Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

A large animal model of periodontal defects in bisphosphonate-related osteonecrosis of the jaw: a comparison of clinical and radiological findings

  • Marius Otto (Department of Pediatric Surgery, Pediatric Urology and Pediatric Orthopedics, DRK Children's Hospital Siegen) ;
  • Andreas Neff (Department of Oral and Maxillofacial Surgery, University Hospital Marburg) ;
  • Thomas Ziebart (Department of Oral and Maxillofacial Surgery, University Hospital Marburg) ;
  • Frank Halling (Department of Oral and Maxillofacial Surgery, University Hospital Marburg)
  • Received : 2022.11.29
  • Accepted : 2023.05.18
  • Published : 2024.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: The objective of this study was to demonstrate the suitability of cone-beam computed tomography (CBCT) for in vivo research in periodontology, with implications for oral implantology, facial traumatology, and all disciplines involved in treating patients with bisphosphonate-related osteonecrosis of the jaw (BRONJ). Methods: Halves of the jaws of 9 Swiss mountain sheep, assigned to a control group (n=3), an osteoporosis group (n=3) and a zoledronate-exposed group (n=3), were examined. Clinical and radiological evaluations were conducted using CBCT imaging to assess whether periodontitis and bone defects were observed to a significant extent after surgical tooth extraction. Results: In contrast to the control and osteoporosis groups, the zoledronate group exhibited significant residual bone defects following tooth extraction (P<0.05). CBCT more objectively revealed these effects and enabled a numerical evaluation (in mm3). Conclusions: Evaluating residual defects in bone blocks from sheep using CBCT analysis was found to be as effective as a clinical examination conducted by specialists in oral and maxillofacial surgery. The strong correlation between radiological findings and clinical conditions suggests that CBCT may become increasingly important in the future, particularly in periodontological research related to BRONJ.

Keywords

Acknowledgement

Special thanks are extended for the resources and collaborative analysis provided by the Department for Oral and Maxillofacial Surgery, Head Prof. Dr. B. Al-Nawas and the Department of Radiology, and Head Prof. Dr. C. Duber of the University Medical Center Mainz.

