Osteoporosis and its medical management. A literature review
Georgios NTAGIANTIS, Nadia THEOLOGIE-LYGIDAKIS
Department of Oral and Maxillofacial Surgery, School of Dentistry, National and Kapodistrian University of Athens (Head: Professor N. G. Papadogeorgakis)
Hellenic Archives of Oral & Maxillofacial Surgery (2018) 2, 89-104
SUMMARY: The traditionally high incidence of osteo- porosis along with the gradually increasing pharmacological treatment with the use of modern antiresorptive medication among others, make it quite certain that the dentist will come across patients, who are being treated with this kind of medication. Medication related osteonecrosis of the jaw (MRONJ), is a serious disease that has been associated among others with teeth extraction, implant surgery, and trauma due to ill-fitting dentures. In this paper, the modern literature concerning osteoporosis, its treatment options, and the management of those patients who are treated with antiresorptive med- ication against osteoporosis, are presented.
KEY WORDS: Osteopenia, osteoporosis, bisphospho- nates, denosumab, antiresorptives, osteonecrosis of the jaw, MRONJ
REFERENCES
Allen MR, Pandya B, Ruggiero SL: Lack of correlation between dura- tion of osteonecrosis of the jaw and sequestra tissue morphology: what it tells us about the condition and what it means for future studies. J Oral Maxillofac Surg. 68:2730–4, 2010
Allen MR, Ruggiero SL: Higher bone matrix density exists in only a subset of patients with bisphosphonate-related osteonecrosis of the jaw. J Oral Maxillofac Surg. 67:1373–7, 2009
Background Document for Meeting of Advisory Committee for Re- productive Health Drugs and Drug Safety and Risk Management Advisory Committee. United States. Food and Drug Administra- tion. September 9, 2011; http://www.fda.gov/downloads/ Adviso- ryCommittees/CommitteesMeetingMaterials/drugs/DrugSafetyan dRiskManagementAdvisoryCommittee/ucm270958.pdf. Accessed February 10, 2014
Barasch A, Cunha-Cruz J, Curro FA, et al: Risk factors for osteonecrosis of the jaws: a case-control study from the CONDOR dental PBRN. J Dent Res. 90:439–44, 2011
Black DM, Clifford J. Rosen, MD: Postmenopausal Osteoporosis. N Engl J Med 374:254-62, 2016
Black DM, Bilezikian JP, Ensrud KE, et al: One year of alendronate after one year of parathyroid hormone (1-84) for osteoporosis. N Engl J Med 353: 555-65, 2016
Black DM, Reid IR, Boonen S, et al: The effect of 3 versus 6 years of zoledronic acid treatment of osteoporosis: a randomized exten- sion to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 27:243, 2012
Bonacina R, Mariani U, Villa F, et al: Preventive strategies and clinical implications for bisphosphonate-related osteonecrosis of the jaw: a review of 282 patients. J Can Dent Assoc 77:b147, 2011
Bone HG, Chapurlat R, Brandi ML, et al: The effect of three or six years of denosumab exposure in women with postmenopausal osteoporosis: results from the FREEDOM extension. J Clin En- docrinol Metab 98(11):4483–4492, 2013
Boonen S, Ferrari S, Miller PD, et al: Postmenopausal osteoporosis treatment with antiresorptives: effects of discontinuation or longterm continuation on bone turnover and fracture risk—a per- spective. J Bone Miner Res. 27(5):963–974, 2012
Burch J, Rice S, Yang H, NeilsonA, Stirk L, Francis R, Holloway P, Selby P, Craig D: Systematic review of the use of bone turnover markers for monitoring the response to osteoporosis treatment: the sec- ondary prevention of fractures, and primary prevention of frac- tures in high-risk groups. Health Technol Assess (Winchester, Eng- land) 18(11):1-206, 2014
Cauley JA, Robbins J, Chen Z, et al: Effects of estrogen plus progestin on risk of fracture and bone mineral density: the Women’s Health Initiative randomized trial. JAMA 290: 1729-38, 2003
Cosman F., S. J. de Beur, M. S. LeBoff, E. M. Lewiecki, B. Tanner, S. Ran- dall, R. Lindsay: Clinician’s Guide to Prevention and Treatment of Osteoporosis. Osteoporos Int. 25:2359–2381, 2014
Cummings SR, San Martin J, McClung MR et al: Denosumab for pre- vention of fractures in postmenopausal women with osteoporosis. N Engl J Med 361(8):756–765, Erratum in: N Engl J Med 361(19):1914, 2009
Dallas SL, Prideaux M, Bonewald LF: The osteocyte: an endocrine cell and more. Endocr Rev. Oct;34(5):658-90, 2013
Damm DD, Jones DM: Bisphosphonate-related osteonecrosis of the jaws: a potential alternative to drug holidays. Gen Dent 61:33, 2013 Dodson TB: The Frequency of Medication-related Osteonecrosis of the Jaw and its Associated Risk Factors. Oral Maxillofac Surg Clin
North Am 27:509-16, 2015
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 20:117, 2009
Ettinger B, Black DM, Mitlak BH, et al: Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. JAMA 282: 637-45, 1999
Fedele S, Porter SR, D'Aiuto F, et al: Non-exposed variant of bispho- sphonate-associated osteonecrosis of the jaw: a case series. Am J Med 123:1060, 2010
