Effect of long-term oral bisphosphonates on implant wound healing: Literature review and a case report

Journal of Periodontology

Volumn 78, Issue 3, 2007, Pages 584-594

  Wang, Hom Lay ^a   Weber, Daniel ^a   McCauley, Laurie K ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bisphosphonate; Dental implants; Fosamax; Osteonecrosis; Wound healing

Indexed keywords

ALENDRONIC ACID; ANTIINFECTIVE AGENT; BISPHOSPHONIC ACID DERIVATIVE; BONE DENSITY CONSERVATION AGENT; PARATHYROID HORMONE[1-34];

AGED; BONE NECROSIS; BONE REGENERATION; BONE TRANSPLANTATION; CASE REPORT; CHEMICALLY INDUCED DISORDER; DRUG CONTRAINDICATION; DRUG EFFECT; FEMALE; HUMAN; JAW DISEASE; MOUTH HYGIENE; ORAL DRUG ADMINISTRATION; REVIEW; TOOTH IMPLANTATION; WOUND HEALING;

ADMINISTRATION, ORAL; AGED; ALENDRONATE; ANTI-BACTERIAL AGENTS; BONE DENSITY CONSERVATION AGENTS; BONE REGENERATION; BONE TRANSPLANTATION; DENTAL IMPLANTATION, ENDOSSEOUS; DENTAL IMPLANTS; DIPHOSPHONATES; FEMALE; HUMANS; JAW DISEASES; MOUTHWASHES; OSTEORADIONECROSIS; TERIPARATIDE; WOUND HEALING;

EID: 33947707231     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2007.060239     Document Type: Review

References (72)

