Current Oral Health Reports

, Volume 5, Issue 1, pp 33–38 | Cite as

Are Sex Steroid Hormones Influencing Periodontal Conditions? A Systematic Review

  • Aliye AkcalıEmail author
  • Zeynep Akcalı
  • Fareeha Batool
  • Catherine Petit
  • Olivier Huck
Systemic Diseases (N Buduneli, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Systemic Diseases


Purpose of Review

The pulsatile fashion of the release of sex steroid hormones has an impact on periodontium. The aim of this systematic review was to determine whether sex steroid hormones influence periodontal diseases or not.

Recent Findings

MEDLINE via OVID, EMBASE, and the Cochrane Database updated until July 2017 were searched and, particularly, the papers published over the past 5 years were reviewed.


The evidence is more supportive towards the effect of sex steroid hormone perturbations on an existing periodontal disease rather than the initiation of disease. Examination of potential diagnostics for preventive or therapeutic applications is needed in order to decrease the composite risks arising from the hormonal changes themselves. Also, further clinical trials comparing sex steroid hormone exposure on patients with similar baseline periodontal conditions are emerging in order to understand the causal mechanisms between the two, eventually, helping to make clearer clinical recommendations and guidelines for hormone-dominated periods in both men and women.


Estrogens Periodontal diseases Periodontal indexes Progesterone Sex steroid hormones Testosterone 