Fedele S, Bedogni G, Scoletta M, et al: Up to a quarter of patients with osteonecrosis of the jaw associated with antiresorptive agents re- main undiagnosed. Br J Oral Maxillofac Surg 53(1):13–7, 2015
Ferlito S, Puzzo S, Liardo C: Preventive protocol for tooth extractions in patients treated with zoledronate: a case series. J Oral Maxillo- fac Surg 69:e1–e4, 2011
Fernández-Tresguerres-Hernández-Gil I, Alobera-Gracia MA, del Canto-Pingarrón M et al: Physiological bases of bone regeneration
II. The remodeling process. Med Oral Patol Oral Cir Bucal 11:E151–E157, 2006
Fitzpatrick SG, Stavropoulos MF, Bowers LM, et al: Bisphosphonate re- lated osteonecrosis of jaws in 3 osteoporotic patients with history of oral bisphosphonate use treated with single yearly zoledronic acid infusion. J Oral Maxillofac Surg 70:325–30, 2012
Fournier P, Boissier S, Filleur S, et al: Bisphosphonates inhibit angiogen- esis in vitro and testosterone-stimulated vascular regrowth in the ventral prostate in castrated rats. Cancer Res 62:6538–44, 2002 International Society for Clinical Densitometry. 2013 Official Positions- Adult. http://www.iscd.org/official-positions/2013- iscd-official-positions-adult/. Accessed Feb 2014
Gallagher JC, Tella SH: Prevention and treatment of postmenopausal osteoporosis, J. Steroid Biochem 142:155-70, 2014
Glaser DL, Kaplan FS: Osteoporosis. Definition and clinical presenta- tion. Spine 22:12S-16S, 1997
Grbic JT, Black DM, Lyles KW, et al: The incidence of osteonecrosis of the jaw in patients receiving 5 milligrams of zoledronic acid: data from the health outcomes and reduced incidence with zoledronic acid once yearly clinical trials program. J Am Dent Assoc 141:1365, 2010
Groetz KA, Piesold J-U, Al-Nawas B: Bisphosphonat-assoziierte Kiefer- nekrose (BPONJ) und andere Medikamenten-assoziierte Kiefer- nekrosen, Mund Kiefer Gesichtschir 10(5):287-300, 2006
Hellstein JW, Adler RA, Edwards B, et al: Managing the care of patients receiving antiresorptive therapy for prevention and treatment of osteoporosis: executive summary of recommendations from the American Dental Association Council on Scientific Affairs. J Am Dent Assoc 142:1243–51, 2011
Heufelder MJ, Hendricks J, Remmerbach T, Frerich B, Hemprich A, Wilde F: Principles of oral surgery for prevention of bisphospho- nate-related osteonecrosis of the jaw. Oral Surg Oral Med Oral Pathol Oral Radiol 117: e429-435, 2014
Kanis JA, Melton III LJ, Christiansen J, Johnston CC, Khaltaev N: The di- agnosis of osteoporosis. J Bone Miner Res 9:1137–41, 1994
Kanis JA, Johnell O, Oden A, Dawson A, De Laet C, Jonsson B: Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos Int 12:989–95, 2001
Karaguzel Gulay, Michael F. Holick: Diagnosis and treatment of os- teopenia. Rev. Endocr. Metab. Disord 11:237–251, 2010
Khan ΑΑ et al: Diagnosis and Management of Osteonecrosis of the Jaw: A Systematic Review and International Consensus. Journal of Bone and Mineral Research, Vol. 30, No. 1, pp 3–23, 2015
Kunchur R, Need A, Hughes T, et al: Clinical investigation of C-terminal crosslinking telopeptide test in prevention and management of bisphosphonate-associated osteonecrosis of the jaws. J Oral Max- illofac Surg 67:1167, 2009
Kyrgidis A, Barbas A: Osteonecrosis of the jaw among bisphosphonate users. Am J Med 121: e21, 2008
Lewiecki EM: Bisphosphonates for the treatment of osteoporosis: in- sights for clinicians. Ther Adv Chronic Dis 1(3):115–128, 2010
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 68:243, 2010
Marx RE, Sawatari Y, Fortin M, Broumand V: Bisphosphonate induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk fac- tors, recognition, prevention, and treatment. J Oral Maxillofac Surg 63:1567–75, 2005
Marx RE, Cillo JE Jr, Ulloa JJ: Oral bisphosphonate induced osteonecro- sis: risk factors, prediction of risk using CTx testing, prevention and treatment. J Oral Maxillofac Surg 65:2397-2410, 2007
McClung M, Harris ST, Miller PD, et al: Bisphosphonate therapy for osteoporosis: benefits, risks, and drug holiday. Am J Med 126 (1):13–20, 2013
Modi A, Siris ES, Tang J, Sen S: Cost and consequences of noncompli- ance with osteoporosis treatment among women initiating ther- apy. Curr Med Res Opin 31: 757-65, 2015
Mozzati M, Arata V, Gallesio G: Tooth extraction in osteoporotic pa- tients taking oral bisphosphonates. Osteoporos Int 24: 1707-1712, 2013
Nakashima T, Hayashi M, Takayanagi H: New insights into osteoclas- togenic signaling mechanisms. Trends Endocrinol Metab. Nov;23(11):582-90, 2012
National Osteoporosis Foundation. Health professional’s guide to reha- bilitation of the patient with osteoporosis. 2003 Washington, DC 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 344: 1434-41, 2001 Nelson HD, Haney EM, Chou R, Dana T, Fu R, Bougatsos C: Screening
for osteoporosis: systematic review to update the 2002 US Pre- ventive Services Task Force Recommendation. Evidence Synthe- ses No. 77. AHRQ Publication No. 10-05145-EF-1. Agency for Healthcare Research and Quality, (US), Rockville, 2010