1. Fleisch H, Russell RG, Bisaz S, Casey P, Muhlbayer R. The influence of pyrophosphate analogues (diphosphonates) on the precipitation and dissolution of calcium phosphate in vitro and in vivo. Calcif Tissue Res 1968; (Suppl.):10-10a.
2. Fleisch H, Russell RG, Straumann F. Effect of pyrophosphate on hydroxyapatite and its implications on calcium hemostasis. Nature 1966;212:901-903.
3. Fleisch H. Development of bisphosphonates. Breast Cancer Res 2002;4:30-34.
4. Francis MD, Russell RG, Fleisch H. Disphosphonates inhibit formation of calcium phosphate crystals in vitro and pathologic calcifications in vivo. Science 1969; 165: 1264-1266.
5. Fleisch H, Russell RG, Francis MD. Disphosphonates inhibit hydroxyapatite dissolution in vitro and bone resorption in tissue culture and in vivo. Science 1969; 165:1262-1264.
6. Green J. Bisphosphonates: Preclinical review. Oncologist 2004;9(Suppl. 4):3-13.
7. Benford HL, Frith JC, Auriola S, Monkkonen J, Rogers MJ. Farnesol and geranylgerniol prevent activation of caspases by aminobisphosphonates: Biochemical evidence for two distinct pharmacological classes of bisphosphonate drugs. Mol Pharmacol 1999;56: 131-140.
8. Bergstrom JD, Bostedor RG, Masarachia PJ, Reszka AA, Rodan G. Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase. Arch Biochem Biophys 2000;373:231-241.
9. Lehenkari PP, Kellinsalmi M, Napankangas JP, et al. Further insight into mechanism of action of clodronate: Inhibition of mitochondrial ADP/ATP translocase by a nonhydrolyzable, adenine-containing metabolite. Mol Pharmacol 2002;61:1255-1262.
10. McClung MR. Bisphosphonates. Endocrinol Metab Clin North Am 2003;32:253-271.
11. Katsuki H, Bloch K. Studies on the biosynthesis of ergosterols in yeast: Formation of methylated intermediates. J Biol Chem 1967;242:222-227.
12. Lynen F. Biosynthetic pathways from acetate to natural products. Pure Appl Chem 1967;14:137-167.
13. Moran LA, Scrimgeour KG, Horton HR, Ochs RS, Rawn JD. Biochemistry, 2nd ed. Upper Saddle River, NJ: Prentice Hall; 1994:852.
14. Watanabe Y, Shiomi M, Tsujita Y, et al. Preventive effect of pravastatin sodium, a potent inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase, on coronary atherosclerosis and xanthoma in WHHL rabbits. Biochim Biophys Acta 1988;960:294-302.
15. Gober HJ, Kistowska M, Angman L, et al. Human T cell receptor gamma delta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003; 197:163-168.
16. Luckman SP, Coxon FP, Ebetino FH, Russell RG, Rogers MJ. Heterocycle-containing bisphosphonates cause apoptosis and inhibit bone resorption by preventing protein prenylation: Evidence from structure-activity relationships in J774 macrophages. J Bone Miner Res 1998;13:1668-1678.
17. Alakangas A, Selander K, Mulari M, et al. Alendronate disturbs vesicular trafficking in osteoclasts. Calcif Tissue Int 2002;70:40-47.
18. Dunford JE, Thompson K, Coxon FP, et al. Structure-activity relationships for inhibition of farnesyl diphosphate synthase in vitro and inhibition of bone resorption in vivo by nitrogen-containing bisphosphonates. J Pharmacol Exp Ther 2001;296:235-242.
19. Monkkonen H, Lehenkari PP, Kellinsalmi M, et al. A new mechanism of action for bisphosphonates: Appi dedicated cytotoxicity of N-BPs. In: Bone Workshops, Davos 2004. Abstracts from the Workshop: Frontiers of Skeletal Biology and Workshop: What is New in Bisphosphonates? Davos, Switzerland, March 20-26, 2004. Bone 2004;34(Suppl. 1):S66.
20. Selander KS, Monkkonen J, Karhukorpi EK, Harkonen P, Hannuniemi R, Vannanen K. Characteristics of clodronate-induced apoptosis in osteoclasts and macrophages. Mol Pharmacol 1996;50:1127-1138.
21. Conte P, Guarneri V. Safety of intravenous and oral bisphosphonates and compliance with dosing regimens. Oncologist 2004;9(Suppl. 4):28-37.
22. Bounameaux HM, Schifferi J, Montani JP, Jung A, Chatelanat F. Renal failure associated with intravenous disphosphonates. Lancet 1983;1:471.
23. Shinoda H, Adamek G, Felix R, Fleisch H, Schenk R, Hagan P. Structure relationships of various bisphosphonates. Calcif Tissue Int 1983;35:87-99.
