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J Am Dent Assoc, Vol 139, No 5, 545-552.
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COVER STORY

JADA Continuing Education

Osteoporosis and Its Implications for Dental Patients

Beatrice J. Edwards, MD and Cesar A. Migliorati, DDS, MS, PhD


   ABSTRACT
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 ABSTRACT
EPIDEMIOLOGY
 PREVENTION
 DIAGNOSIS
 THERAPY OPTIONS
 DENTAL IMPLICATIONS OF...
 CONCLUSION
 REFERENCES
 
Background. Osteoporosis is a common disease in middle-aged and older Americans. The risk of sustaining fractures is a concern, and mortality rates after hip or vertebral fractures are high. Oral health maintenance for adults with osteoporosis is important.

Types of Studies Reviewed. The authors conducted a MEDLINE search of the medical and dental literature with the objective of reviewing osteoporosis, its effect on public health in the population in the United States and the implications in providing dental care for these patients. They selected studies by performing a content search with National Library of Medicine medical subject headings (epidemiology, public health impact, treatment, adverse drug reactions, cost-effectiveness of osteoporosis therapy, oral health, periodontal disease, adverse drug reactions, bisphosphonates and osteonecrosis of the jaw). They then performed a study design search with a filter so that only randomized clinical trials were included.

Results. Osteoporosis and related fractures are more common than coronary disease, stroke and breast cancer. Fractures resulting from osteoporosis can affect a patient’s quality of life severely, and fractures result in functional impairment and increased health care cost and mortality. Medical management of osteoporosis includes diet control, with appropriate intake of calcium and vitamin D, weight-bearing exercise, discontinuation of tobacco and alcohol intake, and use of medications, including selective estrogen receptor modulators, calcitonin, anabolic agents and bisphosphonates. Bisphosphonates have been associated with the development of osteonecrosis of the jaws.

Clinical Implications. Oral health maintenance is important in patients with osteoporosis. Bisphosphonate therapy or other medical treatment for these people should be discontinued only after consultation with the patient’s physician.

Key Words: Aging; bisphosphonate-associated osteonecrosis; bone loss; decision making; dental care for chronically ill patients; dental care for elderly patients; drug therapy

Abbreviations: BMD: Bone mineral density. • BON: Bisphosphonate-associated osteonecrosis. • CTX: Serum C-telopeptide test of type I collagen. • DXA: Dual energy x-ray absorptiometry. • IV: Intravenous route. • PO: Oral route. • SC: Subcutaneous injection. • WHO: World Health Organization.

Osteoporosis is an increasingly prevalent condition in middle-aged and older Americans. It typically goes unnoticed until fractures occur. Osteoporotic fractures are common and place a medical and personal burden on older adults and a significant economic toll on the nation. Despite therapy, the risk of fractures is considerable, and the mortality after hip or vertebral fractures is high. Oral health maintenance for people with osteoporosis is important.

We conducted a MEDLINE search of the medical and dental literature with the objective of reviewing osteoporosis, its effect on public health in the population in the United States and the implications in providing dental care for these patients. We selected studies by performing a content search with National Library of Medicine medical subject headings (epidemiology, public health impact, treatment, adverse drug reactions, cost-effectiveness of osteoporosis therapy, oral health, periodontal disease, adverse drug reactions, bisphosphonates and osteonecrosis of the jaw). We then performed a study design search with a filter so that we included only randomized clinical trials. We were involved in screening titles and results of the search. In the case of conflict, the senior author (B.J.E.) made the final selection.

As an example of the real-life burden of osteoporosis, consider the case of a 73-year-old woman who experienced her first fracture at age 55 years and had had six additional fractures since that time. Each fracture caused tremendous pain and required long hospital stays.1 Unfortunately, she did not tolerate osteoporosis medications well, and her primary treatment consisted of taking estrogen, calcium and vitamin D. The fear of additional fractures had the largest effect on her life, and she limited the time she spent with her grandchildren, as well as the types of activities she enjoyed with them. She found it impossible to lie down on her back or right side and difficult to get into and out of bed or a chair. She had to give up dancing and felt that she had become a drag on family members who had to slow down to accommodate her limitations.


