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ACADEMICS AND EDUCATION Osteoporosis and Osseointegration of Implants J. Cystal Baxter, DMD, MDS, * and LaDeanne Fattme, DDS, MS*

According to medical literature, osteoporosis and related bone pathologies are increasing in epidemic proportions. The exact etiology of the disease is unknown, but hormonal, dietary, and genetic factors all contribute to the related loss of bone density. In the disease process, bone loss occurs throughout the body. Research indicates that the mandible and maxilla are affected, and show oral manifestations. There is no scientific data to contraindicate the use of two-step osseointegrated implants in osteoporotic individuals. The purpose of this article is to review the literature regarding osteoporosis and its relationship to oral bone loss.

J Prosthod 2: 120- 125. Copyright 0 1993 by the American College of Prosthodontists.

INDEX WORDS: osteoporosis, implants, osseointegration, bone, resorption

FALTHY BONE WITH normal regenerative H capacity is imperative for success in all phases of dentistry. Bone is dynamic, and can be affected by local or systemic conditions.' Normal bone metabolism is especially crucial for success in implant treatment, as aberrations in bone physiolqgy are likely to compromise the prognosis for optimal integration. Osteoporosis is a systemic condition with the potential for affecting implant treatment. The disease is particularly alarming because of its high incidence in the expanding older population, which contains the greatest number of candidates for implant therapy.

Osteoporosis occurs in approximately one third of women over 60 years of age: more than one fourth have bone fractures caused by the disease by the age of 60, and nearly one half have bone fractures by the age of 75.* It is responsible for vertebral and hip fractures, and for stress fractures in any affected part of the body. The annual cost to the IJS health care system is at least $10 billion.? Seventeen percent of patients with hip fractures will dip from related causes within 6 months, making conditions related to this disease the twelfth leading cause of death in the adult Caucasian patient.4 The disease appears to be increasing epidemically in recent years. Many orthopedic researchers fear that it may become one of the

From i'tbrthiixstem Lhi?~m,ri&, Chicago, IL. *Asohate Projssor. Pmthodontics. nddre.fr reprint requectr tn J. Cv.rtal Baxter. DMD, MDS, 845 N

Michigan Aue, No. 948W, Chicago, IL 60611. Copyright 0 1993 bl. the American College ofPosthodontists 1059-94IXI 931 0202-O008&i'.OO/ 0

most common problems in the health of the middle- aged or older person in the f ~ t u r c . ~

Osteoporosis is the loss ofbone density that occurs when more calcium is resorbed from the bone than is replaced. Bone constantly undergoes apposition and resorption. In a healthy individiial, bone apposition would be equal to bone resorption, and bone density w~ould remain adequate. In the osteoporotic individ- ual, more bone is lost than replaced, resulting in porous bone with a swiss-cheese or moth-eaten consis- tcncy.6

Two categories of osteoporosis have been identified: primary and secondary. Primary osteoporosis is by far the most common form of the condition and includes postmenopausal osteoporosis (type I), age- related osteoporosis (type 11), and idiopathic osteoporosis. Secondary osteoporosis is caused by an identifi- able agent or disease process, and therefore can be considered a side effect of another condition or medication.'

Type I primary or postmenopausal osteoporosis characteristically affects women within 10 to 15 years after menopause. Vertebral fractures and fracture of the distal radius are the main clinical manifestations. In patients with this type of osteoporosis, the rate of trabeciilar bone loss is usually 2 to 3 times normal, although the rate of cortical bone loss is only slightly above normal. During this accelerated phase of bone loss, trabecular plate perforation with loss of struc- tural trabeculae weakens the vertebrae and predis- poses them to collapse.

Type I osteoporosis seems to be caused by factors closely related to, or exacerbated by, menopause, and therefore is a disease that affecls only women. The

120 Journal OJProsthodontics, Vol2, No 2 (Jum), 1993:pp 120-125

J i m 1993, Volume 2, iVumber 2 121

result is accelerated bone loss, aberrations of the parathyroid hormone (m), and other bone regen- erating functions.*

In type 11 primary or aging-associated osteoporosis a proportionate loss of both cortical and trabecular bone is seen. This process affects both men and women at about the same rate.

In 10% ofwomen and 40% of men presenting with spontaneous vertebral fractures, a secondary cause of osteoporosis can be identified. The most common causes are early surgical hysterectomy in women, hypogonadism in men, or a glucocorticoid state associated with thyroid therapy in persons of either sex.

A major contributing factor to all types of osteoporosis is a deficiency of dietary calcium. Approxi- mately 99% of the total body weight of calcium is stored in the bones of the skeleton. The remaining 1%, found in the cells and interstitial fluid, is vital for nerve signal transmission and blood clotting.

