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Safety of Oral Bisphosphonates:
Controlled Studies on Alveolar Bone
Purpose: Osteoporosis and osteopenia are characterized by reductions in bone mass and may lead toskeletal fragility and fracture. The latest generation of oral bisphosphonate drugs, including alen-dronate and risendronate, has been approved for the prevention and treatment of osteoporosis. Thesemedications are chemically absorbed into bone, decreasing osteoclast number and activity andthereby decreasing bone resorption. The purpose of this report is to present safety data from 2 con-trolled studies in patients receiving oral bisphosphonates. Materials and Methods: Study 1 tested theeffect of alendronate, an inhibitor of bone resorption, on alveolar bone. A total of 335 patients (162men and 173 women, aged 30 to 79 years) with moderate or severe periodontal disease were ran-domized to either placebo or 70 mg alendronate once weekly. Alveolar bone height and safety wereassessed over a 2-year period. Study 2 was a longitudinal single-blind controlled design comparingimplant success in 50 consecutive patients (210 implants), 25 patients who received bisphosphonatetherapy and 25 age-matched control subjects. Implant success and safety, including incidence ofosteonecrosis of the jaws (ONJ), was blindly assessed for at least 3 years. Results: In study 1, nocases of ONJ were observed in either treatment group. Furthermore, a trend toward lower incidencesof infection and tooth loss was observed in the alendronate group. In study 2, no cases of ONJ wereobserved in either group, and implant success was greater than 99% in both groups. Conclusion: Onthe basis of 2 controlled clinical studies, oral bisphosphonate usage was not associated with occur-rence of ONJ. (Controlled Clinical Study) INT J ORAL MAXILLOFAC IMPLANTS 2006;21:349–353 Key words: alveolar bone, bisphosphonates, clinical trials, implants, periodontal disease, treatment Osteoporosis and osteopenia are characterized by menopause, thin or small body frame, race, and reductions in bone mass and may lead to skele- heredity. Lack of calcium intake, lack of exercise, tal fragility and fracture. In 1994 the World Health smoking, and alcohol are modifiable risk factors. Low Organization defined osteoporosis as a bone mineral bone mass, certain medications, and systemic dis- density (BMD) level more than 2.5 standard devia- eases such as hyperparathyroidism are modifiable to tions below the mean of normal young women.1 some extent. Many of the risk factors for osteoporo- Risk factors for osteoporosis can be categorized as sis are similar to risk factors for dental implant nonmodifiable or modifiable.1,2 The nonmodifiable risk factors for osteoporosis include sex, age, early Bone loss in women occurs most rapidly in the years immediately following menopause, when nat-ural levels of estrogen are greatly reduced. In mostwomen, bone mass reaches its peak in the thirddecade of life (around 25 to 35 years of age) and 1Morton Amsterdam Dean and Professor, University of Pennsylva- declines thereafter. This decline in bone mass accel- nia School of Dental Medicine, Philadelphia, Pennsylvania.
erates with the onset of menopause.3,4 While esti-mates of the rate of postmenopausal bone loss may Correspondence to: Dr Marjorie K. Jeffcoat, University of Penn- differ by population and measurement technology, a sylvania School of Dental Medicine, 240 S. 40th Street, Philadel-phia, PA 19104. Fax: +215 573 4075. E-mail: rate of about 0.5% to 1.0% per year has been The International Journal of Oral & Maxillofacial Implants COPYRIGHT 2005 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Osteoporosis is not a substantial health risk, but coded for blind assessment of alveolar evidence, and treatment of osteoporosis is important to the health presence of ONJ and radiolucency. Thus, assessment of patients. Nearly 50% of women develop osteo- of the radiographs was completed by a single inves- porosis. Furthermore, almost 24% of women who suf- tigator with no knowledge of the treatment group fer a hip fracture die within a year due to sequellae of or the patient’s clinical adherence to the study regi- the fracture. Therefore, prevention and treatment of men. Other tooth-related safety data, such as caries osteoporosis is an important part of the chemothera- and gingival index (GI) data, have been reported peutic regimen for patients who may be candidates elsewhere.16 No adverse pattern of events was for dental implants. Recent case repor ts have included observations of osteonecrosis of the jaws The primary efficacy endpoint was the change in (ONJ) in patients receiving bisphosphonates.5–12 ABH. ABH is defined as the distance between the However, in the vast majority of these cases, bisphos- cementoenamel junction (CEJ) and the alveolar bone phonate drugs were administered intravenously crest. In normal conditions, the level of the crest is 1 rather than taken orally for the prevention and treat- Statistical Evaluation. Safety data was tabulated The purpose of this report is to present safety data but not amenable to statistical analysis due to the from 2 controlled studies of oral bisphosphonates.
low level of adverse events in both the placebo andalendronate groups.