   EPIDEMIOLOGY
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 EPIDEMIOLOGY
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 CONCLUSION
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Osteoporosis is a common, yet asymptomatic, disease that is characterized by bone loss leading to skeletal fragility. Osteoporosis is the most important underlying cause of fractures in middle-aged and older adults.2

In 2004, the U.S. surgeon general issued the first report on Bone Health and Osteoporosis.1 Ten million Americans older than 50 years have osteoporosis, and an additional 34 million have osteopenia, which puts them at risk of developing osteoporosis.3 The bone health status of Americans will deteriorate primarily because the U.S. population is aging. The prevalence of osteoporosis and osteoporosis-related fractures will increase in the near future. By 2010, roughly 12 million people older than 50 years are expected to have osteoporosis, and 40 million people older than 50 years are expected to have osteopenia.4,5 By 2020, 14 million people are expected to have osteoporosis, and 47 million are expected to have osteopenia. The number of hip fractures in the United States is expected to double or triple by 2040.

Fractures are common and costly, and they can become a chronic burden on people and society. An estimated 1.5 million people have a bone disease–related fracture each year.6,7 In the United States, four of every 10 white women aged 50 or older will experience a hip, spine (vertebral) or wrist fracture; 13 percent of white men will face a similar fate.8 The risk of sustaining a fracture increases exponentially after menopause. Wrist fractures occur in relatively independent women during the sixth decade of life, vertebral fractures beyond the seventh decade of life and hip fractures past the eighth decade of life. In men, osteoporotic fractures occur at a more advanced age, mostly past the seventh decade of life.8–11 Although the lifetime risk of sustaining a fracture for men and for nonwhite women is decreasing, it is increasing in certain populations such as Hispanic women.12 The incidence of osteoporosis-related fractures in all women is higher than the combined incidence of myocardial infarction, stroke and breast cancer.13

Functional consequences of fractures. Sustaining a fracture can have significant consequences for people and their family members. Fractures result in functional impairment; they affect people’s ability to care for themselves. Functional decline after a fracture has been documented for all osteoporotic fractures (that is, wrist, spine and hip).14,15 Vertebral fractures cause back pain and lead to height loss, rib cage deformity, and a reduction in strength and trunk motion.16–18 Vertebral fractures contribute to pulmonary disorders such as pneumonia in older adults.19 Two-thirds of patients with hip fractures do not return to the level of function they had before the fracture, only 40 to 79 percent of patients regain their previous ambulatory function a year after the hip fracture,20 and less than one-half return to their prefracture status with respect to the activities of daily living.21 People who have experienced hip fractures are as likely to have impaired ambulation and other functional deficits as are people who have had a stroke.22 Hip fractures cause an extra 10 percent of women to become functionally dependent (that is, 10 percent more women become dependent than would have if they had not sustained a fracture), and 19 percent of women who have hip fractures require long-term nursing home care,7 a situation that a majority of participants in one study considered worse than death.23

Mortality attributed to fractures. Hip fractures are associated with a 2.8 to 4.0 times higher risk of mortality during the first six months after the fracture. People with poor health or living in a nursing home are particularly vulnerable to adverse outcomes.24,25 Spine fractures also result in an increase in mortality (20 percent), since they can affect the rib cage and impair the pulmonary system; deaths usually occur after numerous episodes of pneumonia.26,27

Health care expenditures resulting from osteoporosis treatment. Osteoporosis treatment results in 2.4 million office visits, 500,000 hospitalizations and 200,000 admissions to long-term care institutions annually. The direct care expenditures for osteoporotic fractures range from $12.2 to $17.9 billion each year (in 2002 dollars).28 As the U.S. population is aging, these costs may triple by 2020.1 Adding the direct costs of caring for other bone diseases, as well as the indirect costs (for example, lost productivity for patients and family members), likely would add billions of additional dollars to the total cost of osteoporosis-related health care expenditures.