Otto S, Tröltzsch M, Jambrovic V, Panya S, Probst F, Ristow O, Ehren- feld M, Pautke C: Tooth extraction in patients receiving oral or intravenous bisphosphonate administration: A trigger for BRONJ development?, J Craniomaxillofac Surg. 43(6):847-54, 2015
Otto S, Pautke C, Martin Jurado O, Nehrbass D, Stoddart MJ, Ehren- feld M, Zeiter S: Further development of the MRONJ minipig large animal model. J Craniomaxillofac Surg. 45(9):1503-1514, 2017
Papapoulos S, Lippuner K, Roux C, et al: The effect of 8 or 5 years of denosumab treatment in postmenopausal women with osteo- porosis: results from the FREEDOM Extension study. Osteoporos Int 26(12):2773–2783, 2015
Raggatt LJ, Partridge NC: Cellular and molecular mechanisms of bone remodelling. J Biol Chem. 13;285(33):25103-8, 2010
Recker RR, Ste-Marie LG, Chavassieux P, et al: Bone safety with rise- dronate: histomorphometric studies at different dose levels and exposure. Osteoporos Int. 26(1):327–337, 2015
Richman S, Edusa V, Fadiel A, Naftolin F: Low-dose estrogen therapy for prevention of osteoporosis: working our way back to monotherapy. Menopause 13: 148-55, 2006
Root AW, Diamond FB: Disorders of mineral homeostasis in newborn, infant, child, and adolescent. In: Sperling MA, editor. Pediatric en- docrinology. Philadelphia: Elsevier Saunders p. 686–769, 2008
Ripamonti CI, Maniezzo M, Campa T, et al: Decreased occurrence of osteonecrosis of the jaw after implementation of dental preven- tive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan. Ann Oncol 20:137, 2009
Ruggiero SL, Dodson TB, Fantasia J, et al: American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on medication-related os- teonecrosis of the jaw—2014 update. J Oral Maxillofac Surg Oct 72(10):1938–56, 2014
Saad F, Brown JE, Van PC, et al: Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases. Ann Oncol 23:1341–7, 2012
Saia G, Blandamura S, Bettini G, Tronchet A, Totola A, Bedogni G, et al: Occurrence of bisphosphonate-related osteonecrosis of the jaw after surgical tooth extraction. J Oral Maxillofac Surg 68: 797- 804, 2010
Santini D, Vincenzi B, Dicuonzo G, et al: Zoledronic acid induces sig- nificant and long-lasting modifications of circulating angiogenic fac- tors in cancer patients. Clin Cancer Res 9:2893–7, 2003
Schubert M, Klatte I, Linek W, et al: The Saxon bisphosphonate register - therapy and prevention of bisphosphonate-related osteonecrosis of the jaws. Oral Oncol 48:349–54, 2012
Schousboe JT, Nyman JA, Kane RL, Ensrud KE: Costeffectiveness of al- endronate therapy for osteopenic postmenopausal women. Ann Intern Med 142:734–41, 2005
Scoletta M, Arduino PG, Pol R, et al: Initial experience on the outcome of teeth extractions in intravenous bisphosphonate treated pa- tients: a cautionary report. J Oral Maxillofac Surg 69:456–62, 2011 Sharma D, Ivanovski S, Slevin M, et al: Bisphosphonate-related os- teonecrosis of jaw (BRONJ): diagnostic criteria and possible path- ogenic mechanisms of an unexpected anti-angiogenic side effect.
Vasc Cell 5:1–5, 2013
Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al: Bone mineral density thresholds for pharmacological in- terventions to prevent fractures. Arch Intern Med. 164:1108–12, 2004
Soldatos N, Melakopoulos I, Silvestros S, Kontakiotis G, Katsikeris N: Bisphosphonates and implants. Literature review, guidelines and case reports display. Stoma 38:139-147, 2010
Tamiolakis P, Thermos G, Charoulis A, Chrysomali A, Sklavounou-An- drikopoulou A: Medication related osteonecrosis of the jaws. Lit- erature review. Hellenic Archives of Oral and Maxillofacial Sur- gery, 19(1):11-34, 2018
Thumbigere-Math V, Tu L, Huckabay S, et al: A retrospective study evaluating frequency and risk factors of osteonecrosis of the jaw in 576 cancer patients receiving intravenous bisphosphonates. Am J Clin Oncol 35:386–92, 2012
Uyanne J, Calhoun CC, Le AD, et al: Antiresorptive Drug–Related Os- teonecrosis of the Jaw. Dent Clin N Am 58:369–384, 2014
Vandone AM, Donadio M, Mozzati M, et al: Impact of dental care in the prevention of bisphosphonate-associated osteonecrosis of the jaw: a single-center clinical experience. Ann Oncol 23:193, 2012
Vannucci L & Brandi ML: Pharmacological management of osteoporosis – when to treat and when to stop, Expert Review of Clinical Phar- macology, 1:1-8, 2016
Vincenzi B, Santini D, Dicuonzo G, et al: Zoledronic acid-related an- giogenesis modifications and survival in advanced breast cancer patients. J Interferon Cytokine Res 25:144–51, 2005
Watts NB, Adler RA, Bilezikian JP: Endocrine Society et al. Osteoporo- sis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97(6):1802–1822, 2012
Watts NB: Long-term risks of bisphosphonate therapy. Arq Bras En- docrinol Metab 58(5):523–529, 2014
Weinstein RS, Roberson PK, Manolagas SC: Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360:53- 62, 2009
World Health Organization Collaborating Centre for Metabolic Bone Diseases. FRAXA WHO Fracture Risk Assessment Tool. Available at: http://www.shef.ac.uk/FRAX/ (accessed 28.10.09).
