., Vandewoude, S., & Wheler, C. L. (2013). Harkness and Wagner’s biology and medicine of rabbits and rodents (15th ed.). Wiley.Google Scholar
  64. Hartwig, V., Giovannetti, G., Vanello, N., Lombardi, M., Landini, L., & Simi, S. (2009). Biological effects and safety in magnetic resonance imaging: A review. International Journal of Environmental Research and Public Health, 6, 1778–1798.CrossRefGoogle Scholar
  65. Hawn, M. T., Richman, J. S., Vick, C. C., Deierhoi, R. J., Graham, L. A., Henderson, W. G., & Itani, K. M. F. (2013). Timing of surgical antibiotic prophylaxis and the risk of surgical site infection. Journal of the American Medical Association Surgery, 148, 649–657.Google Scholar
  66. Heaton, R. (1998). Serilization of surgical instruments. Community Eye Health, 11, 14–15.Google Scholar
  67. Hermawan, H., Dubé, D., & Mantovani, D. (2010). Developments in metallic biodegradable stents. Acta Biomaterialia, 6, 1693–1697.CrossRefGoogle Scholar
  68. Hildebrandt, I. J., Su, H., & Weber, W. A. (2008). Anesthesia and other considerations for in vivo imaging of small animals. Institute for Laboratory Animal Research Journal, 49, 17–26.CrossRefGoogle Scholar
  69. Holm, S. 2013. Declaration of Helsinki. In International encyclopedia of ethics. Blackwell Publishing Ltd.Google Scholar
  70. Huang, J., Triedman, J. K., Vasilyev, N. V., Suematsu, Y., Cleveland, R. O., & Dupont, P. E. (2007). Imaging artifacts of medical instruments in ultrasound-guided interventions. Journal of Ultrasound in Medicine, 26, 1303–1322.Google Scholar
  71. Issa, J. P. M., Do Nascimento, C., Bentley, M. V. L. B., Del Bel, E. A., Iyomasa, M. M., Sebald, W., & De Albuquerque Jr R. F. (2008). Bone repair in rat mandible by rhBMP-2 associated with two carriers. Micron, 39, 373–379.Google Scholar
  72. Jacobson, J. A. (2005). Musculoskeletal ultrasound and MRI: Which do i choose? Seminars in Musculoskeletal Radiology, 9, 135–149.CrossRefGoogle Scholar
  73. Johnson, J. B., Cogswell, P. M., McKusick, M. A., Binkovitz, L. A., Riederer, S. J., & Young, P. M. (2014). Pretreatment imaging of peripheral vascular malformations. Journal of Vascular Diagnostics, 2014, 121–126.CrossRefGoogle Scholar
  74. Joos, U., Buchter, A., Wiesmann, H. P., & Meyer, U. (2005). Strain driven fast osseointegration of implants. Head & Face Medicine, 1, 6.CrossRefGoogle Scholar
  75. Kato, Y. (2014). Anesthetic management of patients with arrhythmogenic right ventricular cardiomyopathy. Masui The Japanese Journal of Anesthesiology, 63, 39–48.Google Scholar
  76. Keeler, G. D., Durdik, J. M., & Stenken, J. A. (2014). Comparison of microdialysis sampling perfusion fluid components on the foreign body reaction in rat subcutaneous tissue. European Journal of Pharmaceutical Sciences, 57, 60–67.CrossRefGoogle Scholar
  77. Kingsbury, B. F. (2008). Histological technique: A guide for use in a laboratory course in histology. Read Books.Google Scholar
  78. Kneser, U., Stangenberg, L., Ohnolz, J., Buettner, O., Stern-Straeter, J., Möbest, D., et al. (2006). Evaluation of processed bovine cancellous bone matrix seeded with syngenic osteoblasts in a critical size calvarial defect rat model. Journal of Cellular and Molecular Medicine, 10, 695–707.CrossRefGoogle Scholar
  79. Kohn, D. F., Wixson, S. K., White, W. J., & Benson, G. J. (1997). Anesthesia and analgesia in laboratory animals. Elsevier Science.Google Scholar