Changes in ABH from baseline were analyzed by the analysis-of-variance method (ANOVA), includingtreatment group and study center as factors. Treat- ment-by-center interaction was not found to be sig- The first study was a double-blind placebo-con- nificant at the .05 level. Analyses were performed on trolled study of the safety of oral alendronate taken per-patient summaries of the measurements at qual- on a once-weekly basis. The study was designed to ified tooth sites for each individual patient.
explore the effects of alendronate, a potent inhibitorof bone resorption, on alveolar bone loss in patients with moderate or severe periodontal disease.13 The Baseline Characteristics. A total of 162 men and 173 rationale for the study was based on the fact that women were enrolled in the study. The patients periodontal bone loss is mediated by osteoclasts, ranged in age from 30 to 79 years (mean, 50 years).
whose function is selectively inhibited by alen- Approximately 75% of the patients enrolled were dronate.6 Alendronate had previously been shown to Caucasian, while 17% were African Americans. Sixty- decrease periodontal bone loss in 2 animal models two percent were smokers, and 71% of the patients of periodontal disease14,15 and to decrease loss of had severe periodontal disease. Only 3% were dia- alveolar bone height and density in a small number betic. There were no differences between groups in of subjects with moderate periodontal disease.9 The Efficacy. Figure 1 shows the ABH at baseline and A total of 335 patients (age range, 30 to 79 years) after 2 years in subjec ts with low and normal with moderate or severe periodontal disease were mandibular BMD. A significant gain in ABH was seen enrolled in the study. Moderate to severe periodontal in the alendronate-treated group (periodontal bone disease was defined by the presence of pocketing, loss 4.16 ± .11 mm baseline, 3.75 ± .18 mm 2 years) loss in clinical attachment, and loss of at least 3 mm relative to the placebo group (periodontal bone loss of alveolar bone height (ABH). A diagnosis of osteo- 4.22 ± .13 mm baseline, 4.61 ± .23 mm 2 years) (P < porosis was not an inclusion criterion for the study.
.001) in patients with low mandibular BMD at base- Patients were randomized at 12 US sites to either 70 line. This significant difference was not observed in mg alendronate or a placebo once weekly; they alendronate-treated patients with normal BMD at received nonsurgical periodontal treatment at the baseline (4.33 ± 0.13 mm baseline, 4.49 ± 0.21 mm 2 time of randomization. Patients were examined at 2 years) compared with placebo-treated subjects (4.32 clinic visits (screening and baseline) prior to random- ± 0.11 mm baseline, 4.31 ± 0.18 mm 2 years).
ization and once every 3 months thereafter for 2 Safety. Table 1 shows the alveolar bone and perio- years. Maintenance treatment was performed every dontal safety profile. No cases of ONJ were observed over the 2-year study period. In fact, fewer teeth were The primary safety endpoint, or measure of safety, lost in the bisphosphonate group, in spite of the was ONJ. Infection and progressive alveolar bone existence of periodontal disease at baseline, than in loss were also considered. All radiographs were COPYRIGHT 2005 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
*Number of teeth lost shown rather than number of patients who lost Effect of alendronate on alveolar bone. Bone loss from the CEJ (mean ± SD) is shown for patients with low BMD at base-line versus those with normal BMD at baseline. Note a significantdecrease in bone loss16 in the alendronate-treated group in sub-jects with low BMD at baseline. Results Analysis revealed that 100.0% of the implants placed The second study was a parallel-arm controlled study in patients receiving bisphosphonates were success- of dental implant patients receiving oral bisphospho- ful, compared with 99.2% in the group not receiving nates versus control dental implant patients.
bisphosphonates (Fig 2). There was no significant dif-ference between the 2 study groups (P > .95).
