Periodontal disease and bisphosphonates induce osteonecrosis of the jaws in the rat

Journal of Bone and Mineral Research

Volumn 26, Issue 8, 2011, Pages 1871-1882

  Aghaloo, Tara L ^a   Kang, Ben ^a   Sung, Eric C ^a   Shoff, Michael ^a   Ronconi, Matthew ^a   Gotcher, Jack E ^b   Bezouglaia, Olga ^a   Dry, Sarah M ^c   Tetradis, Sotirios ^a,d  

^a UCLA SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

bisphosphonate; BRONJ; ONJ; osteonecrosis of the jaws; periodontitis; rat model

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; ZOLEDRONIC ACID;

ALVEOLAR BONE; ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DENSITY; CONTROLLED STUDY; DRUG ACTIVITY; HISTOPATHOLOGY; JAW OSTEONECROSIS; MALE; MAXILLOFACIAL DISORDER; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; PATHOPHYSIOLOGY; PERIODONTAL DISEASE; RAT;

ANIMALS; DIPHOSPHONATES; HUMANS; IN SITU NICK-END LABELING; JAW DISEASES; MALE; MAXILLA; MODELS, BIOLOGICAL; OSTEOCYTES; OSTEOGENESIS; OSTEONECROSIS; PERIODONTAL DISEASES; RATS; RATS, SPRAGUE-DAWLEY; X-RAY MICROTOMOGRAPHY;

EID: 79958026496     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.379     Document Type: Article

References (63)

