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Journal of Bone and Mineral Research | 2007

Bisphosphonate-Associated Osteonecrosis of the Jaw: Report of a Task Force of the American Society for Bone and Mineral Research

Sundeep Khosla; David B. Burr; Jane A. Cauley; David W. Dempster; Peter R. Ebeling; Dieter Felsenberg; Robert F. Gagel; Vincente Gilsanz; Theresa A. Guise; Sreenivas Koka; Laurie K. McCauley; Joan McGowan; Marc D. McKee; Suresh Mohla; David G. Pendrys; Lawrence G. Raisz; Salvatore L. Ruggiero; David Shafer; Lillian Shum; Stuart L. Silverman; Catherine Van Poznak; Nelson B. Watts; Sook-Bin Woo; Elizabeth Shane

ONJ has been increasingly suspected to be a potential complication of bisphosphonate therapy in recent years. Thus, the ASBMR leadership appointed a multidisciplinary task force to address key questions related to case definition, epidemiology, risk factors, diagnostic imaging, clinical management, and future areas for research related to the disorder. This report summarizes the findings and recommendations of the task force.


Annals of Internal Medicine | 2006

Systematic Review: Bisphosphonates and Osteonecrosis of the Jaws

Sook-Bin Woo; John W. Hellstein; John R. Kalmar

Key Summary Points Osteonecrosis of the jaws is strongly associated with the use of aminobisphosphonates, and the mechanism of disease is probably severe suppression of bone turnover. Ninety-four percent of patients are treated with zoledronic acid or pamidronate or both; 85% of affected patients have multiple myeloma or metastatic breast cancer, and 4% have osteoporosis. The prevalence of osteonecrosis in patients with cancer is 6% to 10% and the prevalence in those taking alendronate for osteoporosis is unknown; osteonecrosis seems to be time- and dose-dependent because of the long half-life of aminobisphosphonates. More than half of all cases (60%) occur after dentoalveolar surgery (such as tooth extraction) to treat infections, and the remaining 40% are probably related to infection, denture trauma, or other physical trauma. Preventive strategies include removing all foci of dental infection before starting bisphosphonate therapy. Treatment is directed toward control of pain and infection and careful local dbridement of dead bone, but not wide excision of lesions. Bisphosphonates are used to treat osteoporosis, Paget disease of bone and other metabolic bone diseases, multiple myeloma, and skeletal events associated with metastatic neoplasms. Their primary mechanism of action is inhibition of osteoclastic resorption of bone. Within the past 2 years, an increasing body of literature has suggested that bisphosphonate use, especially intravenous preparations, may be associated with osteonecrosis of the jaws. We briefly review the action of bisphosphonates, outline the clinical manifestations of bisphosphonate-associated osteonecrosis of the jaws, summarize current treatment strategies, discuss possible mechanisms of etiopathogenesis, and suggest avenues of research. Methods We performed MEDLINE and PubMed searches of English- and foreign-language literature (1966 to 31 January 2006) using the following Medical Subject Headings (MeSH) and terms: osteonecrosis, avascular necrosis, phosphorous necrosis, bisphosphonates, and diphosphonates. We then crossed the same terms with the terms jaw diseases, myeloma, breast cancer, and metastatic cancer. Other references were obtained from citations from retrieved articles. Similar terms were used to search abstracts from meetings of the American Society of Clinical Oncology. We specifically reviewed all case reports and case series of patients with bisphosphonate-associated osteonecrosis of the jaws. We included any report that provided acceptable documentation of disease and use of bisphosphonates, regardless of whether it included information on the sex of patients, the site of the lesions, and the bisphosphonate used. Several authors published more than 1 paper describing patients with osteonecrosis. Through direct communication with these authors, we confirmed that some of the same patients were included in multiple reports. When this occurred, we used and cited data only from the larger, more recent publication. No funding was received for this study. Actions of Bisphosphonates Bisphosphonates are powerful inhibitors of osteoclastic activity. They are analogues of inorganic pyrophosphates with low intestinal absorption, are excreted through the kidneys without metabolic alteration, and have a high affinity for hydroxyapatite crystals (1, 2). Because they are incorporated into the skeleton without being degraded, they are remarkably persistent drugs; the estimated half-life for alendronate is up to 12 years (3). Alendronate, risedronate, pamidronate, zoledronic acid, and ibandronate, which are called aminobisphosphonates, have much higher potency because they contain nitrogen in a side chain (Table 1). Table 1. Bisphosphonate Formulations The nonaminobisphosphonates are metabolized by osteoclasts to inactive nonhydrolyzable adenosine triphosphate analogues that are directly cytotoxic to the cell and induce apoptosis (1, 2). The newer aminobisphosphonates have 2 actions (4): induction of another adenosine triphosphate analogue that induces apoptosis, and inhibition of farnesyl diphosphonate synthase, which is part of the mevalonate pathway of cholesterol synthesis. Such inhibition results in dysregulation of intracellular transport, cytoskeletal organization, and cell proliferation, leading to inhibition of osteoclast function. In addition, aminobisphosphonates reduce