Materials and MethodsDesign. This single-blind controlled study involved theconsecutive analysis of 3-year results from 25 patients (102 implants) receiving oral bisphosphonates (alen-dronate or risendronate) versus 25 age-matched A number of cases of ONJ following treatment with patients (108 implants) who did not receive bisphos- high-dose bisphosphonates, especially in cancer phonates. All patients were postmenopausal women patients treated parenterally and in the presence of with BMD scores indicative of osteoporosis. Only 1 additional risk factors such as chemotherapy, gluco- patient per study arm smoked. Patients in the bisphos- cor ticoids, and poor oral hygiene, have been phonate arm had taken the drug for 1 to 4 years (mean reported to regulatory agencies.5–12 Patients receiv- 3 ± 0.1 years) prior to inclusion in the study.
ing intravenous bisphosphonate therapy were not Following implant placement, patients were fol- studied as part of the present study. This smaller lowed for at least 3 years with oral examinations, population with especially complex medical prob- radiographs, and routine maintenance. Two-stage lems is deserving of controlled studies.
osseointegrated implants were used in all patients.
The present study is, thus far, the largest random- Fixed screw-retained prostheses were placed and ized, placebo-controlled study of an antiresorptive removed to assess implant mobility, which was agent in patients with oral disease that was designed to assess oral side effects and outcomes in a blinded Outcomes. Coded digital radiographs were used controlled manner. After 2 years of treatment, a sig- to provide yearly measurements of bone loss and nificant positive effect of alendronate was observed were examined for evidence of ONJ. Calibrated clini- relative to placebo in the subgroup of patients with cians also measured mobility and assessed clinical evidence of pain, infection, and ONJ.
Other investigators have reported positive results Statistical Analysis. A Kaplan-Meier analysis was with alendronate therapy, primarily on ABH and alveolar used to compare the success rate of implants in bone density, with daily doses equivalent to the weekly patients receiving oral bisphosphonates to implants dose used in the current study.16–22 However, the dura- in patients not receiving oral bisphosphonates. Suc- tion of follow-up in these studies was only 6 months.
cess was defined as less than 2 mm of alveolar bone Study 1 also provided additional data on the loss over the 3-year study period, lack of mobility, safety of once-weekly alendronate. As previously lack of infection, and absence of pain and ONJ.
be missing a greater number of teeth than post-menopausal women with normal BMD.23 Therefore, given the large number of women routinely takingoral bisphosphonates and the relatively few cases ofosteonecrosis seen in the present sample, it appearsthat the small risk of developing osteonecrosis should be considered with due regard for the poten- tial benefits (retardation of alveolar bone loss).
The decision to proceed with any medical or dental Implant success in bisphosphonate-treated and control procedure, be it prescription of oral bisphosphonates patients. One hundred percent of implants in patients receivingoral bisphosphonate met the success criteria, and 99.2% of or placement of a dental implant, involves balancing implants in patients not receiving the drug were successful.
the risks against the benefits and making choices.
Osteoporosis is a serious bone disease requiringtreatment in the absence of major risks. In the 2 con-trolled studies presented, oral bisphosphonates werenot found to pose a risk to alveolar bone comparedto placebo.
70 mg oral alendronate once weekly was generallysafe and well tolerated. This favorable safety profile included maxillar y gingival index and dental adverse experiences. This study supports prior The authors thank Proctor and Gamble Pharmaceutical for par- research17–19,21,22 and shows both reduced rates of tially funding study 2 by providing a Grant in Aid for data analysis.
The authors also thank Merck Research for access to a multicen- bone loss and reduced bone loss with absence of ONJ in a multicenter study population. However, it isacknowledged that, given the relatively long half-lifeof bisphosphonates, the long-term effects of alen- dronate therapy cannot be determined from the 2- to3-year follow-up presented here.
1. Bone Health and Osteoporosis: A Report of the Surgeon Gen- In study 2, oral bisphosphonate therapy was not eral. Rockville, MD: Dept of Health and Human Services, 2004.
associated with any implant failures or adverse 2. Jeffcoat MK. Osteoporosis and oral bone loss: Current litera- events. The patients were followed for at least 3 3. Arneson TJ, Melton LJ III, Lewallen DG, O’Fallon WM. Epidemi- years, and no implant had evidence of aloveolar ology of diaphyseal and distal femoral fractures in Rochester, bone loss exceeding 2 mm around the implant. No Minnesota, 1965-1984. Clin Orthop 1988:234:188–194.