World Health Organization scientific group on the assessment of os- teoporosis at primary health care level, summary meeting report, Brussels, Belgium, 5-7 May 2004
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 68:243, 2010
Marx RE, Sawatari Y, Fortin M, Broumand V: Bisphosphonate induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk fac- tors, recognition, prevention, and treatment. J Oral Maxillofac Surg 63:1567–75, 2005
Marx RE, Cillo JE Jr, Ulloa JJ: Oral bisphosphonate induced osteonecro- sis: risk factors, prediction of risk using CTx testing, prevention and treatment. J Oral Maxillofac Surg 65:2397-2410, 2007
McClung M, Harris ST, Miller PD, et al: Bisphosphonate therapy for osteoporosis: benefits, risks, and drug holiday. Am J Med 126 (1):13–20, 2013
Modi A, Siris ES, Tang J, Sen S: Cost and consequences of noncompli- ance with osteoporosis treatment among women initiating ther- apy. Curr Med Res Opin 31: 757-65, 2015
Mozzati M, Arata V, Gallesio G: Tooth extraction in osteoporotic pa- tients taking oral bisphosphonates. Osteoporos Int 24: 1707-1712, 2013
Nakashima T, Hayashi M, Takayanagi H: New insights into osteoclas- togenic signaling mechanisms. Trends Endocrinol Metab. Nov;23(11):582-90, 2012
National Osteoporosis Foundation. Health professional’s guide to reha- bilitation of the patient with osteoporosis. 2003 Washington, DC 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 344: 1434-41, 2001 Nelson HD, Haney EM, Chou R, Dana T, Fu R, Bougatsos C: Screening
for osteoporosis: systematic review to update the 2002 US Pre- ventive Services Task Force Recommendation. Evidence Synthe- ses No. 77. AHRQ Publication No. 10-05145-EF-1. Agency for Healthcare Research and Quality, (US), Rockville, 2010
Otto S, Tröltzsch M, Jambrovic V, Panya S, Probst F, Ristow O, Ehren- feld M, Pautke C: Tooth extraction in patients receiving oral or intravenous bisphosphonate administration: A trigger for BRONJ development?, J Craniomaxillofac Surg. 43(6):847-54, 2015
Otto S, Pautke C, Martin Jurado O, Nehrbass D, Stoddart MJ, Ehren- feld M, Zeiter S: Further development of the MRONJ minipig large animal model. J Craniomaxillofac Surg. 45(9):1503-1514, 2017
Papapoulos S, Lippuner K, Roux C, et al: The effect of 8 or 5 years of denosumab treatment in postmenopausal women with osteo- porosis: results from the FREEDOM Extension study. Osteoporos Int 26(12):2773–2783, 2015
Raggatt LJ, Partridge NC: Cellular and molecular mechanisms of bone remodelling. J Biol Chem. 13;285(33):25103-8, 2010
Recker RR, Ste-Marie LG, Chavassieux P, et al: Bone safety with rise- dronate: histomorphometric studies at different dose levels and exposure. Osteoporos Int. 26(1):327–337, 2015
Richman S, Edusa V, Fadiel A, Naftolin F: Low-dose estrogen therapy for prevention of osteoporosis: working our way back to monotherapy. Menopause 13: 148-55, 2006
Root AW, Diamond FB: Disorders of mineral homeostasis in newborn, infant, child, and adolescent. In: Sperling MA, editor. Pediatric en- docrinology. Philadelphia: Elsevier Saunders p. 686–769, 2008
Ripamonti CI, Maniezzo M, Campa T, et al: Decreased occurrence of osteonecrosis of the jaw after implementation of dental preven- tive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan. Ann Oncol 20:137, 2009
Ruggiero SL, Dodson TB, Fantasia J, et al: American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on medication-related os- teonecrosis of the jaw—2014 update. J Oral Maxillofac Surg Oct 72(10):1938–56, 2014
Saad F, Brown JE, Van PC, et al: Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases. Ann Oncol 23:1341–7, 2012
Saia G, Blandamura S, Bettini G, Tronchet A, Totola A, Bedogni G, et al: Occurrence of bisphosphonate-related osteonecrosis of the jaw after surgical tooth extraction. J Oral Maxillofac Surg 68: 797- 804, 2010
Santini D, Vincenzi B, Dicuonzo G, et al: Zoledronic acid induces sig- nificant and long-lasting modifications of circulating angiogenic fac- tors in cancer patients. Clin Cancer Res 9:2893–7, 2003
Schubert M, Klatte I, Linek W, et al: The Saxon bisphosphonate register
- therapy and prevention of bisphosphonate-related osteonecrosis of the jaws. Oral Oncol 48:349–54, 2012
Schousboe JT, Nyman JA, Kane RL, Ensrud KE: Costeffectiveness of al- endronate therapy for osteopenic postmenopausal women. Ann Intern Med 142:734–41, 2005
Scoletta M, Arduino PG, Pol R, et al: Initial experience on the outcome of teeth extractions in intravenous bisphosphonate treated pa- tients: a cautionary report. J Oral Maxillofac Surg 69:456–62, 2011 Sharma D, Ivanovski S, Slevin M, et al: Bisphosphonate-related os- teonecrosis of jaw (BRONJ): diagnostic criteria and possible path- ogenic mechanisms of an unexpected anti-angiogenic side effect.