  80. Kon, E., Muraglia, A., Corsi, A., Bianco, P., Marcacci, M., Martin, I., et al. (2000). Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. Journal of Biomedical Materials Research, 49, 328–337.CrossRefGoogle Scholar
  81. Kosonen, P., Vikman, S., Jensen, L. O., Lassen, J. F., Harnek, J., Olivecrona, G. K., et al. (2013). Intravascular ultrasound assessed incomplete stent apposition and stent fracture in stent thrombosis after bare metal versus drug-eluting stent treatment the Nordic Intravascular Ultrasound Study (NIVUS). International Journal of Cardiology, 168, 1010–1016.CrossRefGoogle Scholar
  82. Lane, M. A., Young, V. L., & Camins, B. C. (2010). Prophylactic antibiotics in aesthetic surgery. Aesthetic Surgery Journal, 30(6):859–871 (quiz 873).Google Scholar
  83. Langan, G. P., Harvey, R. C., O’Rourke, D., Fontenot, M. B., & Schumacher, J. (2000). Cardiopulmonary effects of sevoflurane in Garnett’s greater bush baby (Otolemur garnettii). Comparative Medicine, 50, 639–643.Google Scholar
  84. Lehtonen, S. R. K., Taskinen, E. I., & Isoniemi, H. M. (2001). Histological alterations in implant and one-year protocol biopsy specimens of renal allografts. Transplantation, 72, 1138–1144.CrossRefGoogle Scholar
  85. Li, J., Habibovic, P., Yuan, H., van den Doel, M., Wilson, C. E., de Wijn, J. R., et al. (2007). Biological performance in goats of a porous titanium alloy-biphasic calcium phosphate composite. Biomaterials, 28, 4209–4218.CrossRefGoogle Scholar
  86. Lips, K. S., Kauschke, V., Hartmann, S., Thormann, U., Ray, S., Schumacher, M., et al. (2014). Cholinergic nerve fibers in bone defects of a rat osteoporosis model and their regulation by implantation of bone substitution materials. Journal of Musculoskeletal and Neuronal Interactions, 14, 173–188.Google Scholar
  87. Liu, Y., Herman, B. A., Soneson, J. E., & Harris, G. R. (2014). Thermal safety simulations of transient temperature rise during acoustic radiation force-based ultrasound elastography. Ultrasound in Medicine and Biology, 40, 1001–1014.CrossRefGoogle Scholar
  88. Ljungqvist, O., & Søreide, E. (2003). Preoperative fasting. British Journal of Surgery, 90, 400–406.CrossRefGoogle Scholar
  89. Lucke, M., Schmidmaier, G., Sadoni, S., Wildemann, B., Schiller, R., Stemberger, A., et al. (2003). A new model of implant-related osteomyelitis in rats. Journal of Biomedical Materials Research. Part B, Applied Biomaterials, 67, 593–602.CrossRefGoogle Scholar
  90. Maltby, J. R. (1993). New guidelines for preoperative fasting. Canadian Journal of Anaesthesia, 40, R113–R121.CrossRefGoogle Scholar
  91. Mann, F. A., Constantinescu, G. M., & Yoon, H. Y. (2011). Fundamentals of small animal surgery. Wiley.Google Scholar
  92. Mao, K., Yang, Y., Li, J., Hao, L., Tang, P., Wang, Z., et al. (2009). Investigation of the histology and interfacial bonding between carbonated hydroxyapatite cement and bone. Biomedical Materials, 4, 045003.CrossRefGoogle Scholar
  93. Mapara, M., Thomas, B. S., & Bhat, K. M. (2012). Rabbit as an animal model for experimental research. Dental Research Journal (Isfahan), 9, 111–118.CrossRefGoogle Scholar
  94. Mardas, N., Dereka, X., Donos, N., & Dard, M. (2014). Experimental model for bone regeneration in oral and cranio-maxillo-facial surgery. Journal of Investigative Surgery, 27, 32–49.CrossRefGoogle Scholar
