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  Osteoporosis and periodontaldisease progression N ico  C. G eurs , C ora   E lizabeth  L ewis  & M  arjorie  K. J effcoat Osteopenia and osteoporosis are systemic skeletaldiseases characterized by low bone mass andmicro-architectural deterioration with a consequentincrease in bone fragility and susceptibility to frac-ture. According to the World Health Organization,osteoporosis is considered to be present when bonemineral density (BMD) is 2.5 standard deviations(SD) below the young normal. Osteopenia is definedas bone density levels between 1 SD and 2.5 SDbelow normal BMD (29).In the third National Health and Nutrition Exam-ination Survey (NHANES III) the prevalence of osteo-porosis when assessed at the femoral neck was 20%of postmenopausal white women (16). An alternativeapproach is to use morphological deformities in thevertebrae to define osteoporosis. The prevalence of the defined vertebral deformities was found to be12% in both men and women. The increase in fre-quency with age was greater in women, from 5% atage 50–54 to 24% at age 75–79. For men this was 10%at age 50–54 years, rising to 18% at age 75–79 years(18). The prevalence of this relatively silent disease isvery high and on the rise. Future projections indicatea threefold increase in osteoporosis-related hip frac-tures (9).The risk factors for osteoporosis can be dividedinto non-modifiable and modifiable risk factors.The non-modifiable include sex, age, early meno-pause, thin or small body frame, race, and heredity.Lack of calcium intake, lack of exercise, smoking, andalcohol are modifiable risk factors. Low bone mass,certain medications, propensity to fall, and systemicdiseases such as hyperparathyroidism are modifiableto some extent. These risk factors have been dis-cussed previously (5, 6).The risk factors for osteoporosis include many risk factors associated with advanced periodontal dis-ease. Since both osteoporosis and periodontal dis-eases are bone resorptive diseases, it has beenhypothesized that osteoporosis could be a risk factorfor the progression of periodontal disease. Relationbetweensystemicbonemineraldensityandoralbonemineraldensity  Studies discussing the relationship between systemicBMD and oral BMD are summarized in Table 1. Moststudies reported to date concerning this relationshipare cross-sectional studies using different popula-tions and different methods to assess BMD.Kribbs et al. (15) was the first to address the rela-tionship in osteoporotic women in a study assessing total body calcium by neutron activation analysis. Anassociation was found with mandibular density whenmeasured by quantitative analysis on intraoral radio-graphs. In a comparison of 85 osteoporotic womenand 27 normal women, the osteoporotic group hadless mandibular bone mass and density and a thinnercortex at the gonion than the normal group. Theosteoporotic group also had a greater percentage of subjects who were edentulous. In dentate subjects a greater amount of tooth loss was reported for theosteoporotic group. No differences in clinical period-ontal measurements were found between osteoporo-tic and normal groups (12–14).In a study of 12 osteoporotic subjects with a history of fractures, von Wowern et al. (27) found less man-dibular bone mineral content as measured by dualphoton absorptiometry than in 14 normal women.In a longitudinal study of 69 women receiving hormone replacement therapy, lumbar spine BMD was assessed by dual photon absorptiometry. Whencompared to quantitative measurements of standar-dized radiographs of the posterior region, a signifi-cant but moderate correlation was found only at thesecond visit. During the observation period of an 105  Periodontology 2000, Vol. 32, 2003, 105–110 Copyright   #  Blackwell Munksgaard 2003Printed in Denmark. All rights reserved   PERIODONTOLOGY 2000 ISSN 0906-6713  average of 5 years, a positive effect of estrogen repla-cement therapy on the bone mass of the mandibleand the lumbar spine was observed. Different estro-gen regimens resulted in different increases in bonemass (4).Streckfus et al. (24) used quantitative measure-ments of vertical bitewing and hand radiographs inpatients with active periodontitis. The results of thestudy showed that postmenopausal women on estro-gen therapy had more alveolar bone loss (ABL), moremissing teeth, and reduced alveolar and second met-acarpal bone density than premenopausal women. Alveolar bone densities were also strongly correlatedto second metacarpal densities.Most studies relate systemic BMD with mandibu-lar mineral density. In a study of both maxilla andmandible, 41 dentate Caucasian women aged 20 – 78 were evaluated using quantitative intraoral radiogra-phy and systemic bone densities determined by dual-energy X-ray absorptiometry (DXA) (23). The density of maxillary alveolar process bone was signi fi cantly related to the density of the mandibular alveolarprocess, lumbar spine, hip, and radius in healthy  women and maxillary alveolar process bone density declined with age (23).Shrout et al. (22) used morphologic measurementsfrom digitized images of bitewing radiographs tocorrelate with lumbar and femoral BMD in 45 post-menopausal women who had no or only mild period-ontal disease (no probing depths  >  5 mm). Thecomplexity of the trabecular pattern weakly corre-lated with lumbar spine and femoral BMD.In a preliminary report of the oral ancillary study of the Women ’ s Health Initiative, 158 patients with a mean age of 62.2    7.6 years were evaluated (6).Hipbone mineral density was con fi rmed by DXA and mandibular bone density was measured by quantitative digital intraoral radiography. A signi fi -cant correlation was found between mandibularbasal bone and hipbone mineral density (6). Theauthors posed the question whether intraoral radio-graphy could serve as a screening tool for osteopenia. Table 1.  