4. Cooper C, Melton LJ III. Magnitude and impact of osteoporosis The implications of this data are profound, since and fractures. In: Marcus R, Feldman D, Kelsey J (eds). Osteo- they directly address an area of considerable debate porosis. San Diego, CA: Academic Press, 1996:419–434.
5. Durie BG, Katz M, Crowley J. Osteonecrosis of the jaw and bis- in the medical and scientific communities. Although phosphonates. N Engl J Med 2005;353:99–102.
a large majority of bisphosphonate-associated cases 6. Ruggiero SL, Mehrotra B. Ten years of alendronate treatment of ONJ have concerned patients receiving intra- for osteoporosis in postmenopausal women. N Engl J Med venous bisphosphonate therapy, some instances of ONJ in patients on oral therapy have been reported 7. Ruggiero SL, Mehrotra B, Rosenberg TJ, Engroff SL. Osteo- necrosis of the jaws associated with the use of bisphospho- nates: A review of 63 cases. J Oral Maxillofac Surg 2003;61: The findings of the present study suggest that there is benefit to oral bisphosphonate therapy in 8. Schwartz HC. Osteonecrosis and bisphosphonates: Correlation that it protects individuals against periodontal bone versus causation. J Oral Maxillofac Surg 2004;62:763–764.
loss and osteoporosis. This correlates well with previ- 9. Viale PH, Lin A. Exposed bone in oral cavities. Clin J Oncol Nurs ous studies suggesting that osteoporotic individuals 10. Badros A, Weikel D, Salama A, et al. Osteonecrosis of the jaw in are at higher risk for alveolar bone loss and that post- multiple myeloma patients: Clinical features and risk factors. J menopausal women with osteoporosis are likely to COPYRIGHT 2005 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
11. Farrugia MC, Summerlin DJ, Krowiak E, et al. Osteonecrosis of 18. El-Shinnawi UM, El-Tantawy SI. The effect of alendronate the mandible or maxilla associated with the use of new gen- sodium on alveolar bone loss in periodontitis. J Int Acad Peri- eration bisphosphonates. Laryngoscope 2006;116:15–20.
12. Markiewicz MR, Margarone JE III, Campbell JH, Aguirre A. Bis- 19. Lane N, Armitage GC, Loomer P, et al. Bisphosphonate therapy phosphonate-associated osteonecrosis of the jaws: A review improves the outcome of conventional periodontal treat- of current knowledge. J Am Dent Assoc 2005;136:1669–1674.
ment: Results of a 12-month, randomized, placebo-controlled 13. Harada S-I, Rodan GA. Control of osteoblast function and con- study. J Periodontol 2005;76:1113–1122.
trol of bone mass. Nature 2003;423:349–355.
20. Rizzoli R, Greenspan SL, Bone G III, et al. Alendronate once- 14. Brunsvold MA, Chaves ES, Kornman KS, Aufdemorte TB, Wood weekly study group.Two-year results of once-weekly adminis- RJ. Effects of a bisphosphonate on experimental periodontitis tration of alendronate 70 mg for the treatment of postmeno- in monkeys. Periodontol 1992;63:825–830.
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15. Cumming SR, Black DM, Thompson DE. Randomized trials of 21. Rocha M, Nava LE, Vazquez de la Torre C, et al. Clinical and the effect of alendronate on the risk of fractures in women radiological improvement of periodontal disease in patients with low bone density but without vertebral fractures: Results with type 2 diabetes mellitus treated with alendronate: A ran- from the fracture intervention trial. JAMA domized, placebo-controlled trial. J Periodontol 16. Jeffcoat MK, Cizza G, Shi WJ, Lombardi A. Efficacy of bisphos- 22. Rocha ML, Malacara JM, Sánchez-Marin FJ, Vazquez de la Torre phonates for the control of alveolar bone loss in periodontitis CJ, Fajardo ME. Effect of alendronate on periodontal disease in postmenopausal women: A randomized placebo-controlled 17. Jeffcoat MK, Reddy MS. Alveolar bone loss and osteoporosis: trial. J Periodontol 2004;75:1579–1585.
Evidence for a common mode of therapy using the bisphos- 23. Yemm R. Analysis of patients referred over a period of five phonate alendronate. In: Davidovitch Z (ed). The biologic years to a teaching hospital consultant service in dental pros- Mechanism of Tooth Resorption and Replacement by thetics. Br Dent J 1985;159:304–306.
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