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ, Beck J, et al. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res. 2012;91(10):914–20. Scholar
  2. 2.
    Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJL, Marcenes W. Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. J Dent Res. 2014;93(11):1045–53. Scholar
  3. 3.
    Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44. Scholar
  4. 4.
    Ferreira MC, Dias-Pereira AC, Branco-de-Almeida LS, Martins CC, Paiva SM. Impact of periodontal disease on quality of life: a systematic review. J Periodontal Res. 2017;79:1560S.Google Scholar
  5. 5.
    Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. J Clin Periodontol. 2013;40:8–19.CrossRefGoogle Scholar
  6. 6.
    Bartold MP, Mariotti A. The future of periodontal-systemic associations: raising the standards. Curr Oral Health Rep. 2017;4(3):258–62. Scholar
  7. 7.
    Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4(1):1–6. Scholar
  8. 8.
    Mascarenhas P, Gapski R, Al-Shammari K, Wang H-L. Influence of sex hormones on the periodontium. J Clin Periodontol. 2003;30(8):671–81. Scholar
  9. 9.
    Shiau HJ, Aichelmann-Reidy ME, Reynolds MA. Influence of sex steroids on inflammation and bone metabolism. Periodontol 2000. 2014;64(1):81–94. Scholar
  10. 10.
    Lyte M. The role of microbial endocrinology in infectious disease. J Endocrinol. 1993;137(3):343–5. Scholar
  11. 11.
    Kumar PS. Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000. 2013;61(1):103–24. Scholar
  12. 12.
    Mariotti A, Mawhinney M. Endocrinology of sex steroid hormones and cell dynamics in the periodontium. Periodontol 2000. 2013;61(1):69–88. Scholar
  13. 13.
    Mombelli A, Rutar A, Lang NP. Correlation of the periodontal status 6 years after puberty with clinical and microbiological conditions during puberty. J Clin Periodontol. 1995;22(4):300–5. Scholar
  14. 14.
    Nakagawa S, Fujii H, Machida Y, Okuda K. A longitudinal study from prepuberty to puberty of gingivitis. Correlation between the occurrence of Prevotella intermedia and sex hormones. J Clin Periodontol. 1994;21(10):658–65. Scholar
  15. 15.
    Koopman JE, van der Kaaij NCW, Buijs MJ, Elyassi Y, van der Veen MH, Crielaard W, et al. The effect of fixed orthodontic appliances and fluoride mouthwash on the oral microbiome of adolescents—a randomized controlled clinical trial. PLoS One. 2015;10(9):e0137318. Scholar
  16. 16.
    Shourie V, Dwarakanath CD, Prashanth GV, Alampalli RV, Padmanabhan S, Bali S. The effect of menstrual cycle on periodontal health—a clinical and microbiological study. Oral Health Prev Dent. 2012;10(2):185–92.PubMedGoogle Scholar
  17. 17.
    Balan U, Gonsalves N, Jose M, Girish KL. Symptomatic changes of oral mucosa during normal hormonal turnover in healthy young menstruating women. J Contemp Dent Pract. 2012;13(2):178–81.CrossRefPubMedGoogle Scholar
  18. 18.
    Kawamoto A, Sugano N, Motohashi M, Matsumoto S, Ito K. Relationship between oral malodor and the menstrual cycle. J Periodontal Res. 2010;45(5):681–7. Scholar
  19. 19.
    Fischer CC, Persson RE, Persson GR. Influence of the menstrual cycle on the oral microbial flora in women: a case-control study including men as control subjects. J Periodontol. 2008;79(10):1966–73. Scholar
  20. 20.
    Lindhe J, Brånemark PI. Changes in vascular permeability after local application of sex hormones. J Periodont Res. 1967;2(4):259–65. Scholar
  21. 21.
    Baser U, Cekici A, Tanrikulu-Kucuk S, Kantarci A, Ademoglu E, Yalcin F. Gingival inflammation and interleukin-1 beta and tumor necrosis factor-alpha levels in gingival crevicular fluid during the menstrual cycle. J Periodontol. 2009;80(12):1983–90. Scholar
  22. 22.
    Becerik S, Özçaka Ö, Nalbantsoy A, Atilla G, Celec P, Behuliak M, et al. Effects of menstrual cycle on periodontal health and gingival crevicular fluid markers. J Periodontol. 2010;81(5):673–81. Scholar
  23. 23.
    Markou E, Boura E, Tsalikis L, Deligianidis A, Konstantinidis A. The influence of sex hormones on proinflammatory cytokines in gingiva of periodontally healthy premenopausal women. J Periodontal Res. 2011;46(5):528–32. Scholar
  24. 24.
    Khosravisamani M, Maliji G, Seyfi S, Azadmehr A, Abd Nikfarjam B, Madadi S, et al. Effect of the menstrual cycle on inflammatory cytokines in the periodontium. J Periodontal Res. 2014;49(6):770–6. Scholar