   PREVENTION
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 CONCLUSION
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Genetic factors determine 50 to 90 percent of a person’s bone mass and other qualitative aspects of their bones.29 Bone tissue continues to renew or remodel itself throughout life by breaking down old bone (bone resorption) and replacing it with new bone (bone formation). Adolescence is a critical period for bone health, as the amount of bone mineral gained during this period typically equals the amount lost throughout the remainder of adult life.30 Failure to achieve a peak bone mass at the end of adolescence and young adulthood leaves a person with less reserves with which to withstand the normal losses during later life.31 Males have higher peak bone mass than do females. Subsequently, a loss of 0.6 percent bone mass annually results in progressive bone loss in both sexes, which is accentuated in women by menopause.32

Most Americans do not consume recommended levels of calcium; therefore, supplementation with calcium and vitamin D usually is advocated.1 Supplementation methods such as calcium and vitamin D therapy modulate age-related increases in parathyroid hormone levels and bone resorption. Receiving adequate amounts of calcium throughout their lives is necessary for people to achieve peak bone mass and maintain bone mass. Weight-bearing exercise also is necessary for peak bone mass acquisition and maintenance. Complete bed rest and microgravity (as seen in space travel)33 have adverse effects on bone mass. High-impact and resistance exercises, particularly in girls before menarche, stimulate accrual of bone mineral content in the skeleton.34 Tobacco and excessive alcohol intake should be avoided to preserve skeletal health.35

Bone formation predominates in childhood and adolescence, resulting in skeletal growth. Bone formation and resorption generally are in balance with each other during the early to middle adult years. Thereafter, bone loss may progress slowly in both sexes, with a period of more rapid loss in women around the time they undergo menopause. Age-related bone loss is modest (0.6 percent per year), but because of long life expectancies, both sexes may lose 40 percent of bone over a lifetime.32


   DIAGNOSIS
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Unless a fracture occurs, osteoporosis often is asymptomatic, which is a major challenge and may explain why relatively few patients receive a diagnosis of osteoporosis.1 Bone mineral density (BMD) accounts for more than 75 percent of bone strength. Quantitating osteopenia to predict the risk of experiencing fractures is of the same order of magnitude and usefulness as measuring blood pressure or cholesterol levels to predict the risk of experiencing stroke or myocardial infarction.36 Spine and hip BMD reflect the risk of experiencing vertebral and hip fractures. Dual energy x-ray absorptiometry (DXA) is considered the gold standard method for determining BMD. Peripheral BMD measures include peripheral DXA, calcaneal ultrasonography37,38 and digital x-ray radiogrammetry, and they are used for screening and to predict the short-term risk of experiencing fracture.39,40

The World Health Organization (WHO) defines osteoporosis in postmenopausal women as a BMD with T score more than 2.5 standard deviations below the mean for young healthy adults. A BMD between 1.0 and 2.5 standard deviations below the mean (T score = –1.0 to –2.5) is classified as osteopenia. The risk of fracture is proportional to the decrease in BMD; however, more fractures are seen in people with osteopenia than in people with osteoporosis, as the number of people with osteopenia is higher. Personal risk factors for hip fracture (BoxGo41,42) have been identified from epidemiologic studies such as the Study of Osteoporotic Fractures.41 Treatment for osteoporosis is recommended for people who have experienced a hip or vertebral fracture; for people with a BMD T score equal to or less than –2.5 in the femoral neck, total hip or spine regions as determined by DXA; and for postmenopausal women and men 50 years or older with low bone mass (T score –1.0 to –2.5) in the femoral neck, total hip or spine regions as determined by DXA, as well as a 10-year hip fracture probability of greater than or equal to 3 percent or a 10-year all major osteoporosis–related fracture probability of great than or equal to 20 percent based on the U.S.-adapted WHO absolute fracture risk model.43,44


