Skip to main content

Advertisement

Log in

Periodontal bone loss and risk of epithelial ovarian cancer

  • Brief report
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

Periodontitis, a chronic inflammatory response to pathogenic bacteria in the oral microbiome, is common among adults. It is associated with several medical conditions, including cardiovascular diseases, and potentially with esophageal, lung, oral, and pancreatic cancer. One of the proposed mechanisms behind these associations is systemic inflammation, which has also been implicated in ovarian cancer etiology. The aim of this study was to evaluate association between ovarian cancer and periodontal bone loss.

Methods

The association between periodontal bone loss, a marker of periodontitis, and risk of epithelial ovarian cancer was estimated among 60,560 participants of the prospective Nurses’ Health Study using Cox proportional hazards analysis. Competing risks analysis was used to estimate association by histologic subtype.

Results

We did not observe an increased risk of ovarian cancer among participants with periodontal bone loss (HR 0.86, 95 % CI 0.64–1.15). Among women younger than 69 years, periodontal bone loss was associated with a 40 % (HR 0.60, 95 % CI 0.36–0.98) decreased ovarian cancer risk, while there was no association in women older than 69 (HR 1.09, 95 % CI 0.75–1.58), although this difference did not reach statistical significance (p-heterogeneity = 0.06). We observed a suggestive decreased risk for serous tumors (HR 0.76, 95 % CI 0.53–1.09). The number of natural teeth and root canals, other metrics of oral health, were not associated with ovarian cancer risk.

Conclusion

Our results do not support an increased ovarian cancer risk in women with periodontal bone loss; however, there was a significant decrease in risk in women younger than 69. Given the unexpected association between periodontal bone loss and ovarian cancer risk in younger women, further research is warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  1. American Cancer Society (2014) Cancer facts and figures 2014. American Cancer Society, Atlanta

    Google Scholar 

  2. Cramer DW, Welch WR (1983) Determinants of ovarian cancer risk. II. Inferences regarding pathogenesis. J Natl Cancer Inst 71:717–721

    CAS  PubMed  Google Scholar 

  3. Fathalla MF (1971) Incessant ovulation—a factor in ovarian neoplasia? Lancet 2:163

    Article  CAS  PubMed  Google Scholar 

  4. Risch HA (1998) Hormonal etiology of epithelial ovarian cancer, with a hypothesis concerning the role of androgens and progesterone. J Natl Cancer Inst 90:1774–1786

    Article  CAS  PubMed  Google Scholar 

  5. Ness RB, Cottreau C (1999) Possible role of ovarian epithelial inflammation in ovarian cancer. J Natl Cancer Inst 91:1459–1467

    Article  CAS  PubMed  Google Scholar 

  6. Poole EM, Lee IM, Ridker PM, Buring JE, Hankinson SE, Tworoger SS (2013) A prospective study of circulating C-reactive protein, interleukin-6, and tumor necrosis factor alpha receptor 2 levels and risk of ovarian cancer. Am J Epidemiol 178:1256–1264

    Article  PubMed Central  PubMed  Google Scholar 

  7. Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ (2012) Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res 91:914–920

    Article  CAS  PubMed  Google Scholar 

  8. Papapanou PN (1996) Periodontal diseases: epidemiology. Ann Periodontol 1:1–36

    Article  CAS  PubMed  Google Scholar 

  9. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820

    Article  PubMed  Google Scholar 

  10. Joshipura KJ, Wand HC, Merchant AT, Rimm EB (2004) Periodontal disease and biomarkers related to cardiovascular disease. J Dent Res 83:151–155

    Article  CAS  PubMed  Google Scholar 

  11. Moutsopoulos NM, Madianos PN (2006) Low-grade inflammation in chronic infectious diseases: paradigm of periodontal infections. Ann N Y Acad Sci 1088:251–264

    Article  CAS  PubMed  Google Scholar 

  12. Fitzpatrick SG, Katz J (2010) The association between periodontal disease and cancer: a review of the literature. J Dent 38:83–95

    Article  PubMed  Google Scholar 

  13. Bascones-Martinez A, Gonzalez-Febles J, Sanz-Esporrin J (2014) Diabetes and periodontal disease. Review of the literature. Am J Dent 27:63–67

    PubMed  Google Scholar 

  14. Demmer RT, Desvarieux M (2006) Periodontal infections and cardiovascular disease: the heart of the matter. J Am Dent Assoc 137:14S–20S

    Article  PubMed  Google Scholar 

  15. Huck O, Tenenbaum H, Davideau JL (2011) Relationship between periodontal diseases and preterm birth: recent epidemiological and biological data. J Pregnancy 2011:164654

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Meyer MS, Joshipura K, Giovannucci E, Michaud DS (2008) A review of the relationship between tooth loss, periodontal disease, and cancer. Cancer Causes Control 19:895–907

    Article  PubMed Central  PubMed  Google Scholar 

  17. Nakib S, Han J, Li T, Joshipura K, Qureshi AA (2013) Periodontal disease and risk of psoriasis among nurses in the United States. Acta Odontol Scand 71:1423–1429

    Article  PubMed Central  PubMed  Google Scholar 

  18. Colditz GA, Hankinson SE (2005) The Nurses’ Health Study: lifestyle and health among women. Nat Rev Cancer 5:388–396

    Article  CAS  PubMed  Google Scholar 

  19. McCullough ML, Feskanich D, Stampfer MJ, Giovannucci EL, Rimm EB, Hu FB et al (2002) Diet quality and major chronic disease risk in men and women: moving toward improved dietary guidance. Am J Clin Nutr 76:1261–1271