1. Khosla S, Burr D, Cauley J, et al. Bisphosphonate-associated osteonecrosis of the jaw: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2007; 22: 1479-1491. (Pubitemid 351229318)
2. Ruggiero SL, Dodson TB, Assael LA, Landesberg R, Marx RE, Mehrotra B,. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws: 2009 update. J Oral Maxillofac Surg. 2009; 67: S2-12.
3. Marx RE, Sawatari Y, Fortin M, Broumand V,. Bisphosphonate-induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk factors, recognition, prevention, and treatment. J Oral Maxillofac Surg. 2005; 63: 1567-1575. (Pubitemid 41525412)
4. Marx RE,. A new concept in the treatment of osteoradionecrosis. J Oral Maxillofac Surg. 1983; 41: 351-357. (Pubitemid 13054600)
5. Mehrotra B, Ruggiero S,. Bisphosphonate complications including osteonecrosis of the jaw. Hematology, Am Soc Hematol Educ Program. 2006; 356-360: 515.
6. Bamias A, Kastritis E, Bamia C, et al. Osteonecrosis of the jaw in cancer after treatment with bisphosphonates: incidence and risk factors. J Clin Oncol. 2005; 23: 8580-8587. (Pubitemid 46211499)
7. Ruggiero SL, Mehrotra B, Rosenberg TJ, Engroff SL,. Osteonecrosis of the jaws associated with the use of bisphosphonates: a review of 63 cases. J Oral Maxillofac Surg. 2004; 62: 527-534. (Pubitemid 38542516)
8. Tarassoff P, Csermak K,. Avascular necrosis of the jaws: risk factors in metastatic cancer patients. J Oral Maxillofac Surg. 2003; 61: 1238-1239. (Pubitemid 37193509)
9. Bone HG, Hosking D, Devogelaer JP, et al. Ten years' experience with alendronate for osteoporosis in postmenopausal women. N Engl J Med. 2004; 350: 1189-1199. (Pubitemid 38339363)
10. Zervas K, Verrou E, Teleioudis Z, et al. Incidence, risk factors and management of osteonecrosis of the jaw in patients with multiple myeloma: a single-centre experience in 303 patients. Br J Haematol. 2006; 134: 620-623. (Pubitemid 44253605)
11. Durie BG, Katz M, Crowley J,. Osteonecrosis of the jaw and bisphosphonates. N Engl J Med. 2005; 353: 99-102; discussion 99-102.
12. Dimopoulos MA, Kastritis E, Anagnostopoulos A, et al. Osteonecrosis of the jaw in patients with multiple myeloma treated with bisphosphonates: evidence of increased risk after treatment with zoledronic acid. Haematologica. 2006; 91: 968-971. (Pubitemid 44023154)
13. Hoff AO, Toth BB, Altundag K, et al. Frequency and risk factors associated with osteonecrosis of the jaw in cancer patients treated with intravenous bisphosphonates. J Bone Miner Res. 2008; 23: 826-836. (Pubitemid 351768801)
14. Walter C, Al-Nawas B, Grotz KA, et al. Prevalence and Risk Factors of Bisphosphonate-Associated Osteonecrosis of the Jaw in Prostate Cancer Patients with Advanced Disease Treated with Zoledronate. Eur Urol. 2008.
15. Boonyapakorn T, Schirmer I, Reichart PA, Sturm I, Massenkeil G,. Bisphosphonate-induced osteonecrosis of the jaws: prospective study of 80 patients with multiple myeloma and other malignancies. Oral Oncol. 2008; 44: 857-869.
16. Mavrokokki T, Cheng A, Stein B, Goss A,. Nature and frequency of bisphosphonate-associated osteonecrosis of the jaws in Australia. J Oral Maxillofac Surg. 2007; 65: 415-423. (Pubitemid 46343586)
17. Lo JC, O'Ryan FS, Gordon NP, et al. Prevalence of osteonecrosis of the jaw in patients with oral bisphosphonate exposure. J Oral Maxillofac Surg. 2010; 68: 243-253.
18. Ficarra G, Beninati F, Rubino I, et al. Osteonecrosis of the jaws in periodontal patients with a history of bisphosphonates treatment. J Clin Periodontol. 2005; 32: 1123-1128. (Pubitemid 41499467)
19. Bilezikian JP,. Osteonecrosis of the jaw-do bisphosphonates pose a risk? N Engl J Med. 2006; 355: 2278-2281. (Pubitemid 44837776)
20. Marx R,. Oral & Intravenous Bisphosphonate-Induced Osteonecrosis of the Jaws. Chicago: Quintessence Publishing Co., 2007.
21. Dimopoulos MA, Kastritis E, Bamia C, et al. Reduction of osteonecrosis of the jaw (ONJ) after implementation of preventive measures in patients with multiple myeloma treated with zoledronic acid. Ann Oncol. 2009; 20: 117-120.
22. Ripamonti CI, Maniezzo M, Campa T, et al. Decreased occurrence of osteonecrosis of the jaw after implementation of dental preventive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan. Ann Oncol. 2009; 20: 137-145.
23. Kyle RA, Yee GC, Somerfield MR, et al. American Society of Clinical Oncology 2007 clinical practice guideline update on the role of bisphosphonates in multiple myeloma. J Clin Oncol. 2007; 25: 2464-2472. (Pubitemid 46999218)
24. Quinn R,. Comparing rat's to human's age: how old is my rat in people years? Nutrition. 2005; 21: 775-777. (Pubitemid 40733575)
25. Rogers JE, Li F, Coatney DD, et al. Actinobacillus actinomycetemcomitans lipopolysaccharide-mediated experimental bone loss model for aggressive periodontitis. J Periodontol. 2007; 78: 550-558.
26. Bianchi SD, Scoletta M, Cassione FB, Migliaretti G, Mozzati M,. Computerized tomographic findings in bisphosphonate-associated osteonecrosis of the jaw in patients with cancer. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007; 104: 249-258.
27. Bedogni A, Blandamura S, Lokmic Z, et al. Bisphosphonate-associated jawbone osteonecrosis: a correlation between imaging techniques and histopathology. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008; 105: 358-364.
28. Bi Y, Gao Y, Ehirchiou D, et al. Bisphosphonates cause osteonecrosis of the jaw-like disease in mice. Am J Pathol. 2010; 177: 280-290.
29. Coleman RE, Major P, Lipton A, et al. Predictive value of bone resorption and formation markers in cancer patients with bone metastases receiving the bisphosphonate zoledronic acid. J Clin Oncol. 2005; 23: 4925-4935. (Pubitemid 46223998)
30. Stewart AF,. Clinical practice. Hypercalcemia associated with cancer. N Engl J Med. 2005; 352: 373-379.
