Archives of Osteoporosis

, 14:94 | Cite as

An investigation of the bidirectional link between osteoporosis and periodontitis

  • D. C. Penoni
  • M. V. Vettore
  • S. R. Torres
  • M. L. F. Farias
  • A. T. T. Leão
Original Article



This study investigated whether periodontitis affects systemic bone status and whether FRAX® is a screening tool for periodontal disease in elderly women. The findings showed that bone density was not influenced by periodontitis and highlighted that women with FRAX® score above the intervention threshold had greater chance to present severe periodontitis.


This study investigated whether periodontal disease is a predictor for systemic bone loss among elderly women. The utilization of FRAX® as a screening tool for severe periodontitis was also evaluated in this population.


Current bone mineral density (BMD) for lumbar spine and proximal femur was used as an indicator of “bone status.” Number of interdental sites with severe clinical attachment loss, frequency of bleeding on probing, and percentage of tooth loss due to periodontitis represented “periodontal disease” that was tested as a predictor of bone loss in a structural equation modeling analysis involving 110 participants. The intake of antiosteoporosis medication was considered in the analysis. Four other different criteria for periodontitis classification were also tested. FRAX® for major fracture was calculated without BMD, and with intervention threshold set by age. Longitudinally, BMD changes up to 10 years were also obtained and checked for possible association with periodontitis.


Periodontal disease was not a predictor for worse systemic bone status according to the different periodontal disease classifications, and was not associated with BMD changes. Antiosteoporosis medication directly predicted periodontal disease and systemic bone status. Women with FRAX® score above the intervention threshold had higher chance for periodontitis in more advanced stages: III/IV (OR = 1.13, 95% CI [1.04 to 1.22], p = 0.03).


Periodontal disease did not constitute a predictor for reduced systemic bone density in the studied population of elderly women. On the other hand, FRAX® demonstrated to be a useful tool to suggest periodontal evaluation. Antiresorptive medication showed benefits on periodontal and bone status.


Bone density FRAX Osteoporosis Periodontitis Tooth loss Elderly 



The authors thank the Coordination for the Improvement of Higher Education Personnel (CAPES), Brazil.

Compliance with ethical standards

Conflicts of interest


Supplementary material

11657_2019_643_MOESM1_ESM.pdf (205 kb)
ESM 1 (PDF 205 kb)
11657_2019_643_MOESM2_ESM.pdf (182 kb)
ESM 2 (PDF 182 kb)