The calcium levels in and around the cells are strictly controlled by parathyroid hormones. When- ever cellular levels decrease, calcium is needed in- stantly. If calcium is not available from the diet in adequate amounts, it is immediately mobilized from the bones to replenish the cellular supply. If this occurs over an extended period of time, loss of bone density will result.y

Whole-body calcium is normally obtained through dietary sources, but it is lost by the body through several mechanisms. One to two hundred mjlligrams a day is lost through normal urine output, and another 125 to 200 mg is lost into the digestive juices. Women lose additional calcium because of sevcral factors: (1) they are more prone to go on reducing diets with a decrease in the amounts of all nutrients ingested, (2) during pregnancy the fetus requires 400 mg calcium per day; during breast-feeding, an additional 300 mg calcium per day is required, ( 3 ) loss of estrogen and changes in hormonal balances at menopause cause accelerated calcium loss. Any loss of calcium results in loss of calcium from the bone, and an osteoporotic state is the net result.10

Numerous studies illustrate that the average American consumes considerably less calcium than the 1200 mg recommended daily allowance, and the nutritional picture of the older American is probably even worse. A preliminary study that compared the diets of older patients before and after the fabrica- tion and placement of complete dentures showed that calcium deficiencies persisted.I2

In a later study, the diets of five different elderly

groups, all with varying dentitions and/or prosthetic replacements, were compared. Regardless of their dental status, these patients had in common a deficiency in calcium intake.13

In addition to calcium, the mineralization of bone requires normal plasma concentrations of phosphate and vitamin D. If any of these factors are deficient, the organic matrix on bone, or osteoid, will not mineralize normally, and osteomalacia or rickets results. An accumulation of osteoid tissue replaces normal bone. As a result of this lack of mineralization, the skeleton becomes soft, and deformity fractures can occur.

Vitamin D deficiencies can result from a poor diet, inadequate sunlight without vitamin D supple- ments, gastrointestinal disorders such as malabsorp- tion syndromes, impaired vitamin D synthesis such as liver or renal disease, and target cell resistance (vitamin D-resistant rickets, type II). l5

The natural form of vitamin D is cholecalciferol, which is designated as vitamin D. Most cholecalciferol forms in the skin as a result of irradiation of 7-dehydrocholestero1 by ultraviolet rays from the sun. Once cholecalciferol enters the circulation, it is concentrated in the liver, where it is hydroxylated to become 25-hydroxycholecalciferol[25 (OH) DJ] . The final metabolic conversion of the vitamin occurs in the kidneys, where 25 (OH) DYi is hydroxylated to form the active hormone I , 25 dihydroxycholecalciferol [1,25(OH),U,]. It is this substance that ex- presses almost all the stimulatory activity of vitamin D.14

In 1981 Gallagher et a1 reported that serum 1,25 dihydroxycholecalciferol was significantly decreased in both a group of osteoporotic patients and a group of normal elderly patients. They found that intestinal absorption of calcium decreased significantly with age and was lower in osteoporotic, patients than in normal patients matched for either age or habitual calcium intakei5

Kribbs in 1992 reported her findings in a prospective study of 85 postmenopausal women who were administered 1,25 dihydroxycholecalciferol (calcitri- 01) or a placebo for a period of 2 years. She found that there was no significant change in bone mass in the mandibles of patients who received calcitriol versus a placebo and that the drug was not effective in preventing mandibular bone loss.

No study other than Kribbs has evaluated the longitudinal changes in mandibular bone mass in osteoporotic subjects or attempted to increase bone mass in the mandible by pharmacological rneans.l6

122 Osteoporosis and Implants Bmter and Fattore

A number of studies indicate that certain forms of oral bone loss may be related to a generalized osteoporotic state. In 1974 Wical and Swoope attempted to relate dietarycalcium deficiency to resorption in edentulous subjects. These researchers noted a positive correlation between deficient calcium intake and increased mandibular rc~orption. '~

A 1983 study reported on 208 white women, aged 60 to 69 years, who had acquired 218 complete dentures. Each wornan's smoking habits and level of osteoporosis (percent cortical area) were measured at the time she acquired each denture. Of the osteoporotic women who had their natural teeth at age 50,44% had required a complete denture before age 60; in nonosteoporotic women the number was only 15%. The differences in prosthodontic require- ments between these two groups had not existed beforc age 50 but continued after age 60.18 It has also been reported that when skeletal depletion occurs as a result of stimulation by the parathyroid gland, alveolar bone may be affected before the ribs, vertebrae, and long bones."