Vasc Cell 5:1–5, 2013
Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al: Bone mineral density thresholds for pharmacological in- terventions to prevent fractures. Arch Intern Med. 164:1108–12, 2004
Soldatos N, Melakopoulos I, Silvestros S, Kontakiotis G, Katsikeris N: Bisphosphonates and implants. Literature review, guidelines and case reports display. Stoma 38:139-147, 2010
Tamiolakis P, Thermos G, Charoulis A, Chrysomali A, Sklavounou-An- drikopoulou A: Medication related osteonecrosis of the jaws. Lit- erature review. Hellenic Archives of Oral and Maxillofacial Sur- gery, 19(1):11-34, 2018
Thumbigere-Math V, Tu L, Huckabay S, et al: A retrospective study evaluating frequency and risk factors of osteonecrosis of the jaw in 576 cancer patients receiving intravenous bisphosphonates. Am J Clin Oncol 35:386–92, 2012
Uyanne J, Calhoun CC, Le AD, et al: Antiresorptive Drug–Related Os- teonecrosis of the Jaw. Dent Clin N Am 58:369–384, 2014
Vandone AM, Donadio M, Mozzati M, et al: Impact of dental care in the prevention of bisphosphonate-associated osteonecrosis of the jaw: a single-center clinical experience. Ann Oncol 23:193, 2012
Vannucci L & Brandi ML: Pharmacological management of osteoporosis
– when to treat and when to stop, Expert Review of Clinical Phar- macology, 1:1-8, 2016
Vincenzi B, Santini D, Dicuonzo G, et al: Zoledronic acid-related an- giogenesis modifications and survival in advanced breast cancer patients. J Interferon Cytokine Res 25:144–51, 2005
Watts NB, Adler RA, Bilezikian JP: Endocrine Society et al. Osteoporo- sis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97(6):1802–1822, 2012
Watts NB: Long-term risks of bisphosphonate therapy. Arq Bras En- docrinol Metab 58(5):523–529, 2014
Weinstein RS, Roberson PK, Manolagas SC: Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360:53- 62, 2009
World Health Organization Collaborating Centre for Metabolic Bone Diseases. FRAXA WHO Fracture Risk Assessment Tool. Available at: http://www.shef.ac.uk/FRAX/ (accessed 28.10.09).
World Health Organization scientific group on the assessment of os- teoporosis at primary health care level, summary meeting report, Brussels, Belgium, 5-7 May 2004
Department of Oral and Maxillofacial Surgery, School of Dentistry, National and Kapodistrian University of Athens (Head: Professor N. G. Papadogeorgakis)
Hellenic Archives of Oral & Maxillofacial Surgery (2018) 2, 89-104
SUMMARY: The traditionally high incidence of osteo- porosis along with the gradually increasing pharmacological treatment with the use of modern antiresorptive medication among others, make it quite certain that the dentist will come across patients, who are being treated with this kind of medication. Medication related osteonecrosis of the jaw (MRONJ), is a serious disease that has been associated among others with teeth extraction, implant surgery, and trauma due to ill-fitting dentures. In this paper, the modern literature concerning osteoporosis, its treatment options, and the management of those patients who are treated with antiresorptive med- ication against osteoporosis, are presented.
KEY WORDS: Osteopenia, osteoporosis, bisphospho- nates, denosumab, antiresorptives, osteonecrosis of the jaw, MRONJ
REFERENCES
Allen MR, Pandya B, Ruggiero SL: Lack of correlation between dura- tion of osteonecrosis of the jaw and sequestra tissue morphology: what it tells us about the condition and what it means for future studies. J Oral Maxillofac Surg. 68:2730–4, 2010
Allen MR, Ruggiero SL: Higher bone matrix density exists in only a subset of patients with bisphosphonate-related osteonecrosis of the jaw. J Oral Maxillofac Surg. 67:1373–7, 2009
Background Document for Meeting of Advisory Committee for Re- productive Health Drugs and Drug Safety and Risk Management Advisory Committee. United States. Food and Drug Administra- tion. September 9, 2011; http://www.fda.gov/downloads/ Adviso- ryCommittees/CommitteesMeetingMaterials/drugs/DrugSafetyan dRiskManagementAdvisoryCommittee/ucm270958.pdf. Accessed February 10, 2014
Barasch A, Cunha-Cruz J, Curro FA, et al: Risk factors for osteonecrosis of the jaws: a case-control study from the CONDOR dental PBRN. J Dent Res. 90:439–44, 2011
Black DM, Clifford J. Rosen, MD: Postmenopausal Osteoporosis. N Engl J Med 374:254-62, 2016
Black DM, Bilezikian JP, Ensrud KE, et al: One year of alendronate after one year of parathyroid hormone (1-84) for osteoporosis. N Engl J Med 353: 555-65, 2016
Black DM, Reid IR, Boonen S, et al: The effect of 3 versus 6 years of zoledronic acid treatment of osteoporosis: a randomized exten- sion to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 27:243, 2012
Bonacina R, Mariani U, Villa F, et al: Preventive strategies and clinical implications for bisphosphonate-related osteonecrosis of the jaw: a review of 282 patients. J Can Dent Assoc 77:b147, 2011
Bone HG, Chapurlat R, Brandi ML, et al: The effect of three or six years of denosumab exposure in women with postmenopausal osteoporosis: results from the FREEDOM extension. J Clin En- docrinol Metab 98(11):4483–4492, 2013