    CAS  PubMed  Google Scholar 

  20. Bertrand KA, Giovannucci E, Liu Y, Malspeis S, Eliassen AH, Wu K et al (2012) Determinants of plasma 25-hydroxyvitamin D and development of prediction models in three US cohorts. Br J Nutr 108:1889–1896

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Lunn M, McNeil D (1995) Applying Cox regression to competing risks. Biometrics 51:524–532

    Article  CAS  PubMed  Google Scholar 

  22. Beral V, Gaitskell K, Hermon C, Moser K, Reeves G, Peto R (2012) Ovarian cancer and smoking: individual participant meta-analysis including 28,114 women with ovarian cancer from 51 epidemiological studies. Lancet Oncol 13:946–956

    Article  CAS  PubMed  Google Scholar 

  23. Preshaw PM (2013) Oral contraceptives and the periodontium. Periodontol 2000(61):125–159

    Article  Google Scholar 

  24. Taguchi A, Sanada M, Suei Y, Ohtsuka M, Nakamoto T, Lee K et al (2004) Effect of estrogen use on tooth retention, oral bone height, and oral bone porosity in Japanese postmenopausal women. Menopause 11:556–562

    Article  PubMed  Google Scholar 

  25. Genco RJ, Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 2000(62):59–94

    Article  Google Scholar 

  26. Ng N, Kaye EK, Garcia RI (2014) Coffee consumption and periodontal disease in males. J Periodontol 85:1042–1049

    Article  PubMed  Google Scholar 

  27. Riggs BL, Khosla S, Melton LJ 3rd (1998) A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res 13:763–773

    Article  CAS  PubMed  Google Scholar 

  28. Risch HA, Howe GR (1995) Pelvic inflammatory disease and the risk of epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev 4:447–451

    CAS  PubMed  Google Scholar 

  29. Chang WI, Chang JY, Kim YY, Lee G, Kho HS (2011) MUC1 expression in the oral mucosal epithelial cells of the elderly. Arch Oral Biol 56:885–890

    Article  CAS  PubMed  Google Scholar 

  30. Ho SB, Niehans GA, Lyftogt C, Yan PS, Cherwitz DL, Gum ET et al (1993) Heterogeneity of mucin gene expression in normal and neoplastic tissues. Cancer Res 53:641–651

    CAS  PubMed  Google Scholar 

  31. Liu B, Lague JR, Nunes DP, Toselli P, Oppenheim FG, Soares RV et al (2002) Expression of membrane-associated mucins MUC1 and MUC4 in major human salivary glands. J Histochem Cytochem 50:811–820

    Article  CAS  PubMed  Google Scholar 

  32. Li X, Wang L, Nunes DP, Troxler RF, Offner GD (2003) Pro-inflammatory cytokines up-regulate MUC1 gene expression in oral epithelial cells. J Dent Res 82:883–887

    Article  CAS  PubMed  Google Scholar 

  33. Kesavalu L, Chandrasekar B, Ebersole JL (2002) In vivo induction of proinflammatory cytokines in mouse tissue by Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 17:177–180

    Article  CAS  PubMed  Google Scholar 

  34. Rouabhia M, Ross G, Page N, Chakir J (2002) Interleukin-18 and gamma interferon production by oral epithelial cells in response to exposure to Candida albicans or lipopolysaccharide stimulation. Infect Immun 70:7073–7080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Cramer DW, Titus-Ernstoff L, McKolanis JR, Welch WR, Vitonis AF, Berkowitz RS et al (2005) Conditions associated with antibodies against the tumor-associated antigen MUC1 and their relationship to risk for ovarian cancer. Cancer Epidemiol Biomarkers Prev 14:1125–1131

    Article  CAS  PubMed  Google Scholar 

  36. Croce MV, Isla-Larrain MT, Price MR, Segal-Eiras A (2001) Detection of circulating mammary mucin (Muc1) and MUC1 immune complexes (Muc1-CIC) in healthy women Int. J Biol Markers 16:112–120

    CAS  Google Scholar 

  37. Pinheiro SP, Hankinson SE, Tworoger SS, Rosner BA, McKolanis JR, Finn OJ et al (2010) Anti-MUC1 antibodies and ovarian cancer risk: prospective data from the Nurses’ Health Studies. Cancer Epidemiol Biomarkers Prev 19:1595–1601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Kumar R, Burns EA (2008) Age-related decline in immunity: implications for vaccine responsiveness. Expert Rev Vaccines 7:467–479

    Article  PubMed  Google Scholar 

  39. Joshipura KJ, Pitiphat W, Douglass CW (2002) Validation of self-reported periodontal measures among health professionals. J Public Health Dent 62:115–121

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Cancer Institute at the National Institutes of Health (UM1 CA186107, P01 CA87969, 5T32CA009001-38) and the Department of Defense (W81XWH-10-1-0280). We would like to thank the participants and staff of the Nurses’ Health Study for their valuable contributions as well as the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA, WY.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Babic.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Babic, A., Poole, E.M., Terry, K.L. et al. Periodontal bone loss and risk of epithelial ovarian cancer. Cancer Causes Control 26, 941–947 (2015). https://doi.org/10.1007/s10552-015-0575-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-015-0575-7

Keywords

Navigation