Henrikson et a1 compared the bone density of long bones with that of edentulous mandibles to determine the relationship of age arid sex to mineral density and volume. This study indicated a statisti- cally significant correlation between mineral density of the mandible and that of the radius. They con- cluded that when osteoporotic changes occur, these changes qualitatively affect the two parts of the skeleton the same way.2o Disruption or trabecular bone in dentate osteoporotic subjects showed a statis- tically significant relationship to a high incidence of vertebral fractures in the study group, while a nonosteoporotic control group illustrated no such paral- lels.20

Alveolar ridge height (or residual ridge height) and metabolic bone loss have been of interest to many researchers. The overwhelming majority of their studies looked at bone resorption in the niandi- blc, and although no definitive conclusions can be made from any of the studies, a number of them2'-2' found a positive relationship between severe alveolar ridge atrophy and metabolic bone loss.

Kribbs et aIz5 in a 1989 study or 85 postmenopausal women with osteoporosis, found that mandibular alveolar ridge height was significantly correlated with both total body calcium and mandibular bone mass. Although the study failed to utilize a compari- son group, the findings are iinportant because they suggest a relationship between osteoporosis and resorption of the edentulous alvcolar ridge.

Von Wowern and WorsaacZG in 1922 reported that in a stnall study of 28 cdentulous wornen, with and without osteoporosis, a significant amount of bone loss occurred in the maxillae of ostevporotic women as cornpared with age-matched, normal wotnen with the same length of edentulousness.

In 1983, Krolner et aI2' reported that increased function in the form of exercise increased the bone mineral content (BMC) in the axial and appendicu- lar skeleton of a group of postmenopausal women, suggesting that exercise may decrease age-related BMC loss in this group.

It is well known to dentistry that bite force decreases after extraction of teeth and placement of conventional dentures. Von Wowern et alL8 in 1979 showed in rat mandibles that after extraction of all teeth, the trabecular bone mass of the mandibles significantly decreased as a result of what Von l4'0ww-n suggests is a decrease in bite force.

Several studies have stated that osseointegrated implants significantly increase bite force in the edentulous patient.'""" Haraldson and Zarb3' in 1987 reportcd the findings or their 1 0-year follow-up study of bite force after treatment with osseointegrated implant bridges arid found that recorded bite force increased significantly when compared with baseline findings 10 years earlier. Their results coincide with earlier studies' findings that bite force increased and muscle activity (EMG) normalized with the duration of the wearing of an osseointegrated implant prosthe-

Adell et a13? reported in 1986 the results of a small radiographic study of patients fitted with prostheses that were fixed to titanium implants. They found that atrophy of alveolar bone between implant fixtures averaged 0.9 mm after lhe first year and 0.05 mm annually for the next 2 years. Perifixtural bone gradually became more radiopaque, especially in the maxilla, indicating a successive, load-relating remodeling.

In 1990 Von Wowern et a1j3 studied changes in BMC of edentulous mandiblcs with osseointegrated lTl implanls (Straumann Co, Cambridge, MA) sup- porting overdetitnres. BMC measurements were made 3 weeks postoperatively and 2 years later at a follow~-up visit. Measurements were made at the implant site, at the premolar region just distal to the implants, at gonion and in the forearm bones. Her results indicated that BMC changes at the implant site and in the area distal to the implants were significantly smaller than the BhlC changes seen in the rorearm bones and at gonion in the mandibles.

,is.2!3,,3O

June 199.1, Volumf 2. Number 2 123

Her study suggests that increased function leads to a load-related, positive bone remodeling that mini- mizes, or in some cases may counteract, the physiolog- ical, age-related changes in the bone remodeling processes leading to B h K

Early assessment and identification of osteoporotic patients can be accomplished by endocrinolo- gists, g?mecologists or orthopedic surgeons. Routine intraoral periapical or panoramic radiographs are not diagnostic until 40% or greater bone density is lost.34 There are a number of other factors that contribute to osteoporosis. As the number increases, the patient is considered to be at greater risk.

Diagnosis of the disease can be accomplished by the use of dual-photon absorptiometry or dual en- ergy x-ray ahsorptiometry (DEXA). Both are simple, painless procedures that can be accomplished in about an hour. Absorptiornetry, sometimes called densitonietry, uses a radioisotope point source and photon scintillation detection system. The machine is termed a bone mineral analyzer. The systems are accurate for both cortical and trabecular bone mea- s u r e m e n t ~ . ~ ~ , ~ ~

Which patients should one suspect enough to warrant systemic testing? The more of the following factors that hold true for the patient, the greater the risk for the disease: srnall-boned Caucasian women at menopause age or older, younger women who have had hysterectomies or hormonal disturbances, anyone with a calcium-deficient diet, smokers, sedentary individuals, and especially those with a family history of the (Table 1).

Treatment for osteoporosis can include estrogen therapy, calcium supplementation (Tables 2 and 3), exercise, vitamin D therapy, or a cotnbination of two or more of these modalities. Estrogens have bcen shown to diminish the rate of bone loss in postmenopausal women, whether menopause occurred natu- rally or was surgically induced. Furthermore, bone

Table 1. Osteoporosis: Which Patients Are Most at k s k ?