recruitment of osteoclasts and induce osteoblasts to produce an osteoclast-inhibiting factor (5, 6). Aminobisphosphonates exert several antitumor effects, including induction of tumor cell apoptosis, inhibition of tumor cell adhesion to the extracellular matrix, and inhibition of tumor invasion (4, 7). Bisphosphonates also have antiangiogenesis properties (8, 9) and can activate T cells (10, 11). The use of bisphosphonates in patients with multiple myeloma and metastatic cancer to the bones, such as breast, prostate, lung, and renal cell carcinomas, has resulted in a statistically significant reduction in skeletal complications, including pathologic fractures, spinal cord compression, hypercalcemia of malignant disease, and the need for subsequent radiotherapy or surgery to bone (12-14). Intravenous bisphosphonates have improved bioavailability and do not produce gastrointestinal side effects, resulting in better patient adherence. They have become standard therapy in the management of patients with multiple myeloma and metastatic cancer. Potential Adverse Effects of Bisphosphonate Actions In normal bone homeostasis, osteoclastic resorption is tightly linked to osteoblastic bone deposition and both functions are essential for repair of physiologic microdamage. Prolonged use of bisphosphonates may suppress bone turnover to the point that such microdamage persists and accumulates (15). The result is hypodynamic bone with decreased biomechanical competence. Although osteoblastic function is also reduced during bisphosphonate therapy, continued mineralization yields a hard, brittle bone with an osteopetrotic appearance and an increased risk for fracture (16-18). Thus, some experts caution that the benefits of prolonged use of bisphosphonates must be carefully weighed against the potential negative effects of oversuppression of bone metabolism (1, 19, 20). Other experts argue that although long-term use of bisphosphonates may retard fracture healing or slow callus remodeling, it may not affect bone mineralization or mechanical properties (21, 22). Oral Complications of Bisphosphonate Therapy Although oral bisphosphonates may cause oral mucosal lesions (purportedly arising from direct contact injury) (23, 24), we focus our review on bisphosphonate-associated osteonecrosis of the jaw. Table 2 summarizes 368 reported cases of bisphosphonate-associated osteonecrosis of the jaw (25-54). Reported cases manifested as exposure of portions of the bone of the mandible only (65%), maxilla only (26%), or both (9%). Approximately one third of lesions were painless (27), and there was a slight female predilection in a ratio of 3:2 among all reported cases. Multifocal or bilateral involvement was slightly more common in the maxilla than in the mandible (31% vs. 23%). Most lesions were on the posterior lingual mandible near the mylohyoid ridge. Of importance, 60% of cases occurred after a tooth extraction or other dentoalveolar surgery and the remaining cases occurred spontaneously. The latter cases often involved patients wearing dentures, a possible source of local trauma. Marx and colleagues (27) reported that 39% of cases that occurred spontaneously were located on bony exostoses that were easily traumatized. There is 1 case report of dental implant failure associated with bisphosphonate use (55). Table 2. Reports of Cases of Bisphosphonate-Associated Osteonecrosis of the Jaws Most patients (94%) were treated with intravenous bisphosphonates (primarily pamidronate and zoledronic acid), and most patients (85%) had multiple myeloma or metastatic breast cancer (Table 3). The remaining patients were taking oral bisphosphonates for osteoporosis or Paget disease of bone (25, 27-29, 40, 50, 51). Table 3. Primary Diagnoses and Types of Bisphosphonates in Reported Cases of Osteonecrosis of the Jaws Clinically, intraoral lesions appear as areas of exposed yellow-white, hard bone with smooth or ragged borders (Figures 1 and 2). Extraoral or intraoral sinus tracts may be present (Figure 3). Painful ulcers may develop in soft tissues that impinge on the ragged bony margins. Figure 1. Osteonecrosis of the right mandible after tooth extraction in a patient taking zoledronic acid for metastatic breast cancer. Figure 2. Osteonecrosis of the palatal torus in a patient with osteoporosis taking alendronate. Figure 3. Extraoral fistula in a patient with intraoral osteonecrosis. Results of radiographic evaluation may be negative in early cases. Although some investigators have noted subtle changes, such as widening of the periodontal ligament, these findings are indistinguishable from chronic periodontal infection, a predisposing factor for osteonecrosis (27). Advanced cases show a moth-eaten, poorly defined radiolucency, with or without radio-opaque sequestra. In 1 series, 5 of 63 patients developed pathologic jaw fractures (25). Cultures of exposed bone may identify Actinomyces species, but care must be taken to distinguish between a true suppurative infection and mere surface colonization by Actinomyces, because such organisms are a common component of dental plaque. Patients with bisphosphonate-associated osteonecrosis may present similarly to those with osteoradionecrosis of the jaws. Osteoradionecrosis is a complication of radiotherapy. It is thought to result from osteocyte and microvascular damage after the jaws are exposed to ionizing radiation and also frequently occurs after tooth extraction (56). Osteoradionecrosis, however, infrequently involves the maxilla (<5% of cases) and is more common in men than in women (57, 58). Risk Fac