Boonen S, Ferrari S, Miller PD, et al: Postmenopausal osteoporosis treatment with antiresorptives: effects of discontinuation or longterm continuation on bone turnover and fracture risk—a per- spective. J Bone Miner Res. 27(5):963–974, 2012
Burch J, Rice S, Yang H, NeilsonA, Stirk L, Francis R, Holloway P, Selby P, Craig D: Systematic review of the use of bone turnover markers for monitoring the response to osteoporosis treatment: the sec- ondary prevention of fractures, and primary prevention of frac- tures in high-risk groups. Health Technol Assess (Winchester, Eng- land) 18(11):1-206, 2014
Cauley JA, Robbins J, Chen Z, et al: Effects of estrogen plus progestin on risk of fracture and bone mineral density: the Women’s Health Initiative randomized trial. JAMA 290: 1729-38, 2003
Cosman F., S. J. de Beur, M. S. LeBoff, E. M. Lewiecki, B. Tanner, S. Ran- dall, R. Lindsay: Clinician’s Guide to Prevention and Treatment of Osteoporosis. Osteoporos Int. 25:2359–2381, 2014
Cummings SR, San Martin J, McClung MR et al: Denosumab for pre- vention of fractures in postmenopausal women with osteoporosis. N Engl J Med 361(8):756–765, Erratum in: N Engl J Med 361(19):1914, 2009
Dallas SL, Prideaux M, Bonewald LF: The osteocyte: an endocrine cell and more. Endocr Rev. Oct;34(5):658-90, 2013
Damm DD, Jones DM: Bisphosphonate-related osteonecrosis of the jaws: a potential alternative to drug holidays. Gen Dent 61:33, 2013 Dodson TB: The Frequency of Medication-related Osteonecrosis of the Jaw and its Associated Risk Factors. Oral Maxillofac Surg Clin
North Am 27:509-16, 2015
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women with osteoporosis. N Engl J Med 344: 1434-41, 2001 Nelson HD, Haney EM, Chou R, Dana T, Fu R, Bougatsos C: Screening
for osteoporosis: systematic review to update the 2002 US Pre- ventive Services Task Force Recommendation. Evidence Synthe- ses No. 77. AHRQ Publication No. 10-05145-EF-1. Agency for Healthcare Research and Quality, (US), Rockville, 2010
Otto S, Tröltzsch M, Jambrovic V, Panya S, Probst F, Ristow O, Ehren- feld M, Pautke C: Tooth extraction in patients receiving oral or intravenous bisphosphonate administration: A trigger for BRONJ development?, J Craniomaxillofac Surg. 43(6):847-54, 2015
Otto S, Pautke C, Martin Jurado O, Nehrbass D, Stoddart MJ, Ehren- feld M, Zeiter S: Further development of the MRONJ minipig large animal model. J Craniomaxillofac Surg. 45(9):1503-1514, 2017
Papapoulos S, Lippuner K, Roux C, et al: The effect of 8 or 5 years of denosumab treatment in postmenopausal women with osteo- porosis: results from the FREEDOM Extension study. Osteoporos Int 26(12):2773–2783, 2015
Raggatt LJ, Partridge NC: Cellular and molecular mechanisms of bone remodelling. J Biol Chem. 13;285(33):25103-8, 2010
Recker RR, Ste-Marie LG, Chavassieux P, et al: Bone safety with rise- dronate: histomorphometric studies at different dose levels and exposure. Osteoporos Int. 26(1):327–337, 2015
Richman S, Edusa V, Fadiel A, Naftolin F: Low-dose estrogen therapy for prevention of osteoporosis: working our way back to monotherapy. Menopause 13: 148-55, 2006
Root AW, Diamond FB: Disorders of mineral homeostasis in newborn, infant, child, and adolescent. In: Sperling MA, editor. Pediatric en- docrinology. Philadelphia: Elsevier Saunders p. 686–769, 2008
Ripamonti CI, Maniezzo M, Campa T, et al: Decreased occurrence of osteonecrosis of the jaw after implementation of dental preven- tive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan. Ann Oncol 20:137, 2009
Ruggiero SL, Dodson TB, Fantasia J, et al: American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on medication-related os- teonecrosis of the jaw—2014 update. J Oral Maxillofac Surg Oct 72(10):1938–56, 2014
Saad F, Brown JE, Van PC, et al: Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases. Ann Oncol 23:1341–7, 2012
Saia G, Blandamura S, Bettini G, Tronchet A, Totola A, Bedogni G, et al: Occurrence of bisphosphonate-related osteonecrosis of the jaw after surgical tooth extraction. J Oral Maxillofac Surg 68: 797- 804, 2010
Santini D, Vincenzi B, Dicuonzo G, et al: Zoledronic acid induces sig- nificant and long-lasting modifications of circulating angiogenic fac- tors in cancer patients. Clin Cancer Res 9:2893–7, 2003
Schubert M, Klatte I, Linek W, et al: The Saxon bisphosphonate register - therapy and prevention of bisphosphonate-related osteonecrosis of the jaws. Oral Oncol 48:349–54, 2012
Schousboe JT, Nyman JA, Kane RL, Ensrud KE: Costeffectiveness of al- endronate therapy for osteopenic postmenopausal women. Ann Intern Med 142:734–41, 2005
Scoletta M, Arduino PG, Pol R, et al: Initial experience on the outcome of teeth extractions in intravenous bisphosphonate treated pa- tients: a cautionary report. J Oral Maxillofac Surg 69:456–62, 2011 Sharma D, Ivanovski S, Slevin M, et al: Bisphosphonate-related os- teonecrosis of jaw (BRONJ): diagnostic criteria and possible path- ogenic mechanisms of an unexpected anti-angiogenic side effect.