24. Markowitz GS, Apple GB, Fine PL, et al. Collapsing focal segmental glomerulosclerosis following treatment with high-dose pamidronate. J Am Soc Nephrol 2001;12:1164-1172.
25. Rosen LS, Gordon D, Tchekmedyian S, et al. Zolendric acid versus placebo in the treatment of skeletal metastases in patients with lung cancer and other solid tumors: A phase III, double-blind, randomized trial. The Zoledronic Acid Lung Cancer and Other Solid Tumors Study Group. J Clin Oncol 2003;21:3150-3157.
26. Atula S, Powles T, Paterson A, McCloskey E, Nevalainen J, Kanis J. Extended safety profile of oral clodronate after long-term use in primary breast cancer patients. Drug Saf 2003;26:661-671.
27. Tanko LB, McClung M, Schimmer RC, Mahoney P, Christiansen C. The efficacy of 48-week oral ibandronate treatment in postmenopausal osteoporosis when taken 30 versus 60 minutes before breakfast. Bone 2003;32:421-426.
28. Clowes JA, Peel NF, Eastell R. The impact of monitoring on adherence and persistence with antiresorptive treatment for postmenopausal osteoporosis: A randomized controlled trial. J Clin Endocrinol Metab 2004;89:1117-1123.
29. Thakkar SG, Isada C, Smith J, et al. Jaw complications associated with bisphosphonate use in patients with plasma cell dyscrasias. Med Oncol 2006;23:51-56.
30. Marx RE. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: A growing epidemic. J Oral Maxillofac Surg 2003;61: 1115-1117.
31. 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.
32. Migliorati CA. Bisphosphonates and oral cavity avascular bone necrosis. J Clin Oncol 2003;21:4253-4254.
33. 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.
34. Badros A, Weikel D, Salama A, et al. Osteonecrosis of the jaw in multiple myeloma patients: Clinical features and risk factors. J Clin Oncol 2006;24:945-952.
35. Hellstein JW, Marek CL. Bisphosphonate osteochemonecrosis (bis-phossy jaw): Is this phossy jaw of the 21st century? J Oral Maxillofac Surg 2005;63:682-689.
36. Hansen T, Kunkel M, Weber A, James Kirkpatrick C. Osteonecrosis of the jaws in patients treated with bisphosphonates: Histomorphologic analysis in comparison with infected osteoradionecrosis. J Oral Pathol Med 2006;35:155-160.
37. Woo SB, Hellstein JW, Kalmar JR. Narrative review: Bisphosphonates and osteonecrosis of the jaws. Ann Intern Med 2006;144:753-761.
38. Migliorati CA, Siegel MA, Elting LS. Bisphosphonate-associated osteonecrosis: A long-term complication of bisphosphonate treatment. Lancet Oncol 2006;7: 508-514.
39. Strewler GJ. Decimal point-osteoporosis therapy at the 10-year mark. N Engl J Med 2004;350:1172-1174.
40. Dando TM, Noble S. Once-monthly ibandronate. Treat Endocrinol 2005;4:381-387.
41. Emkey R, Koltun W, Beusterien K, et al. Patient preference for once-monthly ibandronate versus once-weekly alendronate in a randomized, open-label, cross-over trial: The Boniva Alendronate Trial in Osteoporosis (BALTO). Curr Med Res Opin 2005;21: 1895-1903.
42. Leu CT, Luegmayr E, Freedman LP, Rodan GA, Reszka AA. Relative binding affinities of bisphosphonates for human bone and relationship to antiresorptive efficacy. Bone 2006;38:628-636.
43. Nancollas GH, Tang R, Phipps RJ, et al. Novel insights into actions of bisphosphonates on bone: Differences in interactions with hydroxyapatite. Bone 2006;38:617-627.
44. Odvina CV, Zerwekh JE, Rao DS, Maalouf N, Gottschalk FA, Pak CY. Severely suppressed bone turnover: A potential complication of alendronate therapy. J Clin Endocrinol Metab 2005;90:1294-1301.
45. Dao TT, Anderson JD, Zarb GA. Is osteoporosis a risk factor for osseointegration of dental implants? Int J Oral Maxillofac Implants 1993;8:137-144.
46. Siris ES, Miller PD, Barrett-Connor E, et al. Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: Results from the National Osteoporosis Risk Assessment. JAMA 2001;286:2815-2822.
47. Gadeleta SJ, Boskey AL, Paschalis E, et al. A physical, chemical, and mechanical study of lumbar vertebrae from normal, ovariectomized, and nandrolone decanoate-treated cynomolgus monkeys (Macaca fascicularis). Bone 2000;27:541-550.