Critical Reviews in Oral Biology & Medicine | 1997

Graft-vs.-Host Disease

Sook-Bin Woo; Stephanie J. Lee; Mark M. Schubert

Bone marrow transplantation (BMT) is the treatment of choice for many leukemias, lymphomas, bone marrow failure syndromes, and immunodeficiency disorders, and is the primary and salvage therapy for many solid malignancies. With the establishment of national and international marrow banks, unrelated allogeneic BMT is being performed with increasing frequency. Graft-vs.-host disease (GVHD) remains a major complication of allogeneic BMT, occurring in 25% to 70% of patients despite GVHD prophylaxis, with the skin, gastro-intestinal tract, and liver as primary target organs. Oral findings are seen in both acute and chronic GVHD. In acute GVHD, the oral lesions are often painful, erythematous, ulcerative, and desquamative. In chronic GVHD, they are lichenoid with associated erythema and ulcerations; additionally, they may be associated with a sicca syndrome characterized by xerostomia and progressive salivary gland atrophy. General principles of BMT are discussed, as are systemic and local therapeutic options for oral GVHD.


Cancer | 1993

A Longitudinal Study of Oral Ulcerative Mucositis in Bone Marrow Transplant Recipients

Sook-Bin Woo; Stephen T. Sonis; Michael Monopoli; Andrew L. Sonis

Background. Few longitudinal studies have investigated the onset, duration, and resolution of ulcerative mucositis in bone marrow transplant recipients. This study prospectively followed a group of such patients on a daily basis to obtain data on the incidence of ulcerative mucositis, location and duration of lesions, severity with different conditioning regimens, and the relationship of such mucositis to the absolute neutrophil count.


Clinical Cancer Research | 2008

Clinical, Radiographic, and Biochemical Characterization of Multiple Myeloma Patients with Osteonecrosis of the Jaw

Noopur Raje; Sook-Bin Woo; Karen Hande; Jeffrey T. Yap; Paul G. Richardson; Sonia Vallet; Nathaniel S. Treister; Teru Hideshima; Niall Sheehy; Shweta Chhetri; Brendan D. Connell; Wanling Xie; Yu-Tzu Tai; Agnieszka Szot-Barnes; Mei Tian; Robert Schlossman; Edie Weller; Nikhil C. Munshi; Annick D. Van den Abbeele; Kenneth C. Anderson

Purpose: Osteonecrosis of the jaw (ONJ) has been reported in patients with a history of aminobisphosphonate use. This study was conducted in order to define ONJ clinically and radiographically and gain insights into its pathophysiology. Experimental Design: Eleven multiple myeloma (MM) patients with ONJ were included in the study. Patients underwent clinical, biochemical, radiographic, and molecular profiling. Ten MM patients on aminobisphosphonates without ONJ and five healthy volunteers were used as controls for biochemical and molecular studies. Results: MM patients with ONJ were treated with either pamidronate (n = 3), zoledronate (n = 4), or both agents sequentially (n = 4) for a mean of 38.7 months. Radiographic studies showed bone sclerosis and fragmentation on plain films and computerized tomography. Quantitative regional analysis of NaF-PET and FDG-PET scans confirmed an increased standardized uptake value (SUVmax) in areas of ONJ. The target to background ratio of SUVmax was significantly greater for NaF-PET compared with FDG-PET scan. Biochemical bone marker data and transcriptional profiling studies showed that genes and proteins involved in osteoblast and osteoclast signaling cascades were significantly down-regulated in patients with ONJ. Conclusions: ONJ was associated with a mean duration of 38.7 months of aminobisphosphonate exposure. Radiographic and functional imaging confirmed sites of clinically established ONJ. Gene and protein studies are consistent with altered bone remodeling, evidenced by suppression of both bone resorption and formation.