  95. Marie, M. (2005). Animal bioethics: Principles and teaching methods. Wageningen Academic Publishers.Google Scholar
  96. Martin, C. (1994). Antimicrobial prophylaxis in surgery general concepts and clinical guidelines. Infection Control and Hospital Epidemiology, 15, 463–471.CrossRefGoogle Scholar
  97. Matsuno, A., Tanaka, H., Iwamuro, H., Takanashi, S., Miyawaki, S., Nakashima, M., et al. (2006). Analyses of the factors influencing bone graft infection after delayed cranioplasty. Acta Neurochirurgica, 148, 535–540.CrossRefGoogle Scholar
  98. McGonigle, P., & Ruggeri, B. (2014). Animal models of human disease: Challenges in enabling translation. Biochemical Pharmacology, 87, 162–171.CrossRefGoogle Scholar
  99. Mckelvey, D., & Hollingshead, K. W. (2003). Veterinary anesthesia and analgesia. Mosby.Google Scholar
  100. Mclaughlin, J. E. (1983). Histological and histochemical methods: Theory and practice J. A. Kiernan Pergamon Press, Oxford, 1981 344 pages. £29.00 (hardback), £10.50 (paperback). Federation of European Biochemical Societies Letters, 151, 311.Google Scholar
  101. Morris, T. H. (1995). Antibiotic therapeutics in laboratory animals. Laboratory Animals, 29, 16–36.CrossRefGoogle Scholar
  102. Mueller, P. P., Arnold, S., Badar, M., Bormann, D., Bach, F. W., Drynda, A., et al. (2012). Histological and molecular evaluation of iron as degradable medical implant material in a murine animal model. Journal of Biomedical Materials Research, Part A, 100, 2881–2889.CrossRefGoogle Scholar
  103. Muir, W. W., & Hubbell, J. A. E. (2014). Handbook of veterinary anesthesia. Elsevier Health Sciences.Google Scholar
  104. Muschler, G. F., Raut, V. P., Patterson, T. E., Wenke, J. C., & Hollinger, J. O. (2009). The design and use of animal models for translational research in bone tissue engineering and regenerative medicine. Tissue Engineering Part B: Reviews, 16, 123–145.CrossRefGoogle Scholar
  105. Nielsen, C. S., Staud, R., & Price, D. D. (2009). Individual differences in pain sensitivity: Measurement, causation, and consequences. The Journal of Pain, 10, 231–237.CrossRefGoogle Scholar
  106. Nishii, T., Sakai, T., Takao, M., Yoshikawa, H., & Sugano, N. (2012). Ultrasound screening of periarticular soft tissue abnormality around metal-on-metal bearings. The Journal of Arthroplasty, 27, 895–900.CrossRefGoogle Scholar
  107. Nishimura, S., Kataoka, T., Hasegawa, T., Kobayashi, Y., Asawa, K., Nakata, S., et al. (2012). Detailed observation of arterial healing after stent implantation in swine arteries by using optical coherence tomography. Osaka City Medical Journal, 58, 1–11.Google Scholar
  108. Noviana, D., Aliambar, S. H., Ulum, M. F., & Siswandi, R. (2012a). Small animal diagnostic ultrasound [Diagnosis ultrasonografi pada hewan kecil] 1, 3–8.Google Scholar
  109. Noviana, D., Estuningsih, S., Ulum, M. F., Paramitha, D., Utami, N. F., Utami, N. D., & Hermawan, H. (2012b). In vivo study of iron based material foreign bodies in mice (Mus musculus albinus). In The 7th International Conference on Biomedical Engineering and Medical Application (ICBEMA) (pp. 91–94).Google Scholar
  110. Noviana, D., Nasution, A. K., Ulum, M. F., & Hermawan, H. (2013a). Degradation of Fe-bioceramic composites at two different implantation sites in sheep animal model observed by X-ray radiography. European Cells & Materials, 26, 56.Google Scholar