Vasc Cell 5:1–5, 2013
Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al: Bone mineral density thresholds for pharmacological in- terventions to prevent fractures. Arch Intern Med. 164:1108–12, 2004
Soldatos N, Melakopoulos I, Silvestros S, Kontakiotis G, Katsikeris N: Bisphosphonates and implants. Literature review, guidelines and case reports display. Stoma 38:139-147, 2010
Tamiolakis P, Thermos G, Charoulis A, Chrysomali A, Sklavounou-An- drikopoulou A: Medication related osteonecrosis of the jaws. Lit- erature review. Hellenic Archives of Oral and Maxillofacial Sur- gery, 19(1):11-34, 2018
Thumbigere-Math V, Tu L, Huckabay S, et al: A retrospective study evaluating frequency and risk factors of osteonecrosis of the jaw in 576 cancer patients receiving intravenous bisphosphonates. Am J Clin Oncol 35:386–92, 2012
Uyanne J, Calhoun CC, Le AD, et al: Antiresorptive Drug–Related Os- teonecrosis of the Jaw. Dent Clin N Am 58:369–384, 2014
Vandone AM, Donadio M, Mozzati M, et al: Impact of dental care in the prevention of bisphosphonate-associated osteonecrosis of the jaw: a single-center clinical experience. Ann Oncol 23:193, 2012
Vannucci L & Brandi ML: Pharmacological management of osteoporosis – when to treat and when to stop, Expert Review of Clinical Phar- macology, 1:1-8, 2016
Vincenzi B, Santini D, Dicuonzo G, et al: Zoledronic acid-related an- giogenesis modifications and survival in advanced breast cancer patients. J Interferon Cytokine Res 25:144–51, 2005
Watts NB, Adler RA, Bilezikian JP: Endocrine Society et al. Osteoporo- sis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97(6):1802–1822, 2012
Watts NB: Long-term risks of bisphosphonate therapy. Arq Bras En- docrinol Metab 58(5):523–529, 2014
Weinstein RS, Roberson PK, Manolagas SC: Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360:53- 62, 2009
World Health Organization Collaborating Centre for Metabolic Bone Diseases. FRAXA WHO Fracture Risk Assessment Tool. Available at: http://www.shef.ac.uk/FRAX/ (accessed 28.10.09).
World Health Organization scientific group on the assessment of os- teoporosis at primary health care level, summary meeting report, Brussels, Belgium, 5-7 May 2004
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 68:243, 2010
Marx RE, Sawatari Y, Fortin M, Broumand V: Bisphosphonate induced exposed bone (osteonecrosis/osteopetrosis) of the jaws: risk fac- tors, recognition, prevention, and treatment. J Oral Maxillofac Surg 63:1567–75, 2005
Marx RE, Cillo JE Jr, Ulloa JJ: Oral bisphosphonate induced osteonecro- sis: risk factors, prediction of risk using CTx testing, prevention and treatment. J Oral Maxillofac Surg 65:2397-2410, 2007
McClung M, Harris ST, Miller PD, et al: Bisphosphonate therapy for osteoporosis: benefits, risks, and drug holiday. Am J Med 126 (1):13–20, 2013
Modi A, Siris ES, Tang J, Sen S: Cost and consequences of noncompli- ance with osteoporosis treatment among women initiating ther- apy. Curr Med Res Opin 31: 757-65, 2015
Mozzati M, Arata V, Gallesio G: Tooth extraction in osteoporotic pa- tients taking oral bisphosphonates. Osteoporos Int 24: 1707-1712, 2013
Nakashima T, Hayashi M, Takayanagi H: New insights into osteoclas- togenic signaling mechanisms. Trends Endocrinol Metab. Nov;23(11):582-90, 2012
National Osteoporosis Foundation. Health professional’s guide to reha- bilitation of the patient with osteoporosis. 2003 Washington, DC 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 344: 1434-41, 2001 Nelson HD, Haney EM, Chou R, Dana T, Fu R, Bougatsos C: Screening
for osteoporosis: systematic review to update the 2002 US Pre- ventive Services Task Force Recommendation. Evidence Synthe- ses No. 77. AHRQ Publication No. 10-05145-EF-1. Agency for Healthcare Research and Quality, (US), Rockville, 2010
Otto S, Tröltzsch M, Jambrovic V, Panya S, Probst F, Ristow O, Ehren- feld M, Pautke C: Tooth extraction in patients receiving oral or intravenous bisphosphonate administration: A trigger for BRONJ development?, J Craniomaxillofac Surg. 43(6):847-54, 2015
Otto S, Pautke C, Martin Jurado O, Nehrbass D, Stoddart MJ, Ehren- feld M, Zeiter S: Further development of the MRONJ minipig large animal model. J Craniomaxillofac Surg. 45(9):1503-1514, 2017
Papapoulos S, Lippuner K, Roux C, et al: The effect of 8 or 5 years of denosumab treatment in postmenopausal women with osteo- porosis: results from the FREEDOM Extension study. Osteoporos Int 26(12):2773–2783, 2015
Raggatt LJ, Partridge NC: Cellular and molecular mechanisms of bone remodelling. J Biol Chem. 13;285(33):25103-8, 2010
