The Strength of AssociationBetween Systemic

PostmenopausalOsteoporosis and

Periodontal Disease

Abdel Rahim Mohammad, DDS, MS, MPH, FACD*University of Southern CaliforniaLos Angeles, California

Michael Brunivold, DDS, MS"

Richard Bauer, MD"'

University of Texas Health Science Centerat San Antonio

San Antonio, Texas

This cross-sectional study examined the strength of association betweensystemic osteoporosis and periodontai status in postmenopausal non-Hispanic white women. Twenty subjects with low bone density and a spinebone density of 0.753 ± 0.039 dual-energy x-ray absorptiometry units (g/cm^land 22 subjects with high bone density and a spine hone density of 1.032 ±0.026 dual-energy x-ray absorptiometry units (g/cm^) were randomly selectedfrom a cohort of 565 women. Periodontal assessment included Plaque Indei;,Gingival Index, pocket depth, gingival recession, and periodontai attachmentlevel. There were no significant differences in Plaque Index, C;ingival Index,and probing depth in both groups; however, there were significantdifferences in gingival recession components of periodontal attachment levelin both groups. This study suggests that systemic osteoporosis may contributeto periodontal attachment loss in the form of gingival recession.Int I Prosthodont 1996:9:479-48i.

Osteoporosis and periodontal disease are bothmajor health problems and have other simi-

larities. They have multiple causes, involve loss ofbone mass, cause crippling effects in millions ofpeople, and cost billions of dollars annually totreat.^ Although dental plaque is generally ac-cepted as the most important single etiologic factorin periodontitis, it has been suggested that osteo-porosis might be a contributing etiologic

'Clinical Professor of Orai Medicine & Geriatric Dentistry,Department of Dental Medicine and Public Health, Schoolof Dentistry.

"Associate Professor of Periodontology, Department ofPeriodontoiogy, School of Dentistry.

"'Associate Professor, Department of Medicine, School ofMedicine.

Reprint requests: Dr Abdel Rahim Mohammad, Department ofDental Medicine and Public Health, School of Dentistry Df/V4214, University of Southern California. University Park MC-0641, Los Angeles, California 90089-0641.

This relationship has not been fairiy established,however. Other studies that have measured perio-dontal status and mineral status of the skeletonhave found no clear correlation between thetwo.^"^ There is agreement that generalizetJ osteo-porosis affects the speed of résorption and bonedensity of the maxillae and mandible.^'^

The purpose of this study was to investigate thestrength of association between periodontal diseaseand spinal bone density. Periodontal disease wasassessed by measuring pocket depth, gingival reces-sion. Gingival Index (including bleeding on probingas an indicator of active periodontal disease).Plaque Index, and periodontal attachment levels.Spine bone density was measured by dual photonabsorptiometry, a tool recently applied to evaluateand monitor osteoporosis.^ Dental plaque and gin-gival condition were also measured to ascertainwhether or not osteoporosis had any correlationwith these variables.

9, Number S, 1996 4 7 9 The International lournal of Prosthodontics

Systemic Poítmeimpauíal Osteoporosis .ird Pcriodontjl Disease

CEJ Y

FGM ^

BP

. A

Fig 1 Calcuiation of attachment ioss when there is reces-sion, CEJ = cementoenamei junction; FGM = free gingivaimargin; BP = base ot pocket; B = recession; A = pocketdeplh, A (3 mm) + B (2 mm) - 5 mm of atlaohment ioss.

Materials and Methods

Periodontal status was assessed in two groups ofwomen that had received previous spinal bonedensity measurements. Twenty women, in the bot-tom tertile of bone density (with a mean spinebone density of 0.753 ± 0.039 gm/cm-) formed theexperimental group, and 22 women in the top ter-tile of bone density (with a mean spine bone den-sity of 1,032 ± 0,028 gm/cm') formed the controlgroup. Subjects ranged in age from 50 to 75 years.The mean age of both groups was 66 years.