  111. Noviana, D., Nasution, A. K., Ulum, M. F., & Hermawan, H. (2013b). Monitoring of early biodegradation of Fe-bioceramic composites by B-mode ultrasonography imaging in sheep animal model. European Cells & Materials, 26, 57.Google Scholar
  112. Obernier, J. A., & Baldwin, R. L. (2006). Establishing an appropriate period of acclimatization following transportation of laboratory animals. Institute for Laboratory Animal Research Journal, 47, 364–369.CrossRefGoogle Scholar
  113. Ozawa, T., Mickle, D. A. G., Weisel, R. D., Koyama, N., Wong, H., Ozawa, S., & Li, R.-K. (2002). Histologic changes of nonbiodegradable and biodegradable biomaterials used to repair right ventricular heart defects in rats. Journal of Thoracic and Cardiovascular Surgery, 124, 1157–1164.CrossRefGoogle Scholar
  114. Page, D. L. (1983). Theory and practice of histological techniques. Human Pathology, 14, 925–926.CrossRefGoogle Scholar
  115. Palmeri, M. L., & Nightingale, K. R. (2004). On the thermal effects associated with radiation force imaging of soft tissue. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, 51, 551–565.CrossRefGoogle Scholar
  116. Panjaitan, B., Gunanti, Noviana, D., Ulum, M. F., & Sukmana, I. (2014). The effect of porous tantalum coated by hydroxyapatatite implantation in sprague dawley rat on red blood parameters. Journal Kedokteran Hewan, 8, 151–153.Google Scholar
  117. Paramitha, D., Estuningsih, S., Noviana, D., Ulum, M. F., & Hermawan, H. (2013). Distribution of Fe-based degradable materials in mice skeletal muscle. European Cells & Materials, 26, 55.Google Scholar
  118. Park, S.-J., Park, D.-W., Kim, Y.-H., Kang, S.-J., Lee, S.-W., Lee, C. W., et al. (2010). Duration of dual antiplatelet therapy after implantation of drug-eluting stents. New England Journal of Medicine, 362, 1374–1382.CrossRefGoogle Scholar
  119. Pearce, A. I., Richards, R. G., Milz, S., Schneider, E., & Pearce, S. G. (2007). Animal models for implant biomaterial research in bone: A review. European Cells & Materials, 13, 1–10.Google Scholar
  120. Phillips, C. (2008). The welfare of animals: The silent majority. Springer.Google Scholar
  121. Piccinini, M., Cugnoni, J., Botsis, J., Ammann, P., & Wiskott, A. (2014). Influence of gait loads on implant integration in rat tibiae: Experimental and numerical analysis. Journal of Biomechanics, 47, 3255–3263.CrossRefGoogle Scholar
  122. Pithon, M. M., Figueiredo, D. S., & Oliveira, D. D. (2013). Mechanical evaluation of orthodontic mini-implants of different lengths. Journal of Oral and Maxillofacial Surgery, 71, 479–486.CrossRefGoogle Scholar
  123. Portaluppi, F., Smolensky, M. H., & Touitou, Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiology International, 27, 1911–1929.CrossRefGoogle Scholar
  124. Potapova, T. A., Sivakumar, S., Flynn, J. N., Li, R., & Gorbsky, G. J. (2011). Mitotic progression becomes irreversible in prometaphase and collapses when Wee1 and Cdc25 are inhibited. Molecular Biology of the Cell, 22, 1191–1206.CrossRefGoogle Scholar
  125. Reefhuis, J., Honein, M. A., Whitney, C. G., Chamany, S., Mann, E. A., Biernath, K. R., et al. (2003). Risk of bacterial meningitis in children with cochlear implants. New England Journal of Medicine, 349, 435–445.CrossRefGoogle Scholar