  25. 25.
    • Rathore S, Khuller N, Dev YP, Singh P, Basavaraj P, Gera K. Effects of scaling and root planing on gingival status during menstrual cycle—a cross-sectional analytical study. J Clin Diagn Res. 2015;9:35–9. The manuscript demonstrates the beneficial effects of non-surgical periodontal treatment on females during the menstrual cycle. Google Scholar
  26. 26.
    Grady D. Clinical practice. Management of menopausal symptoms. N Engl J Med. 2006;355(22):2338–47. Scholar
  27. 27.
    Marjoribanks J, Farquhar C, Roberts H, Lethaby A, Lee J. Long-term hormone therapy for perimenopausal and postmenopausal women. Farquhar C, editor. Cochrane Database Syst Rev. 2017;1:CD004143.Google Scholar
  28. 28.
    Karsenty G. The mutual dependence between bone and gonads. J Endocrinol. 2012;213(2):107–14. Scholar
  29. 29.
    Sophia K, Suresh S, Sudhakar U, Jayakumar P, Mathew D. Comparative analysis of salivary alkaline phosphatase in post menopausal women with and without periodontitis. J Clin Diagn Res. 2017;11:122–4.CrossRefGoogle Scholar
  30. 30.
    Babür C, Ozcan G, Cebi DU, Pervane B, Ozdemir B, Yücel A, et al. Gingival crevicular fluid levels of osteoprotegerin (OPG) in premenopausal and postmenopausal women with or without chronic periodontitis. J Dent. 2012;40(5):364–71. Scholar
  31. 31.
    Millen AE, Andrews CA, LaMonte MJ, Hovey KM, Swanson M, Genco RJ, et al. Vitamin D status and 5-year changes in periodontal disease measures among postmenopausal women: the Buffalo OsteoPerio Study. J Periodontol. 2014;85(10):1321–32. Scholar
  32. 32.
    Singh A, Sharma RK, Siwach RC, Tewari S, Narula SC. Association of bone mineral density with periodontal status in postmenopausal women. J Investig Clin Dent. 2014;5(4):275–82. Scholar
  33. 33.
    Alves RC, Félix SA, Rodriguez-Archilla A, Oliveira P, Brito J, Santos Dos JM. Relationship between menopause and periodontal disease: a cross-sectional study in a Portuguese population. Int J Clin Exp Med. 2015;8(7):11412–9.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Savić Pavičin I, Dumančić J, Jukić T, Badel T. The relationship between periodontal disease, tooth loss and decreased skeletal bone mineral density in ageing women. Gerodontology. 2017;85:596.Google Scholar
  35. 35.
    Maier AW, Orban B. Gingivitis in pregnancy. Oral Surg Oral Med Oral Pathol. 1949;2(3):334–73. Scholar
  36. 36.
    •• Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand. 1963;21(6):533–551. This manuscript represents pregnancy as a modifier in periodontal disease sex steroid hormone association. Scholar
  37. 37.
    Figuero E, Carrillo-de-Albornoz A, Martin C, Tobías A, Herrera D. Effect of pregnancy on gingival inflammation in systemically healthy women: a systematic review. J Clin Periodontol. 2013;40(5):457–73. Scholar
  38. 38.
    Daalderop LA, Wieland BV, Tomsin K, Reyes L, Kramer BW, Vanterpool SF, et al. Periodontal disease and pregnancy outcomes: overview of systematic reviews. JDR Clin Transl Res. 2017;122:238008441773109–18.Google Scholar
  39. 39.
    Gürsoy M, Gursoy UK, Sorsa T, Pajukanta R, Könönen E. High salivary estrogen and risk of developing pregnancy gingivitis. J Periodontol. 2013;84(9):1281–9. Scholar
  40. 40.
    Machado FC, Cesar DE, Apolônio ACM, Ribeiro LC, Ribeiro RA. Longitudinal study on clinical and microbial analysis of periodontal status in pregnancy. Braz Oral Res. 2016;30:e87.PubMedGoogle Scholar
  41. 41.
    • González-Jaranay M, Téllez L, Roa-López A, Gómez-Moreno G, Moreu G. Periodontal status during pregnancy and postpartum. PLoS One. 2017;12(5):e0178234. The manuscript demonstrates transitional effect of sex steroid hormones during pregnancy. Scholar
  42. 42.
    Mishra PS, Marawar PP, Mishra SS. A cross-sectional, clinical study to evaluate mobility of teeth during pregnancy using periotest. Indian J Dent Res. 2017;28(1):10–5. Scholar
  43. 43.
    Gümüş P, Emingil G, Öztürk V-Ö, Belibasakis GN, Bostanci N. Oxidative stress markers in saliva and periodontal disease status: modulation during pregnancy and postpartum. BMC Infect Dis. 2015;15(1):261. Scholar
  44. 44.