48. Friberg B, Ekestubbe A, Mellstrom D, Sennerby L. Brånemark implants and osteoporosis: A clinical exploratory study. Clin Implant Dent Relat Res 2001;3: 50-56.
49. Minsk L, Polson AM. Dental implant outcomes in postmenopausal women undergoing hormone replacement. Compend Contin Educ Dent 1998;19:859-862.
50. August M, Chung K, Chang Y, Glowacki J. Influence of estrogen status on endosseous implant osseointegration. J Oral Maxillofac Surg 2001;59:1285-1289.
51. 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.
52. 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.
53. Shlomi B, Levy Y, Kleinman S. Avascular necrosis of the jaw bone after bisphosphonate therapy (in Hebrew). Harefuah 2005;144:536-539, 599-600.
54. Migliorati CA, Schubert MM, Peterson DE, Seneda LM. Bisphosphonate-associated osteonecrosis of mandibular and maxillary bone. Cancer 2005;104:83-93.
55. Lackner H, Benesch M, Moser A, et al. Aseptic osteonecrosis in children and adolescents treated for hemato-oncologic diseases: A 13-year longitudinal observational study. J Pediatr Hematol Oncol 2005;27:259-263.
56. Gralow J. Evolving role of bisphosphonates in women undergoing treatment for localized and advanced breast cancer. Clin Breast Cancer 2005;5(Suppl. 2):S54-S62.
57. Park S-H, Lee K-W, Oh T-J, Misch CE, Shotwell JL, Wang H-L. Effect of absorbable membranes on sandwich bone augmentation. Clin Oral Implants Res; in press.
58. Neer RM, Arnaud CD, Zanchetta JR, et al. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 2001;344:1434-1441.
59. Seeman E, Delmas PD. Reconstructing the skeleton with intermittent parathyroid hormone. Trends Endocrinol Metab 2001;12:281-283.
60. Dempster DW, Cosman F, Kurland ES, et al. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: A paired biopsy study. J Bone Miner Res 2001;16:1846-1853.
61. Lindsay R, Nieves J, Henneman E, Shen V, Cosman F. Subcutaneous administration of the amino-terminal fragment of human parathyroid hormone-(1-34): Kinetics and biochemical response in estrogenized osteoporotic patients. J Clin Endocrinol Metab 1993;77: 1535-1539.
62. Lindsay R, Nieves J, Formica C, et al. Randomised controlled study of effect of parathyroid hormone on vertebral-bone mass and fracture incidence among postmenopausal women on oestrogen with osteoporosis. Lancet 1997;350:550-555.
63. Hock JM, Gera I. Effects of continuous and intermittent administration and inhibition of resorption on the anabolic response of bone to parathyroid hormone. J Bone Miner Res 1992;7:65-72.
64. Lacey DL, Timms E, Tan HL, et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 1998;93:165-176.
65. Yasuda H, Shima N, Nakagawa N, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 1998;95: 3597-3602.
66. Ma YL, Cain RL, Halladay DL, et al. Catabolic effects of continuous human PTH (1-38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology 2001;142:4047-4054.
67. Locklin RM, Khosla S, Turner RT, Riggs BL. Mediators of the biphasic responses of bone to intermittent and continuously administered parathyroid hormone. J Cell Biochem 2003;89:180-190.
68. Tam CS, Heersche JN, Murray TM, Parsons JA. Parathyroid hormone stimulates the bone apposition rate independently of its resorptive action: Differential effects of intermittent and continuous administration. Endocrinology 1982;110:506-512.
69. Ardine M, Generali D, Donadio M, et al. Could the long-term persistence of low serum calcium levels and high serum parathyroid hormone levels during bisphosphonate treatment predispose metastatic breast cancer patients to undergo osteonecrosis of the jaw? Ann Oncol 2006;17:1336-1337.
70. Vinholes J, Guo CY, Purohit OP, Eastell R, Coleman RE. Metabolic effects of pamidronate in patients with metastatic bone disease. Br J Cancer 1996;73:1089-1095.
71. Berruti A, Dogliotti L, Tucci M, Tarabuzzi R, Fontana D, Angeli A. Metabolic bone disease induced by prostate cancer: Rationale for the use of bisphosphonates. J Urol 2001;166:2023-2031.
72. American Academy of Periodontology. AAP statement on bisphosphonates. Available at: http://www.perio.org/resources-products/ bisphosphonates.htm. Accessed May 25, 2006.