  1. 1.
    Holmstrup P, Damgaard C, Olsen I, Klinge B, Flyvbjerg A, Nielsen CH, Hansen PR (2017) Comorbidity of periodontal disease: two sides of the same coin? An introduction for the clinician. J Oral Microbiol 9:1332710CrossRefGoogle Scholar
  2. 2.
    Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 4:368–381CrossRefGoogle Scholar
  3. 3.
    Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY (2013) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 24:23–57CrossRefGoogle Scholar
  4. 4.
    Manolagas SC (2018) The quest for osteoporosis mechanisms and rational therapies: how far we’ve come, how much further we need to go. J Bone Miner Res 33:371–385CrossRefGoogle Scholar
  5. 5.
    Wang CJ, McCauley LK (2016) Osteoporosis and periodontitis. Curr Osteoporos Rep 14:284–291CrossRefGoogle Scholar
  6. 6.
    Mark Bartold P, Van Dyke TE (2017) Host modulation: controlling the inflammation to control the infection. Periodontol 2000(75):317–329CrossRefGoogle Scholar
  7. 7.
    Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, Greenwell H, Herrera D, Kao RT, Kebschull M, Kinane DF, Kirkwood KL, Kocher T, Kornman KS, Kumar PS, Loos BG, Machtei E, Meng H, Mombelli A, Needleman I, Offenbacher S, Seymour GJ, Teles R, Tonetti MS (2018) Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 45(Suppl 20):S162–s170CrossRefGoogle Scholar
  8. 8.
    Marcenes W, Kassebaum NJ, Bernabe E, Flaxman A, Naghavi M, Lopez A et al (2013) Global burden of oral conditions in 1990-2010: a systematic analysis. J Dent Res 92:592–597CrossRefGoogle Scholar
  9. 9.
    Chapple IL, Bouchard P, Cagetti MG, Campus G, Carra MC, Cocco F et al (2017) Interaction of lifestyle, behaviour or systemic diseases with dental caries and periodontal diseases: consensus report of group 2 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. J Clin Periodontol 44(Suppl 18):S39–s51CrossRefGoogle Scholar
  10. 10.
    McCloskey EV, Johansson H, Oden A, Kanis JA (2009) From relative risk to absolute fracture risk calculation: the FRAX algorithm. Curr Osteoporos Rep 7:77–83CrossRefGoogle Scholar
  11. 11.
    Alli F, Bhandal GK, Thacker HL, Palomo L (2015) Can the FRAX tool be a useful aid for clinicians in referring women for periodontal care? Menopause 22:75–78CrossRefGoogle Scholar
  12. 12.
    Kanis JA, Harvey NC, Cooper C, Johansson H, Oden A, McCloskey EV (2016) A systematic review of intervention thresholds based on FRAX : a report prepared for the National Osteoporosis Guideline Group and the International Osteoporosis Foundation. Arch Osteoporos 11:25CrossRefGoogle Scholar
  13. 13.
    Anbinder AL, Moraes RM, Lima GMG, Oliveira FE, Campos DRC, Rossoni RD, Oliveira LD, Junqueira JC, Ma Y, Elefteriou F (2016) Periodontal disease exacerbates systemic ovariectomy-induced bone loss in mice. Bone 83:241–247CrossRefGoogle Scholar
  14. 14.
    Choi JK, Kim YT, Kweon HI, Park EC, Choi SH, Lee JH (2017) Effect of periodontitis on the development of osteoporosis: results from a nationwide population-based cohort study (2003-2013). BMC Womens Health 17:77CrossRefGoogle Scholar
  15. 15.
    Mau LP, Kuan YC, Tsai YC, Lin JJ, Huynh-Ba G, Weng PW et al (2017) Patients with chronic periodontitis present increased risk for osteoporosis: a population-based cohort study in Taiwan. J Periodontal Res 52:922–929CrossRefGoogle Scholar
  16. 16.
    Nesse W, Abbas F, van der Ploeg I, Spijkervet FK, Dijkstra PU, Vissink A (2008) Periodontal inflamed surface area: quantifying inflammatory burden. J Clin Periodontol 35:668–673CrossRefGoogle Scholar
  17. 17.
    Penoni DC, Torres SR, Farias MLF, Fernandes TM, Luiz RR, Leão ATT (2016) Association of osteoporosis and bone medication with the periodontal condition in elderly women. Osteoporos Int 27:1887–1196CrossRefGoogle Scholar
  18. 18.
    Penoni DC, Leão ATT, Torres SR, Farias MLF, Fernandes TM, Crivelli M, Vettore MV (2018) Effects of bone fragility and antiresorptive drugs on periodontal disease and tooth loss: a longitudinal study. JDR Clinical & Translational Research 3:10CrossRefGoogle Scholar
  19. 19.
    Zerbini CA, Szejnfeld VL, Abergaria BH, McCloskey EV, Johansson H, Kanis JA (2015) Incidence of hip fracture in Brazil and the development of a FRAX model. Arch Osteoporos 10:224CrossRefGoogle Scholar
  20. 20.
    Clark P, Denova-Gutierrez E, Zerbini C, Sanchez A, Messina O, Jaller JJ et al (2018) FRAX-based intervention and assessment thresholds in seven Latin American countries. Osteoporos Int 29:707–715CrossRefGoogle Scholar
  21. 21.
    Kanis JA, McCloskey EV, Johansson H, Strom O, Borgstrom F, Oden A (2008) Case finding for the management of osteoporosis with FRAX--assessment and intervention thresholds for the UK. Osteoporos Int 19:1395–1408CrossRefGoogle Scholar