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  		BOX Major risk factors for osteoporosis and related fractures in white postmenopausal women.*{dagger}

 

   THERAPY OPTIONS
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Medications used to treat osteoporosis include selective estrogen receptor modulators (for example, raloxifene [Evista, Eli Lilly, Indianapolis]), bisphosphonates (for example, alendronate [Fosamax, Merck, Whitehouse Station, N.J.],45 risedronate [Actonel, Procter & Gamble, Cincinnati],46 ibandronate [Boniva, Hoffman-LeRoche, Nutley, N.J.] and zoledronate [Reclast, Novartis, Cambridge, Mass.]),47 calcitonin (for example, Miacalcin, Novartis)48 and the anabolic agent teriparatide (Forteo, Eli Lilly)49 (TableGo). Medication is effective in preventing bone loss and preserving BMD. Medication use for treatment can increase BMD and reduce the risk of experiencing vertebral and nonvertebral fractures. The results of studies in which the safety of taking bisphosphonates after five50,51 and 10 years52 was assessed showed no abnormalities in bone architecture or mineralization.


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  		TABLE U.S. Food and Drug Administration–approved medications for prevention and treatment of osteoporosis.

 
Medication used to treat osteoporosis can reduce the risk of fracture by 35 to 50 percent.45,46,49 Therapy should be monitored by means of BMD testing within 18 to 24 months. Sustained increases in BMD have been shown for as long as 10 years of treatment.52 Treatment with alendronate for five years followed by discontinuation for four years results in relative maintenance of BMD without an increased risk of fractures. However, by five years after discontinuation, there is a decline in BMD and an increase in the risk of clinical vertebral fractures.53,54


   DENTAL IMPLICATIONS OF OSTEOPOROSIS
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Although osteoporosis is the main focus of our article, several other factors also affect the dental management of this disease. Patients who have or are at risk of developing osteoporosis often have other chronic diseases. As a result of taking medications to treat these diseases and of physical disability and compliance issues, these patients’ oral health often is compromised. They often have significant dental needs, and their poor oral health can compromise systemic health. Preserving their natural dentition promotes better nutrition and improves appearance.55,56 On the other hand, poor oral health in this population can contribute to increased morbidity and decreased quality of life.57 People with chronic diseases and poor oral health are at increased risk of developing opportunistic infections such as pneumonia58 and for xerostomia induced by medications.59,60 Patients’ poor oral hygiene, loss of hand dexterity, lack of compliance and poor dentition can impair oral function.61 Therefore, there is an indication that these patients need dental care; to provide adequate care, dentists need to understand osteoporosis, its treatments and its complications.

Bisphosphonate-associated osteonecrosis (BON). BON is an oral complication resulting from undergoing bisphosphonate therapy and is defined as the presence of necrotic bone anywhere in the oral cavity in a patient who is taking a bisphosphonate, who has not received radiation to the head and neck and in whom the necrotic area does not heal within eight weeks after diagnosis after receiving proper care.62 Reports of BON have implications for the dental care of patients with osteoporosis.63–68 Most reported cases of BON have been associated with the intravenous administration of zoledronic acid or pamidronate in patients with cancer that metastasized to the bones.63,66,67 BON also has been diagnosed, although in a smaller number, in patients taking oral bisphosphonates such as alendronate, risedronate, ibandronate and clodronate (not available in the United States) to prevent and treat osteoporosis.63,66–71

It is important to identify patients who are taking a bisphosphonate through careful review of their medical histories. Because most bisphosphonates are taken either weekly or monthly, patients frequently forget to disclose to dentists that they are taking the medication. Asking patients specific questions about osteoporosis and the use of a bisphosphonate may facilitate the identification of those who are using this therapy. Predisposing factors associated with the development of BON include the presence of periodontal disease, smoking, diabetes mellitus, glucocorticoid use and prolonged bisphosphonate therapy.62,71,72