  126. Reinhardt, C. A. (2008). Alternatives to animal testing: New ways in the biomedical sciences, trends & progress. Wiley.Google Scholar
  127. Richardson, C. A., & Flecknell, P. A. (2005). Anaesthesia and post-operative analgesia following experimental surgery in laboratory rodents: Are we making progress? ATLA: Alternatives to Laboratory Animals, 33, 119–127.Google Scholar
  128. Romano, M. M., Soares, M. S., Pastore, C. A., Tornelli, M. J., De Oliveira Guare, R., & Adde, C. A. (2012). A study of effectiveness of midazolam sedation for prevention of myocardial arrhythmias in endosseous implant placement. Clinical Oral Implants Research, 23, 489–495.Google Scholar
  129. Rothman, K. J., & Michels, K. B. (2000). Declaration of Helsinki should be strengthened. BMJ. British Medical Journal, 321, 442–445.CrossRefGoogle Scholar
  130. Ruehe, B., Niehues, S., Heberer, S., & Nelson, K. (2009). Miniature pigs as an animal model for implant research: Bone regeneration in critical-size defects. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology, 108, 699–706.CrossRefGoogle Scholar
  131. Russell, W. M. S., & Burch, R. L. (1959). The principles of humane experimental technique. Methuen.Google Scholar
  132. Sacher, F., Probst, V., Iesaka, Y., Jacon, P., Laborderie, J., Mizon-Gérard, F., et al. (2006). Outcome after implantation of a cardioverter-defibrillator in patients with brugada syndrome: A multicenter study. Circulation, 114, 2317–2324.CrossRefGoogle Scholar
  133. Sachse, A., Wagner, A., Keller, M., Wagner, O., Wetzel, W. D., Layher, F., et al. (2005). Osteointegration of hydroxyapatite-titanium implants coated with nonglycosylated recombinant human bone morphogenetic protein-2 (BMP-2) in aged sheep. Bone, 37, 699–710.CrossRefGoogle Scholar
  134. Schliephake, H., Gruber, R., Dard, M., Wenz, R., & Scholz, S. (2004). Repair of calvarial defects in rats by prefabricated hydroxyapatite cement implants. Journal of Biomedical Materials Research, Part A, 69A, 382–390.CrossRefGoogle Scholar
  135. Schumacher, J., Citino, S. B., Hernandez, K., Hutt, J., & Dixon, B. (1997). Cardiopulmonary and anesthetic effects of propofol in wild turkeys. American Journal of Veterinary Research, 58, 1014–1017.Google Scholar
  136. Sennerby, L., Dasmah, A., Larsson, B., & Iverhed, M. (2005). Bone tissue responses to surface-modified zirconia implants: A histomorphometric and removal torque study in the rabbit. Clinical Implant Dentistry and Related Research, 7, s13–s20.CrossRefGoogle Scholar
  137. Shanks, N., Greek, R., & Greek, J. (2009). Are animal models predictive for humans? PEHM: Philosophy, Ethics, and Humanities in Medicine, 4, 2–2Google Scholar
  138. Shiver, S. A., Lyon, M., & Blaivas, M. (2005). Detection of metallic ocular foreign bodies with handheld sonography in a porcine model. Journal of Ultrasound in Medicine, 24, 1341–1346.Google Scholar
  139. Sneddon, L. U., Elwood, R. W., Adamo, S. A., & Leach, M. C. (2014). Defining and assessing animal pain. Animal Behaviour, 97, 201–212.CrossRefGoogle Scholar
  140. Sofka, C. M., Potter, H. G., Adler, R. S., & Pavlov, H. (2006). Musculoskeletal imaging update: Current applications of advanced imaging techniques to evaluate the early and long-term complications of patients with orthopedic implants. Hospital for Special Surgery Journal, 2, 73–77.Google Scholar