Both groups were selected from a cohort of 565women who were surveyed for risk factors of car-diovascular disease, diabetes, and osteoporosis atthe University of Texas Health Science Center atSan Antonio, Texas, between 1989 and 1993, Partof the survey included bone density measurementsof the spine assessed by dual energy x-ray absorp-tiometry (DEXA) using a Hologic Q1000 bone den-sitometer (Hologic, Waltham, MA) where diagnosisof low bone density is reported when a degree ofbone density is greater than two standard deviations

below normal.'' This system measured bone densityby emitting a directed x-ray beam through the areaof interest with residual radiation detected by anabsorptiometer. The degree of absorption was di-rectly related to the amount of bone present. Toidentify high and low bone density individuals, allbone densities were age adjusted. Those individualsbelow the age-adjusted mean were classified as lowbone density, and those above the mean were clas-sified as high bone density.

Periodontal examination included measurementof pocket depths, gingival recession, periodontalattachment loss. Plaque Index, and GingivalIndes,"' Attachment loss was calculated by addingpocket depth to the amount of recession as shownin Fig 1, Pocket depths were measured at threebuccal sites and one midlingual site for all teeth ofeach subject. Pocket depths were measured with aperiodontal probe from the free gingival margin tothe base of the pocket. Recession was measuredfrom ihe cementoenamel junction (CE|) to the gin-gival margin on the midfacial and midlingual sur-faces of all teeth for each subject. All periodontalmeasurements were made by one examiner whowas blinded concerning the bone density of thesubjects, Intraexaminer reliability was tested by re-peat measures at different visits. An agreement ofover 90% was observed.

The number of remaining teeth was not used asa criterion for subject selection except that com-pletely edentulous subjects were excluded. Themean number of missing teeth of subjects in thebottom tertile of spine bone density was 8.60. Inthe top tertile of spine bone density, the meannumber of missing teeth was 6.36. Means werecalculated for each patient, and then a group meanwas calculated from those means.

Student's í test was used to compare the meansof the periodontal parameters in the low- and high-density groups, Pearson correlation coefficients^^were calculated for the multivariate analysis of theperiodontal variables and spine bone density.

Results

The mean age for both the high- and low-densitygroups was 66 years (Table 1), Spine bone densitymean scores for the two groups were significantlydifferent, as expected (P < ,01), Mean PlaqueIndex scores and Gingival Index scores were notsignificantly different between the two groups, andthe mean attachment loss was significantly differ-ent in the two groups (P < ,05) (Table 1), The dif-ference in attachment loss resulted more from re-cession than pocket depth. There was no

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Po5tmeno|raiMl Oslenpomsis anti Pmodontal Di;

Table 1 Periodontal Status in Women in the Top andBottom Tertile of Spine Bone Densify (Mean and SD)

AgeSpine bone densityPiaque indexGingival IndexAttachment lossPocket depthRecession

•P i .O5.••P<.O1Standard (JeuiaLion is given IF

Bottom tertile(n = 20)

68.0 (6.8)0 753(0.039)"1.05 (0 65)0.50 ¡0.68)3.42 ¡1.35)*1.57 ¡0.51)1.85 ¡1.06)*'

1 parentlieses.

Top tertile(n - 22)

651 ¡7.2)1.032 ¡0.028)0.98 (0.49)0.33 (0.44)2.37 (1.22)1.49 ¡0.62)0.89 ¡0.82)

Table 2 Correlation Coefficient Between Spine Bone Density and Indicators ofPeriodontal Disease

Spine bone densityGingival IndexPlaque IndexAgeAttachment lossRecessionPocket depth

•P<.O5••p<.oi.

Missingteeth

-0.5800.300'

0.376"0.2830.306-0.118

Spine bonedensity

-0.156

-0.173-0.348'-0 411"-0.078

Gingii/alIndex

-0.424"0.2070.478"0.454"0.296*

Age

0 2010 2060.102

Attachmentloss

-0.452*'

0.925**0.076**

Recession

-0.303"

0.383"

significant difference in the two groups regardingpocket depth. Recession in the low-density groupwas significantly greater than in the high-densifygroup ¡P< ,05).

Pearson correlation coefficients were calculatedto determine strength of association between bonedensity and the periodontal variables (Table 2). Asignificant negative correlation ¡-0.348) was foundbetween attachment loss and spine bone density.This correlation depended to a much greater extenton recession than pocket depth. Of the periodontalvariables measured, recession showed the mostsignificant negative correlation ¡-0.411 ) with spinebone density. Pocket depths were not significantlycorrelated with spine bone density.