References

  1. Marx RE. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic. J Oral Maxillofac Surg 2003;61:1115-7. https://doi.org/10.1016/S0278-2391(03)00720-1
  2. Ruggiero SL, Dodson TB, Assael LA, Landesberg R, Marx RE, Mehrotra B, et al. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws--2009 update. J Oral Maxillofac Surg 2009;67:2-12.
  3. Walter C, Laux C, Sagheb K. Radiologic bone loss in patients with bisphosphonate-associated osteonecrosis of the jaws: a case-control study. Clin Oral Investig 2014;18:385-90. https://doi.org/10.1007/s00784-013-0974-7
  4. Marx RE, Cillo JE Jr, Ulloa JJ. Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg 2007;65:2397-410. https://doi.org/10.1016/j.joms.2007.08.003
  5. Eggers G, Klein J, Welzel T, Muhling J. Geometric accuracy of digital volume tomography and conventional computed tomography. Br J Oral Maxillofac Surg 2008;46:639-44. https://doi.org/10.1016/j.bjoms.2008.03.019
  6. Kasaj A, Willershausen B. Digital volume tomography for diagnostics in periodontology. Int J Comput Dent 2007;10:155-68.
  7. Raichur PS, Setty SB, Thakur SL, Naikmasur VG. Comparison of radiovisiography and digital volume tomography to direct surgical measurements in the detection of infrabony defects. J Clin Exp Dent 2012;4:e43-7. https://doi.org/10.4317/jced.50711
  8. Stockmann P, Hinkmann FM, Lell MM, Fenner M, Vairaktaris E, Neukam FW, et al. Panoramic radiograph, computed tomography or magnetic resonance imaging. Which imaging technique should be preferred in bisphosphonate-associated osteonecrosis of the jaw? A prospective clinical study. Clin Oral Investig 2010;14:311-7.
  9. Voss P, Ludwig U, Poxleitner P, Bergmaier V, El-Shafi N, von Elverfeldt D, et al. Evaluation of BP-ONJ in osteopenic and healthy sheep: comparing ZTE-MRI with µCT. Dentomaxillofac Radiol 2016;45:20150250.
  10. Voss PJ, Stoddart M, Ziebart T, Zeiter S, Nelson K, Bittermann G, et al. Zoledronate induces osteonecrosis of the jaw in sheep. J Craniomaxillofac Surg 2015;43:1133-8. https://doi.org/10.1016/j.jcms.2015.04.020
  11. Voss PJ, Stoddart MJ, Bernstein A, Schmelzeisen R, Nelson K, Stadelmann V, et al. Zoledronate induces bisphosphonate-related osteonecrosis of the jaw in osteopenic sheep. Clin Oral Investig 2016;20:31-8. https://doi.org/10.1007/s00784-015-1468-6
  12. Zarrinkalam MR, Beard H, Schultz CG, Moore RJ. Validation of the sheep as a large animal model for the study of vertebral osteoporosis. Eur Spine J 2009;18:244-53. https://doi.org/10.1007/s00586-008-0813-8
  13. Ruggiero SL. Bisphosphonate-related osteonecrosis of the jaw: an overview. Ann N Y Acad Sci 2011;1218:38-46. https://doi.org/10.1111/j.1749-6632.2010.05768.x
  14. Fundamentals of mathematics: exercise materials for secondary level I/II: 5th to 10th school year: basic knowledge with media. Berlin: Cornelsen-Verlag; 2022.
  15. Assiri H, Dawasaz AA, Alahmari A, Asiri Z. Cone beam computed tomography (CBCT) in periodontal diseases: a Systematic review based on the efficacy model. BMC Oral Health 2020;20:191.
  16. Mol A, Balasundaram A. In vitro cone beam computed tomography imaging of periodontal bone. Dentomaxillofac Radiol 2008;37:319-24. https://doi.org/10.1259/dmfr/26475758
  17. Mengel R, Candir M, Shiratori K, Flores-de-Jacoby L. Digital volume tomography in the diagnosis of periodontal defects: an in vitro study on native pig and human mandibles. J Periodontol 2005;76:665-73. https://doi.org/10.1902/jop.2005.76.5.665
  18. Almeida VC, Pinheiro LR, Salineiro FC, Mendes FM, Neto JB, Cavalcanti MG, et al. Performance of cone beam computed tomography and conventional intraoral radiographs in detecting interproximal alveolar bone lesions: a study in pig mandibles. BMC Oral Health 2017;17:100.
  19. Kluge A, Neudert M, Kunert-Keil C, Lailach S, Zahnert T, Kemper M. The obliteration of noncritical size bone defects with bone dust or bone replacement material (bioactive glass S53P4). Otol Neurotol 2019;40:e415-23. https://doi.org/10.1097/MAO.0000000000002178
  20. Miller F, Burghard A, Salcher R, Scheper V, Leibold W, Lenarz T, et al. Treatment of middle ear ventilation disorders: sheep as animal model for stenting the human Eustachian tube--a cadaver study. PLos One 2014;9:e113906.
  21. Goldhahn J, Neuhoff D, Schaeren S, Steiner B, Linke B, Aebi M, et al. Osseointegration of hollow cylinder based spinal implants in normal and osteoporotic vertebrae: a sheep study. Arch Orthop Trauma Surg 2006;126:554-61. https://doi.org/10.1007/s00402-006-0185-7
  22. Lill CA, Fluegel AK, Schneider E. Sheep model for fracture treatment in osteoporotic bone: a pilot study about different induction regimens. J Orthop Trauma 2000;14:559-65. https://doi.org/10.1097/00005131-200011000-00007
  23. Lill CA, Fluegel AK, Schneider E, Schneider E. Effect of ovariectomy, malnutrition and glucocorticoid application on bone properties in sheep: a pilot study. Osteoporos Int 2002;13:480-6. https://doi.org/10.1007/s001980200058
  24. Cankaya AB, Erdem MA, Isler SC, Demircan S, Soluk M, Kasapoglu C, et al. Use of cone-beam computerized tomography for evaluation of bisphosphonate-associated osteonecrosis of the jaws in an experimental rat model. Int J Med Sci 2011;8:667-72. https://doi.org/10.7150/ijms.8.667
  25. Wilde F, Heufelder M, Lorenz K, Liese S, Liese J, Helmrich J, et al. Prevalence of cone beam computed tomography imaging findings according to the clinical stage of bisphosphonate-related osteonecrosis of the jaw. Oral Surg Oral Med Oral Pathol Oral Radiol 2012;114:804-11. https://doi.org/10.1016/j.oooo.2012.08.458
  26. Lorenzo-Pouso AI, Perez-Sayans M, Chamorro-Petronacci C, Gandara-Vila P, Lopez-Jornet P, Carballo J, et al. Association between periodontitis and medication-related osteonecrosis of the jaw: a systematic review and meta-analysis. J Oral Pathol Med 2020;49:190-200. https://doi.org/10.1111/jop.12963
  27. Aghaloo TL, Kang B, Sung EC, Shoff M, Ronconi M, Gotcher JE, et al. Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat. J Bone Miner Res 2011;26:1871-82. https://doi.org/10.1002/jbmr.379
  28. Williams DW, Ho K, Lenon A, Kim S, Kim T, Gwack Y, et al. Long-term ligature-induced periodontitis exacerbates development of bisphosphonate-related osteonecrosis of the jaw in mice. J Bone Miner Res 2022;37:1400-10. https://doi.org/10.1002/jbmr.4614
  29. Dommisch H, Kuzmanova D, Jonsson D, Grant M, Chapple I. Effect of micronutrient malnutrition on periodontal disease and periodontal therapy. Periodontol 2000 2018;78:129-53. https://doi.org/10.1111/prd.12233
  30. Leite de Marcelos PG, Perez DE, Soares DM, de Araujo SS, Evencio LB, Pontual ML, et al. The effects of zoledronic acid on the progression of experimental periodontitis in rats: histological and microtomographic analyses. J Periodontal Implant Sci 2021;51:264-75. https://doi.org/10.5051/jpis.2001100055
  31. Cutress TW, Schroeder HE. Histopathology of periodontitis ('broken-mouth') in sheep: a further consideration. Res Vet Sci 1982;33:64-9. https://doi.org/10.1016/S0034-5288(18)32361-0
  32. Kwoen MJ, Park JH, Kim KS, Lee JR, Kim JW, Lee H, et al. Association between periodontal disease, tooth extraction, and medication-related osteonecrosis of the jaw in women receiving bisphosphonates: a national cohort-based study. J Periodontol 2023;94:98-107. https://doi.org/10.1002/JPER.21-0611
  33. Berg BI, Mueller AA, Augello M, Berg S, Jaquiery C. Imaging in patients with bisphosphonate-associated osteonecrosis of the jaws (MRONJ). Dent J (Basel) 2016;4:29.
  34. Ruetters M, Kim TS, Hagenfeld D, Kronsteiner D, Gehrig H, Lux CJ, et al. Ex vivo assessment of the buccal and oral bone by CBCT. J Orofac Orthop 2023;84:41-8. https://doi.org/10.1007/s00056-021-00335-w