  141. Stokes, W. S. (2002). Humane endpoints for laboratory animals used in regulatory testing. Institute for Laboratory Animal Research Journal, 43, S31–S38.Google Scholar
  142. Suckow, M. A., Stevens, K. A., & Wilson, R. P. (2012). The laboratory rabbit, guinea pig, hamster, and other rodents. Elsevier Academic Press.Google Scholar
  143. Sul, Y.-T., Johansson, C. B., & Albrektsson, T. (2002). Oxidized titanium screws coated with calcium ions and their performance in rabbit bone. The International Journal of Oral & Maxillofacial Implants, 17, 625–634.Google Scholar
  144. Tchelepi, H., & Ralls, P. W. (2009). Color comet-tail artifact: Clinical applications. American Journal of Roentgenology, 192, 11–18.CrossRefGoogle Scholar
  145. Teefey, S. A., Middleton, W. D., Patel, V., Hildebolt, C. F., & Boyer, M. I. (2004). The accuracy of high-resolution ultrasound for evaluating focal lesions of the hand and wrist. The Journal of Hand Surgery, 29, 393–399.CrossRefGoogle Scholar
  146. Tempany, C. C., & McNeil, B. J. (2001). Advances in biomedical imaging. Journal of the American Medical Association, 285, 562–567.CrossRefGoogle Scholar
  147. Törnqvist, E., Annas, A., Granath, B., Jalkesten, E., Cotgreave, I., & Öberg, M. (2014). Strategic focus on 3R principles reveals major reductions in the use of animals in pharmaceutical toxicity testing. PLoS One, 9, e101638.CrossRefGoogle Scholar
  148. Touitou, Y., Portaluppi, F., Smolensky, M. H., & Rensing, L. (2004). Ethical principles and standards for the conduct of human and animal biological rhythm research. Chronobiology International, 21, 161–170.CrossRefGoogle Scholar
  149. Tranquilli, W. J., Thurmon, J. C., & Grimm, K. A. (2013). Lumb and Jones’ veterinary anesthesia and analgesia. Wiley.Google Scholar
  150. Troyer, D. L., Cash, W. C., Provo-Klimek, J., & Kennedy, G. A. (2002). A novel method for preparing histology slides without a microtome. Anatomia, Histologia, Embryologia, 31, 129–131.CrossRefGoogle Scholar
  151. Üçeyler, N., Eberle, T., Rolke, R., Birklein, F., & Sommer, C. (2007). Differential expression patterns of cytokines in complex regional pain syndrome. Pain, 132, 195–205.CrossRefGoogle Scholar
  152. Ulum, M. F., Arafat, A., Noviana, D., Yusop, A. H., Nasution, A. K., Kadir, M. R. A., & Hermawan, H. (2014a). In vitro and in vivo degradation evaluation of novel iron-bioceramic composites for bone implant applications. Materials Science and Engineering C, 36, 336–344.CrossRefGoogle Scholar
  153. Ulum, M. F., Kurniawan, A., Arif, A., Shatilla, G. S., Affidatunissa, K., Indrian, R., Noviana, D., & Gunanti. (2012). In vivo study of wild brown silk (Attacus atlas L.) for surgical thread as new biomaterial expectation. In The 7th International Conference on Biomedical Engineering and Medical Application (ICBEMA) (pp. 126–129).Google Scholar
  154. Ulum, M. F., Murni, N. S., Noviana, D., & Hermawan, H. (2014b). Peri-implant assessment of Fe-HA composite for temporary bone implants. European Cells & Materials, 28, 81.Google Scholar
  155. Ulum, M. F., Nasution, A. K., Yusop, A. H., Arafat, A., Kadir, M. R. A., Juniantito, V., et al. (2015). Evidences of in vivo bioactivity of Fe-bioceramic composites for temporary bone implants. Journal of Biomedical Materials Research. Part B, Applied Biomaterials, 103B, 1354–1365.CrossRefGoogle Scholar