The Gingival Index correlated significantly with at-tachment loss (0.478) and Plaque Index (-0.424), asseen in Table 2. Age in this study did not correlatewith attachment loss or Plaque Index. Attachmentloss was significantly correlated with the PlaqueIndex (-0.452). Recession was also significantly cor-related with the Plaque Index (-0.305).

Discussion

The most important finding of this study was the sig-nificantly greater attachment loss found in the osteo-porotic group compared to controls. This finding isin disagreement with recent studies that will be sum-marized later in this discussion. Most of this differ-ence was the result of recession rather than pocketdepth. The recession component of attachment losshas recently received increased interest from resultsof epidemiologic studies. These reports^'-'^ showthat attachment loss in older populations is more re-lated to recession than pocket formation. These find-ings, along witb the present investigation, suggestthat attachment loss studies should always includerecession as an important component. The etiologyof recession is multifactorlal, and a review of thistopic is not within the scupe of this article. A recom-mended reference is a recent report by Loe andcoworkers'*' concerning the prevalence, severity,and extent of gingival recession in large populationsin Norway and Sri Lanka.

Volume 9. NLmber 5,19i)6 481 The iiilernatioriai

: Pdstmonopüus.ii Ostcoporoiis .iriít l'eiioftonla Moíiammad el al

Only a few previous studies reported on the rela-tionship between skeletal bone mass and perio-dontal status. Findings from these studies are con-flicting, making conclusions difficult.

Groen et al- studied the periodontal condition of38 subjects with clinical and radiographie signs ofvertebral osteoporosis. The Russell Index andradiographs were used to determine periodontalstatus. Twenty-seven of the 38 subjects had severeperiodontal disease, and only two had no signs ofperiodontal disease. This was not a controlledstudy, so definite conclusions cannot be made, butit suggested a possible relationship between osteo-porosis and periodontal disease.

Ward and Manson'' measured metacarpal index,alveolar bone loss score, and rapidity of bone ioss in101 subjects aged .35 to 45 years, A PeriodontalDisease Index was obtained for 62 of the patients, Asignificant correlation was found between themetacarpal index and rapidity of bone loss in fe-males but not in males. This study also was not con-trolled but suggests a possible relationship betweenO5teoporo5is and periodontal disease in females,

Phillips and Ashley^ also measured metacarpalbone density and periodontal disease in 113 fe-males aged 30 to 40 years, Russell's PeriodontalIndex was used to determine periodontai status.When only posterior teelh were analyzed therewas a significant correlation between metacarpalbone density and periodontal disease. It is impor-tant to note that Russell's Periodontal Index andthe Periodontal Disease Index measure pocketdepth but not recession as in the present study. Thethree studies summarized above, although not con-trolled, support the findings of the present investi-gation of a possible association between osteo-porosis and periodontal disease.

In contrast, more reccnl reports found no clearassociation between osteoporosis and periodontaldisease.""^ Von Wowern and Stoltze^ measuredborte mineral conleni of the forearms of 15 patientswith localized juvenik periodontitis and found thatthe bone mineral content values were within nor-mal limits,

Kribbs' compared periodontal measurements in27 normal and 85 osteoporotic women with amean age of 69 years, Periodontal measurementsincluded pocket depths, recession, and bleedingafter probing around all mandibular teeth. No dif-ferences in periodontal measurements of mandibu-lar teeth were found between osteoporotic andnormal subjects. This study was most similar in de-sign to the present investigation, A major differ-ence, however, was that the Kribbs study includedonly mandibular teeth.

Elders et al" studied lumbar bone density andmelacarpal cortical thickness in 226 dentate fe-male volunteers between 46 and 55 years of age.Oral clinical parameters of mean probing depth,occurrence of bleeding upon probing, number ofmissing teeth, and alveolar bone height were alsomeasured. Bone mass measurements showed nosignificant correlation with the clinical parameters.They concluded thai systemic bone mass is not atiimportant factor in the pathogenesis of periodonti-tis. These patients, however, were not diagnosed ashaving osteoporosis, and severe periodontitis is notcommon in this age group.

The present study, therefore, refutes to some ex-tent the findings of more recent reports but sup-ports earlier ones. Differences in study design andpatient populations may help to explain these vari-ations in results. Only one other study was foundto include recession as one of the periodontal pa-rameters,''

Further similar studies need to be performed inlarger samples of osteoporotic patients and inmales with osteoporosis. Most of the previous stud-ies have involved only women. This was probablybecause osteoporosis is a greater public healthproblem for women.