The ideal dental management protocol for patients taking oral bisphosphonates has elicited discussion. It has been suggested that patients be given a "drug holiday" when surgical dental intervention that includes bone manipulation is needed.72 The literature, however, provides no scientific evidence to support the idea that discontinuation of bisphosphonate therapy will improve treatment outcomes.73 Therefore, before discontinuing bisphosphonate therapy, dentists and physicians must collaborate to determine the best way to manage the treatment of each patient. A medical consultation would allow for the evaluation of several health indicators, including BMD, degree of risk of experiencing spine and hip fractures, and duration of bisphosphonate therapy. This consultation also would help health care practitioners make a decision about whether a drug holiday is acceptable for a particular patient.

The risk of fracture after the discontinuation of an oral bisphosphonate for a patient with osteoporosis has not been well-established. In a recent study of postmenopausal women in which the effects of continuing or stopping oral alendronate therapy for up to 10 years were evaluated, researchers found that BMD was maintained and bone remodeling was suppressed with no detectable increase in fracture risk.54 In the group of women who discontinued oral alendronate use after five years, the BMD and bone remodeling were maintained at higher levels than those obtained at baseline. Although the radiographic diagnosis of vertebral fractures in those who stopped bisphosphonate therapy after five years did not increase, the clinical diagnosis of vertebral fractures increased significantly.54 This finding indicates the importance of determining which patients are at a higher risk of experiencing fractures before discontinuing alendronate therapy. The association of hip fracture with high mortality also is important.24,25

Managing the care of a patient who has BON and is taking a bisphosphonate is based mostly on expert opinion.68,74 Several strategies have been attempted, including sequestrectomy, surgical local débridement and periodontal flap surgery, as well as less invasive procedures like antibiotic therapy and mouthrinses.73 For example, a recent study reported the care of 11 patients with BON who were taking oral bisphosphonates.75 Treatments ranged from less invasive procedures (administration of systemic antibiotics and oral hygiene measures) to local surgical débridement to hospitalization and extensive surgery. Treatment outcomes varied from complete healing to partial healing to no healing. The researchers did not mention whether therapy was discontinued. Dentists must keep in mind that the management of BON is difficult. The osteonecrotic process does not respond to routine therapy, and more aggressive surgical manipulation of the area is not recommended.74,75 Conservative approaches such as minor local débridement and systemic antibiotic therapy are indicated when there is clinical evidence of active infection. Sharp bone edges should be eliminated when there is trauma to the soft tissues. Routine oral hygiene maintenance is indicated, and it can be complemented with topical chlorhexidine.74

When a patient taking oral bisphosphonate needs to undergo a surgical procedure, some experts suggest that the patient take a drug holiday and undergo a serum C-telopeptide test of type I collagen (CTX) before the procedure.72 CTX is used to measure bone resorption and detect the fragments of collagen type I peptide released in the circulatory system when osteoclasts resorb bone. It has been suggested that when the CTX level is higher than 150 picograms per milliliter, the risk of BON developing after an invasive surgical procedure is small.72 There are, however, no scientific data to support the use of CTX to predict the development of BON. Before using this test, dentists should keep in mind that the results indicate the status of bone resorption of the entire skeleton and not of only the jawbones. Although the use of laboratory testing to monitor the effect of bisphosphonates on suppression of bone remodeling might prove useful in the future, more scientific research is needed before it can be used to support dental treatment decisions. Because BON can be a devastating complication of bisphosphonate therapy, a collaborative effort between dentists and physicians in deciding on the patient’s dental treatment is recommended, because it can minimize complications and adverse events.68,74