31. Duivenvoorden WC, Vukmirovic-Popovic S, Kalina M, Seidlitz E, Singh G,. Effect of zoledronic acid on the doxycycline-induced decrease in tumour burden in a bone metastasis model of human breast cancer. Br J Cancer. 2007; 96: 1526-1531. (Pubitemid 46762946)
32. Diel IJ, Body JJ, Lichinitser MR, et al. Improved quality of life after long-term treatment with the bisphosphonate ibandronate in patients with metastatic bone disease due to breast cancer. Eur J Cancer. 2004; 40: 1704-1712. (Pubitemid 38902906)
33. Lin JT, Lane JM,. Osteoporosis: a review. Clin Orthop Relat Res. 2004; 425: 126-134. (Pubitemid 39062759)
34. Russell RG, Watts NB, Ebetino FH, Rogers MJ,. Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int. 2008; 19: 733-759.
35. Chung WO, Dommisch H, Yin L, Dale BA,. Expression of defensins in gingiva and their role in periodontal health and disease. Curr Pharm Des. 2007; 13: 3073-3083. (Pubitemid 350130959)
36. Taubman MA, Nash DA,. The scientific and public-health imperative for a vaccine against dental caries. Nat Rev Immunol. 2006; 6: 555-563. (Pubitemid 43980528)
37. Slade GD, Beck JD,. Plausibility of periodontal disease estimates from NHANES III. J Public Health Dent. 1999; 59: 67-72.
38. Allen MR, Burr DB,. The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data. J Oral Maxillofac Surg. 2009; 67 (5 Suppl): 61-70.
39. Allen MR, Burr DB,. Mandible matrix necrosis in beagle dogs after 3 years of daily oral bisphosphonate treatment. J Oral Maxillofac Surg. 2008; 66: 987-994. (Pubitemid 351522818)
40. Burr DB, Allen MR,. Mandibular necrosis in beagle dogs treated with bisphosphonates. Orthod Craniofac Res. 2009; 12: 221-228.
41. Sonis ST, Watkins BA, Lyng GD, Lerman MA, Anderson KC,. Bony changes in the jaws of rats treated with zoledronic acid and dexamethasone before dental extractions mimic bisphosphonate-related osteonecrosis in cancer patients. Oral Oncol. 2009; 45: 164-172.
42. Kikuiri T, Kim I, Yamaza T, et al. Cell-based immunotherapy with mesenchymal stem cells cures bisphosphonate-related osteonecrosis of the jaw-like disease in mice. J Bone Miner Res. 2010; 25: 1668-1679.
43. Hokugo A, Christensen R, Chung EM, et al. Increased prevalence of bisphosphonate-related osteonecrosis of the jaw with vitamin D deficiency in rats. J Bone Miner Res. 2010; 25: 1337-1349.
44. Gotcher JE, Jee WS,. The progress of the periodontal syndrome in the rice cat. II. The effects of a diphosphonate on the periodontium. J Periodontal Res. 1981; 16: 441-455. (Pubitemid 11008745)
45. Gotcher JE, Jee WS,. The progress of the periodontal syndrome in the rice rat. I. Morphometric and autoradiographic studies. J Periodontal Res. 1981; 16: 275-291. (Pubitemid 11091581)
46. Ferreira RI, de Almeida SM, Boscolo FN, Santos AO, Camargo EE,. Bone scintigraphy as an adjunct for the diagnosis of oral diseases. J Dent Educ. 2002; 66: 1381-1387.
47. Arias JA, Pardo C, Olmos A, Cuadrado ML, Ruibal A,. Dental diseases and radionuclide imaging of the jaws. Nucl Med Commun. 2004; 25: 305-310. (Pubitemid 38393524)
48. Lyons KP, Jensen JL,. Dental lesions causing abnormalities on skeletal scintigraphy. Clin Nucl Med. 1979; 4: 509-512. (Pubitemid 10201694)
49. Strittmatter EJ, Keller DL, LaBounty GL, Lewis DM, Graham GD,. The relationship between radionuclide bone scans and dental examinations. Oral Surg Oral Med Oral Pathol. 1989; 68: 576-581. (Pubitemid 19278836)
50. Tow DE, Garcia DA, Jansons D, Sullivan TM, Niederman R,. Bone scan in dental diseases. J Nucl Med. 1978; 19: 845-847. (Pubitemid 9114096)
51. de Almeida JM, Theodoro LH, Bosco AF, Nagata MJ, Oshiiwa M, Garcia VG,. Influence of photodynamic therapy on the development of ligature-induced periodontitis in rats. J Periodontol. 2007; 78: 566-575.
52. Badran Z, Kraehenmann MA, Guicheux J, Soueidan A,. Bisphosphonates in periodontal treatment: a review. Oral Health Prev Dent. 2009; 7: 3-12.
53. Allen MR, Follet H, Khurana M, Sato M, Burr DB,. Antiremodeling agents influence osteoblast activity differently in modeling and remodeling sites of canine rib. Calcif Tissue Int. 2006; 79: 255-261. (Pubitemid 44673719)
54. Feher A, Koivunemi A, Koivunemi M, et al. Bisphosphonates do not inhibit periosteal bone formation in estrogen deficient animals and allow enhanced bone modeling in response to mechanical loading. Bone. 46: 203-207.
55. Kashii M, Hashimoto J, Nakano T, Umakoshi Y, Yoshikawa H,. Alendronate treatment promotes bone formation with a less anisotropic microstructure during intramembranous ossification in rats. J Bone Miner Metab. 2008; 26: 24-33. (Pubitemid 350307995)
56. Ekuni D, Yamamoto T, Yamanaka R, Tachibana K, Watanabe T,. Proteases augment the effects of lipopolysaccharide in rat gingiva. J Periodontal Res. 2003; 38: 591-596. (Pubitemid 37494409)
57. Meer S, Coleman H, Altini M, Alexander T,. Mandibular osteomyelitis and tooth exfoliation following zoster-CMV co-infection. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006; 101: 70-75. (Pubitemid 41797041)
58. Farah CS, Savage NW,. Oral ulceration with bone sequestration. Aust Dent J. 2003; 48: 61-64. (Pubitemid 38011274)
59. Schwartz HC,. Osteonecrosis of the jaws: a complication of cancer chemotherapy. Head Neck Surg. 1982; 4: 251-253. (Pubitemid 12172078)
60. Junquera L, Gallego L,. Nonexposed bisphosphonate-related osteonecrosis of the jaws: another clinical variant? J Oral Maxillofac Surg. 2008; 66: 1516-1517. (Pubitemid 351822447)
61. Aghaloo TL, Felsenfeld AL, Tetradis S,. Osteonecrosis of the jaw in a patient on Denosumab. J Oral Maxillofac Surg. 68: 959-963.
62. Taylor KH, Middlefell LS, Mizen KD,. Osteonecrosis of the jaws induced by anti-RANK ligand therapy. Br J Oral Maxillofac Surg. 2010; 48: 221-223.
63. Kyrgidis A, Toulis KA,. Denosumab-related osteonecrosis of the jaws. Osteoporosis Int. 2011; 22: 369-370.