Recker RR, Ste-Marie LG, Chavassieux P, et al: Bone safety with rise- dronate: histomorphometric studies at different dose levels and exposure. Osteoporos Int. 26(1):327–337, 2015
Richman S, Edusa V, Fadiel A, Naftolin F: Low-dose estrogen therapy for prevention of osteoporosis: working our way back to monotherapy. Menopause 13: 148-55, 2006
Root AW, Diamond FB: Disorders of mineral homeostasis in newborn, infant, child, and adolescent. In: Sperling MA, editor. Pediatric en- docrinology. Philadelphia: Elsevier Saunders p. 686–769, 2008
Ripamonti CI, Maniezzo M, Campa T, et al: Decreased occurrence of osteonecrosis of the jaw after implementation of dental preven- tive measures in solid tumour patients with bone metastases treated with bisphosphonates. The experience of the National Cancer Institute of Milan. Ann Oncol 20:137, 2009
Ruggiero SL, Dodson TB, Fantasia J, et al: American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on medication-related os- teonecrosis of the jaw—2014 update. J Oral Maxillofac Surg Oct 72(10):1938–56, 2014
Saad F, Brown JE, Van PC, et al: Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases. Ann Oncol 23:1341–7, 2012
Saia G, Blandamura S, Bettini G, Tronchet A, Totola A, Bedogni G, et al: Occurrence of bisphosphonate-related osteonecrosis of the jaw after surgical tooth extraction. J Oral Maxillofac Surg 68: 797- 804, 2010
Santini D, Vincenzi B, Dicuonzo G, et al: Zoledronic acid induces sig- nificant and long-lasting modifications of circulating angiogenic fac- tors in cancer patients. Clin Cancer Res 9:2893–7, 2003
Schubert M, Klatte I, Linek W, et al: The Saxon bisphosphonate register
- therapy and prevention of bisphosphonate-related osteonecrosis of the jaws. Oral Oncol 48:349–54, 2012
Schousboe JT, Nyman JA, Kane RL, Ensrud KE: Costeffectiveness of al- endronate therapy for osteopenic postmenopausal women. Ann Intern Med 142:734–41, 2005
Scoletta M, Arduino PG, Pol R, et al: Initial experience on the outcome of teeth extractions in intravenous bisphosphonate treated pa- tients: a cautionary report. J Oral Maxillofac Surg 69:456–62, 2011 Sharma D, Ivanovski S, Slevin M, et al: Bisphosphonate-related os- teonecrosis of jaw (BRONJ): diagnostic criteria and possible path- ogenic mechanisms of an unexpected anti-angiogenic side effect.
Vasc Cell 5:1–5, 2013
Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al: Bone mineral density thresholds for pharmacological in- terventions to prevent fractures. Arch Intern Med. 164:1108–12, 2004
Soldatos N, Melakopoulos I, Silvestros S, Kontakiotis G, Katsikeris N: Bisphosphonates and implants. Literature review, guidelines and case reports display. Stoma 38:139-147, 2010
Tamiolakis P, Thermos G, Charoulis A, Chrysomali A, Sklavounou-An- drikopoulou A: Medication related osteonecrosis of the jaws. Lit- erature review. Hellenic Archives of Oral and Maxillofacial Sur- gery, 19(1):11-34, 2018
Thumbigere-Math V, Tu L, Huckabay S, et al: A retrospective study evaluating frequency and risk factors of osteonecrosis of the jaw in 576 cancer patients receiving intravenous bisphosphonates. Am J Clin Oncol 35:386–92, 2012
Uyanne J, Calhoun CC, Le AD, et al: Antiresorptive Drug–Related Os- teonecrosis of the Jaw. Dent Clin N Am 58:369–384, 2014
Vandone AM, Donadio M, Mozzati M, et al: Impact of dental care in the prevention of bisphosphonate-associated osteonecrosis of the jaw: a single-center clinical experience. Ann Oncol 23:193, 2012
Vannucci L & Brandi ML: Pharmacological management of osteoporosis
– when to treat and when to stop, Expert Review of Clinical Phar- macology, 1:1-8, 2016
Vincenzi B, Santini D, Dicuonzo G, et al: Zoledronic acid-related an- giogenesis modifications and survival in advanced breast cancer patients. J Interferon Cytokine Res 25:144–51, 2005
Watts NB, Adler RA, Bilezikian JP: Endocrine Society et al. Osteoporo- sis in men: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 97(6):1802–1822, 2012
Watts NB: Long-term risks of bisphosphonate therapy. Arq Bras En- docrinol Metab 58(5):523–529, 2014
Weinstein RS, Roberson PK, Manolagas SC: Giant osteoclast formation and long-term oral bisphosphonate therapy. N Engl J Med 360:53- 62, 2009
World Health Organization Collaborating Centre for Metabolic Bone Diseases. FRAXA WHO Fracture Risk Assessment Tool. Available at: http://www.shef.ac.uk/FRAX/ (accessed 28.10.09).
World Health Organization scientific group on the assessment of os- teoporosis at primary health care level, summary meeting report, Brussels, Belgium, 5-7 May 2004
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