The reported incidence of BON in patients taking oral bisphosphonates is relatively low, which may be due to underreporting, different duration of therapy in countries that have adopted bisphosphonates more recently and different definitions of BON.62 There are an estimated 0.7 cases per 100,000 patient-treatment years in the United States.62,69,74 However, some geographic variations in incidence are being reported such as in Australia, where the number of cases could be much higher.71 Others believe that the incidence of BON is low, considering the millions of patients with osteoporosis who are taking oral bisphosphonates.73 The development of new bisphosphonates may enhance the safety of this medication. A recent clinical trial reported the results of treating patients with osteoporosis with a new formulation of bisphosphonate.47 Patients received an annual intravenous infusion of 5 milligrams of zoledronic acid for as long as three years. The results demonstrated a significant reduction of the risk of vertebral, hip and other fractures. Only two cases of BON were detected; one was in the treatment group, and one was in the placebo group. It is not uncommon, however, that drug adverse events emerge only after the drug receives U.S. Food and Drug Administration approval and is in widespread clinical use.

Oral bone health and osteoporosis. Two review articles about osteoporosis and periodontal disease discussed a number of issues regarding general BMD and oral alveolar bone loss, early loss of teeth and increased severity of periodontal disease in patients with osteoporosis.76,77 Risk factors for osteoporosis such as smoking, old age, and low intake of calcium and vitamin D also are common in patients with advanced periodontal disease. Conducting clinical and radiographic dental examinations, as well as recognizing common risk factors for both osteoporosis and periodontal disease, can help dentists identify patients who are at risk of developing osteoporosis. The results of an assessment of an alveolar trabecular pattern can be a clinical indicator of BMD.78 The results of other studies suggest that routine panoramic radiographs also can be used to detect low BMD, osteoporosis and risk of experiencing vertebral fracture in postmenopausal women.79–81 The results also showed that providing special training to general practitioners in how to use specific evaluation techniques to read the panoramic radiographs enhanced their detection of significant radiographic changes. In short, the mandibular inferior cortex can show changes that vary from normal when the endosteal cortical margins are even and sharp on both sides, to mild or moderate erosion of the inferior cortex, to severe erosion and presence of heavy endosteal cortical residues and porosity of the inferior mandibular cortex.81 The authors of two of the studies concluded that this procedure can help detect a high percentage of postmenopausal women with undetected low BMD, as well as undetected spinal fractures.80,81

Physicians and dentists have a mutual interest in identifying patients at risk of developing osteoporosis and periodontal disease. Collaboration between these professionals in the prevention and early diagnosis of osteoporosis, low BMD and fractures can lead to early osteoporosis therapy. In the future, it will be important to recognize if patients with osteopenia and osteoporosis who are receiving medical treatment respond better to treatment and control of bone diseases in the head and neck.


   CONCLUSION
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 ABSTRACT
 EPIDEMIOLOGY
 PREVENTION
 DIAGNOSIS
 THERAPY OPTIONS
 DENTAL IMPLICATIONS OF...
 CONCLUSION
REFERENCES
 
The prevalence of osteoporosis in the general population is increasing rapidly, and fractures associated with this disease can have devastating consequences for the patients. Therefore, diagnosis of osteoporosis in its early stages is important. It is recommended that physicians and dentists collaborate to improve early detection of patients at risk of experiencing or who have osteoporosis. All health care professionals involved in the care of all dental patients, particularly patients who are taking oral bisphosphonates, should discuss patient care decisions.


   FOOTNOTES
 

Dr. Edwards is an associate professor of medicine, Feinberg School of Medicine, Northwestern University, 645 North Saint Clair, Suite 630, Chicago, Ill. 60611, e-mail "BJE168{at}northwestern.edu". Address reprint requests to Dr. Edwards.


Dr. Migliorati is a professor, Oral Medicine, Nova Southeastern University, College of Dental Medicine, Fort Lauderdale, Fla.


Disclosures. Dr. Edwards has received research grants from Merck, Whitehouse Station, N.J., and Procter & Gamble, Cincinnati, in 2001 and 2003, respectively. She also is a consultant for Eli Lilly, Indianapolis; Roche, Basel, Switzerland; and GlaxoSmithKline, Philadelphia. Dr. Migliorati has been a consultant for Colgate-Palmolive, New York City, and is a member of an adjudication committee for Amgen, Thousand Oaks, Calif.


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