  22. 22.
    Tonetti MS, Greenwell H, Kornman KS (2018) Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Clin Periodontol 45(Suppl 20):S149–s161CrossRefGoogle Scholar
  23. 23.
    Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ (2012) Update of the case definitions for population- based surveillance of periodontitis. J Periodontol 83:1449–1454CrossRefGoogle Scholar
  24. 24.
    Machtei EE, Christersson LA, Grossi SG, Dunford R, Zambon JJ, Genco RJ (1992) Clinical criteria for the definition of “established periodontitis”. J Periodontol 63:206–214CrossRefGoogle Scholar
  25. 25.
    Tomar SL, Asma S (2000) Smoking-attributable periodontitis in the United States: findings from NHANES III. J Periodontol 71:743–751CrossRefGoogle Scholar
  26. 26.
    Beck JD, Koch GG, Rozier RG, Tudor GE (1990) Prevalence and risk indicators for periodontal attachment loss in a population of older community-dwelling blacks and whites. J Periodontol 61:521–528CrossRefGoogle Scholar
  27. 27.
    Westland J (2012) Lower bounds on sample size in structural equation modeling. Electron Commer Res Appl 11:445CrossRefGoogle Scholar
  28. 28.
    Kanis JA, McCloskey EV, Harvey NC, Johansson H, Leslie WD (2015) Intervention thresholds and the diagnosis of osteoporosis. J Bone Miner Res 30:1747–1753CrossRefGoogle Scholar
  29. 29.
    Penoni DC, Fidalgo TK, Torres SR, Varela VM, Masterson D, Leao ATT et al (2017) Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res 96:261–269CrossRefGoogle Scholar
  30. 30.
    Jepsen S, Caton JG, Albandar JM, Bissada NF, Bouchard P, Cortellini P, et al (2018) Periodontal manifestations of systemic diseases and developmental and acquired conditions: consensus report of workgroup 3 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 8;89 Suppl 1:S237-s248CrossRefGoogle Scholar
  31. 31.
    Albandar JM, Susin C, Hughes FJ (2018) Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: case definitions and diagnostic considerations. J Clin Periodontol 45(Suppl 20):S171–s189CrossRefGoogle Scholar
  32. 32.
    Baker SR (2007) Testing a conceptual model of oral health: a structural equation modeling approach. J Dent Res 86:708–712CrossRefGoogle Scholar
  33. 33.
    MacCallum RC, Austin JT (2000) Applications of structural equation modeling in psychological research. Annu Rev Psychol 51:201–226CrossRefGoogle Scholar
  34. 34.
    Needleman I, Garcia R, Gkranias N, Kirkwood KL, Kocher T, Iorio AD, Moreno F, Petrie A (2018) Mean annual attachment, bone level, and tooth loss: a systematic review. J Clin Periodontol 45(Suppl 20):S112–s129CrossRefGoogle Scholar
  35. 35.
    Bhavsar NV, Trivedi SR, Dulani K, Brahmbhatt N, Shah S, Chaudhri D (2016) Clinical and radiographic evaluation of effect of risedronate 5 mg as an adjunct to treatment of chronic periodontitis in postmenopausal women (12-month study). Osteoporos Int 27:2611–2619CrossRefGoogle Scholar
  36. 36.
    Palomo L, Buencamino-Francisco MC, Carey JJ, Sivanandy M, Thacker H (2011) Is long-term bisphosphonate therapy associated with benefits to the periodontium in postmenopausal women? Menopause 18:164–170PubMedGoogle Scholar
  37. 37.
    Akram Z, Abduljabbar T, Kellesarian SV, Abu Hassan MI, Javed F, Vohra F (2017) Efficacy of bisphosphonate as an adjunct to nonsurgical periodontal therapy in the management of periodontal disease: a systematic review. Br J Clin Pharmacol 83:444–454CrossRefGoogle Scholar
  38. 38.
    Gourlay ML, Fine JP, Preisser JS, May RC, Li C, Lui LY, Ransohoff DF, Cauley JA, Ensrud KE, Study of Osteoporotic Fractures Research Group (2012) Bone-density testing interval and transition to osteoporosis in older women. N Engl J Med 366:225–233CrossRefGoogle Scholar
  39. 39.
    Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386CrossRefGoogle Scholar
  40. 40.
    Lamster IB, Asadourian L, Del Carmen T, Friedman PK (2016) The aging mouth: differentiating normal aging from disease. Periodontol 2000 72:96–107CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2019

Authors and Affiliations

  1. 1.Department of Preventive DentistryOdontoclínica Central da Marinha, Brazilian NavyRio de JaneiroBrazil
  2. 2.Department of Dental Clinic, Division of Periodontics, Dental SchoolUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Rio de JaneiroBrazil
  4. 4.Department of Social and Preventive Dentistry, Dental SchoolFederal University of Minas GeraisBelo HorizonteBrazil
  5. 5.Department of Oral Pathology and Diagnosis, Dental SchoolUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  6. 6.Division of Endocrinology, Department of Internal MedicineUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil

Personalised recommendations