Supportive Care in Cancer | 2010

A systematic review of bisphosphonate osteonecrosis (BON) in cancer

Cesar A. Migliorati; Sook-Bin Woo; Ian Hewson; Andrei Barasch; Linda S. Elting; Fred K. L. Spijkervet; Michael T. Brennan

PurposeThis systematic review aims to examine the prevalence of bisphosphonate osteonecrosis (BON) in the cancer population, prevention and treatment protocols, and quality of life issues.MethodsA search of MEDLINE/PubMed and EMBASE form October 2003 to December 31, 2008 was conducted with the objective of identifying publications that contained original data regarding BON.ResultsA total of 28 publications fulfilled inclusion criteria, but only 22 were used for prevalence analysis. No randomized controlled clinical trials, meta-analysis, or quality of life papers were found that contained information regarding either prevalence or treatment protocols for the management of BON. The overall weighted prevalence of BON included a sample of 39,124 patients with a mean weighted prevalence of 6.1%. The weighted prevalence was 13.3% for studies with documented follow-up with a sample size of 927 individuals. The weighted prevalence in studies with undocumented follow-up was 0.7% in a sample of 8,829 chart reviews. Epidemiological studies evaluated a total of 29,368 individual records, and the weighted BON prevalence was 1.2%.ConclusionsHigh-quality studies are needed to accurately characterize the prevalence of BON, and to determine effective treatment protocols.


Oncologist | 2011

Quality of Life Implications of Bisphosphonate-Associated Osteonecrosis of the Jaw

Rebecca A. Miksad; Kuan-Chi Lai; Thomas B. Dodson; Sook-Bin Woo; Nathaniel S. Treister; O. Akinyemi; M. M. Bihrle; Guy Maytal; Meredith August; Gazelle Gs; Swan Js

PURPOSE Potentially debilitating, osteonecrosis of the jaw (ONJ) is an emerging complication of bisphosphonates. However, its effect on quality of life (QoL) is unknown. We determined the ONJ-related QoL decline in a cancer patient cohort. PATIENTS AND METHODS Thirty-four cancer patients with bisphosphonate-associated ONJ completed a telephone survey (October 2007 through May 2008). The Oral Health Impact Profile 14 (OHIP) retrospectively assessed participant oral health-related QoL before and after ONJ. Standardized ONJ descriptions were developed in a multidisciplinary, iterative process and were evaluated with three frequently used preference-based QoL measurement methods on a 0 (death) to 1 (perfect health) scale: Visual Analogue Scale (VAS), Time Trade-Off (TTO), and EQ-5D. RESULTS ONJ significantly (p < .001) increased OHIP scores (worse QoL) for additive (3.56-16.53) and weighted (7.0-17.5) methods. Seven individual OHIP items significantly increased (Bonferroni correction p < .0035): pain, eating discomfort, self-consciousness, unsatisfactory diet, interrupted meals, irritability, and decreased life satisfaction. Mean preference-based QoL values significantly decreased (p < .001) with worsening ONJ stage (VAS, TTO, and EQ-5D): no ONJ (0.76, 0.86, 0.82), ONJ stage 1 (0.69, 0.82, 0.78), ONJ stage 2 (0.51, 0.67, 0.55), and ONJ stage 3 (0.37, 0.61, 0.32). As ONJ worsened, EQ-5D domain scores significantly increased (p < .001). Pain/discomfort and anxiety/depression contributed most to declining QoL. CONCLUSIONS ONJ significantly affects QoL, a detriment that increases with worsening ONJ. QoL impairments for ONJ stages 2 and 3 are similar to other treatment side effects that influence decision-making. Bisphosphonate-associated ONJ QoL is an important consideration for patients, clinicians, and policy makers.


Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology | 2010

Use of cone-beam computerized tomography for evaluation of bisphosphonate-associated osteonecrosis of the jaws

Nathaniel S. Treister; Bernard Friedland; Sook-Bin Woo

BACKGROUND AND OBJECTIVE Bisphosphonate-associated osteonecrosis of the jaws (BONJ) is characterized by exposed nonvital maxillary or mandibular bone. Cone-beam computerized tomography (CBCT) is an attractive modality for 3-dimensional imaging of the jaws. The purpose of this study was to compare the clinical and radiographic features of a series of 7 subjects with BONJ who were evaluated by both CBCT and digital panoramic radiography. STUDY DESIGN Seven subjects with BONJ were evaluated by clinical examination, CBCT, and digital panoramic radiography. RESULTS Radiographic findings included sclerosis, cortical irregularity, lucency, mottling, fragmentation/sequestra formation, sinus communication, and persistent sockets. There was high correlation between the anatomic location of clinical and radiographic findings. In nearly all cases, CBCT demonstrated a greater extent and quality of changes compared with panoramic radiography. CONCLUSIONS Cone-beam CT is superior to panoramic radiography in its ability to characterize the nature and extent of radiographic changes in BONJ. Use of CBCT should be strongly considered when radiographic evaluations are included in prospective research investigations of BONJ. However, in the majority of cases of BONJ the clinical significance of improved imaging remains unclear, and therefore specific guidelines for routine clinical care cannot be recommended at this time.


Cancer | 1990

The role of herpes simplex virus in the development of oral mucositis in bone marrow transplant recipients

Sook-Bin Woo; Stephen T. Sonis; Andrew L. Sonis

Herpes simplex virus (HSV) has been implicated as a major etiologic factor in the development of ulcerative mucositis in bone marrow transplant (BMT) recipients. in this study, 60 patients who received BMTs were evaluated for at least 30 days post‐transplant for ulcerative mucositis and the presence of culturable HSV. Fiftynine patients received prophylactic acyclovir. Forty‐six patients developed ulcerative lesions and 45 of these were culture negative for HSV. Neither the source of transplant (autologous versus allogenic) nor the HSV antibody status of the patient affected the frequency of mucositis. the conditioning regimen appeared to be the most significant factor contributing to the severity of ulcerative mucositis. While the majority of ulcers occurred on movable nonkeratinized mucosa in BMT recipients, the usual sites of reactivation of intraoral HSV are nonmovable, keratinized mucosa. We conclude that HSV is probably not a major etiologic agent of mucositis in BMT recipients and that acyclovir is an effective agent in preventing HSV reactivation.


Modern Pathology | 2013

Human papillomavirus-associated oral intraepithelial neoplasia

Sook-Bin Woo; Emma C Cashman; Mark A. Lerman

This study evaluated an unusual subset of oral epithelial dysplasia for the presence of transcriptionally active high-risk HPV subtypes and to further characterize the histological criteria for this condition. There were 20 cases diagnosed as epithelial dysplasia with marked apoptosis of the anterior oral cavity. Clinical and follow-up data were collected and histopathological features were documented. Immunoperoxidase studies were performed for p16 and in situ hybridization studies were performed for low- and high-risk HPV sub-types. Gender- and site-matched controls of conventional moderate-to-severe oral epithelial dysplasia were similarly evaluated using immunoperoxidase studies for p16 and in situ hybridization; the number of apoptotic cells for study and control cases was counted at two different tissue sites. There were 17 men and 3 women with a median age of 56 years. Seventeen lesions were described as white and five were described as rough or papillary. Thirteen were located on the lateral or ventral tongue, some extending onto the floor of the mouth. Epithelial hyperplasia with marked karyorrhexis and apoptosis were present in all the cases, along with features of conventional oral epithelial dysplasia. A statistically significant number of apoptotic cells were identified in the study cases when compared with controls (P>0.0001). Twenty cases were positive for high-risk HPV by in situ hybridization and all 19 nineteen cases evaluated for p16 demonstrated overexpression. Two patients were diagnosed with squamous cell carcinomas and one patient developed recurrent disease. We report a subset of oral epithelial dysplasia that occurs mostly in adult men on the ventral or lateral tongue and is positive for high-risk HPV and for p16. We propose use of the term ‘HPV-associated Oral Intraepithelial Neoplasia’ to characterize these lesions of the oral cavity for consistency in nomenclature with HPV-associated lesions of the lower anogenital tract. One case recurred and one developed invasive cancer.

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Alessandro Villa

Brigham and Women's Hospital

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