The amount of attachment loss in the low-bonedensity group was only slightly over 1 mm greaterthan the high-density group. Although this differencewas found to be statistically significant, it may notbe clinically significant, A small study populationwas used; a much larger population is needed to es-tablish a stronger correlation between periodontaldisease and osteoporosis. If the finding of increasedrecession in osteoporotic subjects is supported bymore studies, in the future recession might be tjsedas an early warning sign or marker for osteoporosis.

Further research in larger populations is neededto confirm these conclusions and further elucidatethe association between systemic osteoporosis andperiodontal disease.

Conclusions

Factors associated witb periodontal disease wereassessed in 20 women known to have lower bonedensity and were compared to the same factorsfound in 22 women of normal bone density.Within the limitations of tbe size of the study andthe parameters measured, the following conclu-sions may be made:

1. The results of this study suggest that osteoporo-sis may contribute to periodontal attachmentloss.

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l'ustmenojjausal O;[enpuro5Í5 jnd Perioílontal Di;

2, Subjects with osteoporosis did not have signifi-cantly greater pocket depths than control sub-jects with normal bone density,

3. Subjects with osteoporosis had significantlygreater gingival recession compared to confrolsubjects.

Acknowledgments

The authori wish to acknowledge Ihe support and encourage-ment ot Dr5 Michelle Saunders and Michael Katz, the co-direc-tor and director of the Geriatric Research and EducationalCenter at the University of Texas Health Science Center at SanAntonio, Texas.

This study was supported by the Geriatr ic LeadershipAcademic Award Grant awarded to the first author.

References

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4, Ward V, Manson |, Alveolar hone loss in periodontal diseaseand the metacarpal indsx, | Periodontol 1973;44:763-759,

5, Von Wcwern N, Stoltze K, Juvenile periodontitis: Skeletalbone mineral content. I Clin Periodontol 1977;4:272-277,

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n , Elston R, Johnson W. Essentiais of Biostatislics, Phiiadeiphia:Davis, 1987:194-195,

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13. Yoneyama T, O kam oto H, Lindhel, Socransky S, Haffsjee A.Probing depth, attachment loss and gingival recession.Findings from a clinical examination in Ushiku, |apan. J ClinPeriodontol I93B:I5:S81-591,

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Literature Abstract

Combination syndrome associated with a mandibuiar implant-supportedoverdenture; A clinical report

Combination syndrome is characterized by bone loss in the maxillary anterior ridge, over-

growth of the tuberosities, palatal papillary hyperplasia, supereruption of mandibular anterior

teeth, and bone loss beneath removable partial denture bases. Patients whose dentition is

restored by mandibuiar implant-supported prostheses opposing complete dentures may tace

similar phenomena to the classic combination syndrome because the implants encourage

patients to incise antenorly with maximum force The passive threshold lor tactile function of

dental implants has been reported to be approximately 60 times that ot natural teeth. The in-

creased torce generation by tiie implants coupled with anterior functional contact leads to ré-

sorption of the anterior maxillary ridge. The authors stated that symptoms ot combination

syndrome developed within 2 years of delivery of an endcsseous implant-retained mandibu-

lar overdenture opposing a maxillary complete denture. To prevent the consequences of

combination syndrome, the authors emphasized that maintenance of anterior-posterior oc-

clusal stability, particularly in protrusive movements, is especially important The authors rec-

ommend that anterior teeth have no occlusal contact in centric position and minimal contact

during excursive mandibular movements. The use of maxillary impiants and maxillary ridge

augmentation may minimize the detrimental effects of combination syndrome,

Thiel CP, Evans DB, Burnett RR. J Prosthet Dent 1996,75 107-113, References: 16. Reprints:

Cynlhia P,Thiel, 82 Dental Squaöran/SGD, 149 Hart Sireet, Suite 4, Sheppard Air Force Base, Texas

76311-3481 .—Seung-il Eom, DDS, Advanced Education Program in Proslhodontics. New York

University College of Dentistry, New York, New York

9, Number 5,1996 4 8 3 The Intemational loumai oí Proslhodontics