Small-boned Caucasian women, cspecially thosc At mcnopause ag-c or older With a history of surgical hysterectomy With histories of anorexia or bulimia

Persons of either sex with Genetic history of the disease Calcium-deficient diets History of heavy smoking Sedentary habits Medical trcatmcnt involving steroid or thyroid

niedicatioris

Table 2. Major Dietary Sources of Calcium ~ ~~

Milk Whole Skim

Yogurt Cottage cheese Swiss cheese American cheese Ice cream Sardines (with bones) Salmon (with bones,

Iof11 Green leafv vegetables

canncd)

290 mg/8 oz 300 mg/8 oz 400 mg/8 oz 170 mg/8 oz 270 mgloz 170 mg/oz 180 mg/8 oz 125 mg/oa

60 mg/oz 280 mg/8 oz 400 me/cup

dcnsity nieasurernenls show that estrogen therapy limits bone loss in pseudomenopausal states such as estrogen deficiency in premenopausal women associated with excessive exercise or anore~ia/bulimia.~~ Epidemiological studies have shown that functional delay of menopause through estrogen therapy will substantially decrease the ultimate risk of hip fracture.

Estrogen therapy is frequently administered to reduce bone loss and to prevent both osteoporosis and bone fractures.8 However, there is no strong evidence that estrogen thcrapy rebuilds bone or replenishes bone density, and it should not be recommended for women who have already lost consider- able amounts of bone?9 Estrogen therapy should be initiatcd in high-risk women as soon after the onset of menopause as possible, continuing for 5 to 15 years. Estrogen therapy is not indicated for women who arc more than 10 to 15 years postmenopausal, as they have already experienced the period of accelerated bone loss that accompanies and follows the menopause.

The National Osteoporosis Foundation recom- merids the following guidelines for estrogen therapy:

Utilize rstrogen therapy to preoent ostrojmosir in w o n m ielho are at high ritk, who tiaut. no ooritraindications, and who understand the bencjits andcomplicationJ 4th drug.

Table 3. Relative Calcium Loads ofVarious Salts

% Calcium Salt

Calcium carbonate Calcium sulfate Uibasic calcium phosphate Tribasic calcium phosphate Calcium lactate Calcium gluconate Calcium ascorbate Calcium citrate Calcium citratr malate

40 36.1 29.5 38.8 13 9.3

10.3 24.1 23.7

124 Osteopmosir and Implantr Bmter and Fattore

Prescribe low-dose ET ( eg . 0.62.5 m a f m 25 or 26 d a y monthb, and add a progestin (eg. 10 mg medro~f l~gater- one) on days 12-15 to days 25 or 26.

Insure that fhP patient unhgms a thorough annual physical examination yearly.

Initiute exstragen theraiy as soon as possible ajer the menopause. andplan to continue itfor at least 5 to 15years (during the period ofaccelerated bone 10~s).

Etrogen therapy may also be considered fo r older women within 5 to 15 yearr @rtmenopause who are actiwb

jacturing bones (.g. hace clinicalb ecident oste(@~ro.rir).~~

Conclusions The dentist who is considering osseointegration for a patient should be aware of any systemic diseases, especially those affecting bone. The prognosis for integration can be improved for the osteoporotic patient who is receiving treatment by a physician. Osteoporotic bone does not heal differently than bone with more density, but the biological changes may warrant some additional caution. The patient should be informed of the risks involved.

References 1. Baxter JC: Osteoporosis: Oral manifestations 0 1 a systemic

disease. Quintessence Int 1987;18:427-4'29 2. &ggs EL, h4elton LJ 111: Involutional osteoporosis. N Engl J

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4. National Institutes of Health: Consensus Confrrenrc: Osteo- porosis.JAhL4 1 984;2.52:799-802

5. Cummings SK, Rubiri SM, Black D: The future of hip fractures in thc United States: Numbers, costs and potential effects ofpostmenopausal cstrogen. Clin Orthop 1990;252: 163- I66

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7. Riggs BL, Wahner I W , Seeman E, et al: Changes in bone mineral density of the proximal femur and spine with aging: Differences between the postmenopausal and senile osteoporosis syndromes. J Clin Invest 1982:70:716-723

8. Gallagher JC, Goldgai D, Muy A4: Total bone calcium in normal women: Effect of age and menopause status. J Bone Miner Res 1987;2:491-496

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and bonc health in the elderly. Am Clin Nutr 1982;36986- 1013

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24. IIabets LLMH. Bras J, von Merkesteyn JPR hlandibular atrophy and metabolic bone loss. Histomorphometry of iliac crest biopsies in 74 patients. Int J Oral Maxillofac Surg 198X; 17:325-329

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June 1993, Volume 2, iVumher 2 125

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