Relation between systemic bone mineral density (BMD) and oral bone mineral density   Authors Population Major Result Type of study  Jeffcoat et al. (6) 158 postmenopausal women Age 62.2    7.6 yearsSignificant correlation betweenhip BMD and mandibularbasal BMDCross-sectional study Shrout et al. (22) 45 postmenopausal women with no ormild periodontitisMean age 57.4    5.8Complexity of the trabecularpattern weakly correlated withlumbar spine and femoral BMDCross-sectional study Southard et al. (23) 41 dentate Caucasian women aged20 to 78 yearsSignificant correlation between thedensity of maxillary and mandibularalveolar process, lumbar spine,hip, and radius in healthy women.Cross-sectional study Streckfus et al. (23) 28 healthy womenaged 23 – 78Strong correlation between alveolar boneand the second metacarpal densities.Both reduced in postmenopausal womenCross-sectional study Jacobs et al. (4) 69 women receiving HRTaged 32 – 64 at entry Correlation between spinal density andmandibular bone mass at the secondexamination (average follow-up 5.1 years)longitudinal study von Wowernet al. (27)12 women withosteoporotic fracturesOsteoporotic subjects had less bonemineral contentCross-sectional study Kribbs et al. (14) 50 normal womenaged 20 – 90Mandibular bone mass correlated withbone mass at spine and wristCross-sectional study Kribbs (12) 85 osteoporotic womenand 27 normal women aged 50 – 85Osteoporotic group had less mandibularbone mass and density Cross-sectional study Kribbs et al. (13) 85 osteoporotic women Total body calcium, bone mass at radius,and bone density at spine correlated with mandibular massCross-sectional study Kribbs et al. (15) 30 postmenopausal womenTotal body calcium associated withmandibular bone density Cross-sectional study  Geurs et al. 106   The usefulness of the alveolar trabecular patternanalysis and mandibular alveolar bone mass for pre-diction of the skeletal BMD was further evaluated by Jonasson et al. (8). They used an index to assess thealveolar trabecular patterns and found a signi fi cantcorrelation with skeletal BMD. The evaluation of thecoarseness of trabeculation of the alveolar bone asseen on intraoral radiographs could be a helpful clin-ical indicator of skeletal BMD and better than densi-tometric measurements of the alveolar bone. Densetrabeculation is a strong indicator of high BMD, whereas sparse trabeculation may be used to predictlow BMD.The data gathered on the mostly cross-sectionalstudies appears to indicate a relationship betweensystemic BMD and oral BMD. Additional data fromongoing longitudinal studies will further elaboratethis relationship. Periodontaldiseaseandosteoporosis The relationship of tooth loss and BMD has beenstudied. Several reports  fi nd a correlation betweentooth loss and diminished systemic BMD (5, 11, 24,25). Other reports fail to  fi nd this correlation (1, 10,19). The use of tooth loss as a surrogate for period-ontal disease extent has several limitations. Theunderlying reason for the loss of the teeth is oftenunknown. The extent of the disease around theremaining teeth is not taken into account in theseanalyses. Therefore, an accurate measurement of theextent of periodontal destruction can not be made by using tooth loss as a variable in the analysis of therelationship between osteoporosis and periodontitis.Several mostly cross-sectional reports have used a variety of parameters to evaluate the periodontal dis-ease severity in subjects with decreased BMD. Thesereports are summarized in Table 2.In a report by Elders et al. (1), lumbar BMD andmetacarpal cortical thickness (MCT) were comparedto alveolar bone height measured on bitewing radio-graphs and clinical parameters of periodontitis. Nosigni fi cant relation was observed between the bonemass measurements and alveolar bone height or per-iodontal parameters. The mean age in this group wasrelatively young, between 46 and 55 years of age, which could have contributed to the lack of cor-relation.Similar  fi ndings were reported in a study of toothloss and attachment loss when related to vertebraland proximal femoral BMD. In that study, 135 women with at least 10 teeth and no evidence of moderate or severe periodontal disease were exam-ined. Attachment loss was correlated with tooth lossbut not with vertebral or proximal femur bone den-sity (3). When comparing the number of sites with loss of attachment with BMD in 292 dentate women (aver-age age 75.5 years) no statistically signi fi cant associa-tion was found (28).In an age cohort of 70-year-old women, 15 subjects with osteoporosis were compared to 21 subjects withnormal BMD (17). No statistically signi fi cant differ-ences were found in gingival bleeding, probing pocket depths, gingival recession, or marginal bonelevel between the women with osteoporosis and the women with normal BMD (17).In contrast to these reports, other authors havereported a signi fi cant relation between