  156. Ulum, M. F., Paramitha, D., Estuningsih, S., Noviana, D., & Hermawan, H. (2013). Metal ion level and polymorphonuclear leukocyte cells number as determination factors for early in vivo rejection of biodegradable metals. European Cells & Materials, 26, 59.Google Scholar
  157. Vepari, C., & Kaplan, D. L. (2007). Silk as a biomaterial. Progress in Polymer Science, 32, 991–1007.CrossRefGoogle Scholar
  158. Viñuela-Fernández, I., Jones, E., Welsh, E. M., & Fleetwood-Walker, S. M. (2007). Pain mechanisms and their implication for the management of pain in farm and companion animals. The Veterinary Journal, 174, 227–239.CrossRefGoogle Scholar
  159. Walker, K. A., Duffield, T. F., & Weary, D. M. (2011). Identifying and preventing pain during and after surgery in farm animals. Applied Animal Behaviour Science, 135, 259–265.CrossRefGoogle Scholar
  160. Wang, H., Li, Y., Zuo, Y., Li, J., Ma, S., & Cheng, L. (2007). Biocompatibility and osteogenesis of biomimetic nano-hydroxyapatite/polyamide composite scaffolds for bone tissue engineering. Biomaterials, 28, 3338–3348.CrossRefGoogle Scholar
  161. Weary, D. M., Niel, L., Flower, F. C., & Fraser, D. (2006). Identifying and preventing pain in animals. Applied Animal Behaviour Science, 100, 64–76.CrossRefGoogle Scholar
  162. Wick, M. R. (2012). Histochemistry as a tool in morphological analysis: A historical review. Annals of Diagnostic Pathology, 16, 71–78.CrossRefGoogle Scholar
  163. Willbold, E., & Witte, F. (2010). Histology and research at the hard tissue–implant interface using Technovit 9100 new embedding technique. Acta Biomaterialia, 6, 4447–4455.CrossRefGoogle Scholar
  164. Wilson, G. S., & Gifford, R. (2005). Biosensors for real-time in vivo measurements. Biosensors & Bioelectronics, 20, 2388–2403.CrossRefGoogle Scholar
  165. World Medical Association. (2001). World Medical Association Declaration of Helsinki. Ethical principles for medical research involving human subjects. Bulletin of the World Health Organization, 79, 373–374.Google Scholar
  166. Yang, R. N., Ye, F., Cheng, L. J., Wang, J. J., Lu, X. F., Shi, Y. J., et al. (2011). Osteoinduction by Ca-P biomaterials implanted into the muscles of mice. Journal of Zheijang University Science B - Biomedicine & Biotechnology, 12, 582–590.Google Scholar
  167. Yavari, S. A., van der Stok, J., Ahmadi, S. M., Wauthle, R., Schrooten, J., Weinans, H., & Zadpoor, A. A. (2014). Mechanical analysis of a rodent segmental bone defect model: The effects of internal fixation and implant stiffness on load transfer. Journal of Biomechanics, 47, 2700–2708.CrossRefGoogle Scholar
  168. Yu, K., Chen, L., Zhao, J., Li, S., Dai, Y., Huang, Q., & Yu, Z. (2012). In vitro corrosion behavior and in vivo biodegradation of biomedical β-Ca3(PO4)2/Mg–Zn composites. Acta Biomaterialia, 8, 2845–2855.CrossRefGoogle Scholar
  169. Zhang, X., Vandamme, K., Torcasio, A., Ogawa, T., van Lenthe, G. H., Naert, I., & Duyck, J. (2012). In vivo assessment of the effect of controlled high- and low-frequency mechanical loading on peri-implant bone healing. Journal of the Royal Society, Interface, 9, 1697–1704.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Deni Noviana
    • 1
  • Sri Estuningsih
    • 1
  • Mokhamad Fakhrul Ulum
    • 1
  1. 1.Bogor Agricultural UniversityBogorIndonesia

Personalised recommendations