systemicosteopenia and periodontal bone loss. Von Wowernet al. (27) found greater amounts of loss of attach-ment in osteoporotic women in a small population with a mean age of 68. Osteoporosis was assessedusing bone mineral content of the mandible andforearm determined by dual photon scanning.In a study population of 70 postmenopausalCaucasian women aged 51 – 78, skeletal systemicBMD was assessed by DXA (26). Clinical attachmentloss and interproximal ABL represented periodontaldisease severity. Mean ABL signi fi cantly correlated with systemic BMD. A trend for a correlationbetween clinical attachment levels and BMD wasfound (26).The cross-sectional studies have limitations. Noinformation about the diseases studied prior to theexam is available. Although both osteopenia and per-iodontal disease are chronic diseases and can beassumed to have been present prior to the observa-tions, it is incorrect to conclude that both diseaseshave been present. To better evaluate this relation-ship, prospective longitudinal studies are needed. Todate, few longitudinal studies have been performed.In a 2-year longitudinal clinical study, the alveolarbone height and density changes in 21 osteoporotic/osteopenic women compared with 17 women withnormal lumbar spine BMD were studied. The sub- jects were postmenopausal women enrolled in a periodontal maintenance program. Osteoporotic/osteopenic women exhibited a higher frequency of alveolar bone height loss and crestal and subcrestaldensity loss relative to women with normal BMD.Estrogen de fi ciency was associated with increasedfrequency of alveolar bone crestal density loss in 107  Osteoporosis and periodontal disease progression  the osteoporotic/osteopenic women. The authorsconcluded that osteoporosis/osteopenia and estro-gen de fi ciency are risk factors for alveolar bone den-sity loss in postmenopausal women with a history of periodontitis.Fifty-nine moderate/advanced adult periodontitispatients and 16 non-periodontitis subjects, all within5 years after menopause at baseline, were strati fi edbased on serum estradiol levels. Attachment loss wasassessed over a 2-year period and correlated to BMDand serum estradiol levels. Serum estradiol levels didnot in fl uence the percentage of sites losing attach-ment for either periodontitis or non-periodontitisgroups. The estradiol-de fi cient group had a trendtoward a higher frequency of sites with attachmentloss   2 mm.Larger prospective longitudinal studies are neededto further evaluate osteoporosis as a risk factor forperiodontal disease progression. The oral ancillary study of the Women ’ s Health Initiative at theUniversity of Alabama at Birmingham was designedto determine if there is an association between sys-temic osteoporosis and oral bone loss. In this report,preliminary prospective longitudinal data will bepresented. The Women ’ s Health Initiative is a study of women ’ s health after menopause in the UnitedStates. Risk factors for diseases in this populationare being studied nationwide and include heart dis-ease and osteoporosis. Utilizing the unique opportu-nity for collaboration with the Women ’ s HealthInitiative at the University of Alabama at Birming-ham, an oral ancillary study was established. All subjects enrolled in the study were post-meno-pausal females. Hipbone mineral density was con- fi rmed with DXA. Comprehensive medical historiesand examinations were linked with the results of oral Table 2.  Relationship of periodontal destruction and bone mineral density (BMD)  Authors Population Major result Type of study  Lundstrom et al. (17) 15 women withosteoporosis, 21 women with normal BMDNo statistically significantdifferences in gingival bleeding,probing pocket depths, gingivalrecession and marginal bone levelCross-sectionalstudy Tezal et al. (26) 70 postmenopausal Caucasian women aged 51 – 78Mean ABL was significantly correlated with BMD.Cross-sectionalstudy  Weyant et al. (28) 292 dentate women (averageage 75.5 years)No statistically significant associationbetween periodontal disease andsystemic BMD.Cross-sectionalstudy Payne (20) Female periodontal maintenancepatients within 5 years of menopause; 21 with normalBMD, 17 osteoporotic womenGreater ABL, crestal andsubcrestal density loss in theosteoporotic and estrogen-deficient women.2-year longitudinalclinical study Reinhardt et al. (21) Women within 5 years of menopause, 59 with adultperiodontitis and 16non-periodontitis. Stratifiedby serum estradiol levelsIn non-smoking osteopenic/osteoporotic periodontitis patients with estrogen deficiency hadmore bleeding on probing andclinical attachment levels2-year prospectivelongitudinal study Hildebolt et al. (3) 135 postmenopausal womenaged 41 – 70 years, no moderate,severe periodontitis Attachment loss was correlated withtooth loss but not with BMD.Cross-sectionalstudy Streckfus et al. (24) 28 healthy womenaged 23 – 78More ABL, more missing teeth, inpostmenopausal women onestrogen therapy thanpremenopausal women.Cross-sectionalstudy von Wowernet al. (27)12 women with osteoporoticfracturesOsteoporotic subjects had moreloss of attachment than normalsubjectsCross-sectionalstudy Elders et al. (1) 216 females between 46and 55 yearsNo significant correlation wasobserved between probing depth,bleeding on probing, missing teeth, alveolar bone height andbone massCross-sectionalstudy  108 Geurs et al.

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