    Gümüş P, Öztürk VÖ, Bozkurt E, Emingil G. Evaluation of the gingival inflammation in pregnancy and postpartum via 25-hydroxy-vitamin D3, prostaglandin E2 and TNF-α levels in saliva. Arch Oral Biol. 2016;63:1–6. Scholar
  45. 45.
    Wu M, Chen S-W, Su W-L, Zhu H-Y, Ouyang S-Y, Cao Y-T, et al. Sex hormones enhance gingival inflammation without affecting IL-1β and TNF-α in periodontally healthy women during pregnancy. Mediat Inflamm. 2016;2016:4897890–6.Google Scholar
  46. 46.
    Otenio CCM, Fonseca I, Martins MF, Ribeiro LC, Assis NMSP, Ferreira AP, et al. Expression of IL-1β, IL-6, TNF-α, and iNOS in pregnant women with periodontal disease. Genet Mol Res. 2012;11(4):4468–78. Scholar
  47. 47.
    Borgo PV, Rodrigues VAA, Feitosa ACR, Xavier KCB, Ávila-Campos MJ. Association between periodontal condition and subgingival microbiota in women during pregnancy: a longitudinal study. J Appl Oral Sci. 2014;22(6):528–33. Scholar
  48. 48.
    Usin MM, Tabares SM, Parodi RJ, Sembaj A. Periodontal conditions during the pregnancy associated with periodontal pathogens. J Investig Clin Dent. 2013;4(1):54–9. Scholar
  49. 49.
    Gogeneni H, Budunelİ N, Ceyhan-Öztürk B, Gümüş P, Akcali A, Zeller I, et al. Increased infection with key periodontal pathogens during gestational diabetes mellitus. J Clin Periodontol. 2015;42(6):506–12. Scholar
  50. 50.
    Geisinger ML, Geurs NC, Bain JL, Kaur M, Vassilopoulos PJ, Cliver SP, et al. Oral health education and therapy reduces gingivitis during pregnancy. J Clin Periodontol. 2014;41(2):141–8. Scholar
  51. 51.
    Penova-Veselinovic B, Keelan JA, Wang CA, Newnham JP, Pennell CE. Changes in inflammatory mediators in gingival crevicular fluid following periodontal disease treatment in pregnancy: relationship to adverse pregnancy outcome. J Reprod Immunol. 2015;112:1–10. Scholar
  52. 52.
    Chiga S, Ohba T, Miyoshi J, Tanoue D, Kawase H, Katoh T, et al. Oral health status of pregnant women in Kumamoto Prefecture. Nihon Eiseigaku Zasshi. 2015;70(2):167–72. Scholar
  53. 53.
    Chen L, Lu H-X, Wei T-Y, Feng X-P. Multiple factors analysis of periodontal status in pregnant women in Shanghai. Shanghai Kou Qiang Yi Xue. 2014;23(4):452–6.PubMedGoogle Scholar
  54. 54.
    Cohen L, Schaeffer M, Davideau J-L, Tenenbaum H, Huck O. Obstetrician’s knowledge, attitude and behavior concerning periodontal diseases and treatment needs in pregnant women: situation and influencing factors in France. J Periodontol. 2015;86(3):398–405. Scholar
  55. 55.
    Wiener RC, Wiener-Pla R. Literacy, pregnancy and potential oral health changes: the Internet and readability levels. Matern Child Health. 2014;18(3):657–62. Scholar
  56. 56.
    Basaria S. Reproductive aging in men. Endocrinol Metab Clin N Am. 2013;42(2):255–70. Scholar
  57. 57.
    Orwoll ES, Chan BKS, Lambert LC, Marshall LM, Lewis C, Phipps KR. Sex steroids, periodontal health, and tooth loss in older men. J Dent Res. 2009;88(8):704–8. Scholar
  58. 58.
    Samietz S, Holtfreter B, Friedrich N, Mundt T, Hoffmann W, Völzke H, et al. Prospective association of sex steroid concentrations with periodontal progression and incident tooth loss. J Clin Periodontol. 2016;43(1):10–8. Scholar
  59. 59.
    Daltaban O, Saygun I, Bolu E. Periodontal status in men with hypergonadotropic hypogonadism: effects of testosterone deficiency. J Periodontol. 2006;77(7):1179–83. Scholar
  60. 60.
    Steffens JP, Wang X, Starr JR, Spolidório LC, Van Dyke TE, Kantarci A. Associations between sex hormone levels and periodontitis in men: results from NHANES III. J Periodontol. 2015;86(10):1116–25. Scholar
  61. 61.
    Vandenput L, Mellström D, Laughlin GA, Cawthon PM, Cauley JA, Hoffman AR, et al. Low testosterone, but not estradiol, is associated with incident falls in older men: the international MrOS study. J Bone Miner Res. 2017;32(6):1174–81. Scholar
  62. 62.
    Singh BP, Makker A, Tripathi A, Singh MM, Gupta V. Association of testosterone and bone mineral density with tooth loss in men with chronic periodontitis. J Oral Sci. 2011;53(3):333–9. Scholar
  63. 63.
    Meisel P, Reifenberger J, Haase R, Nauck M, Bandt C, Kocher T. Women are periodontally healthier than men, but why don’t they have more teeth than men? Menopause. 2008;15(2):270–5. Scholar
  64. 64.
    Kellesarian SV, Malmstrom H, Abduljabbar T, Vohra F, Kellesarian TV, Javed F, et al. Low testosterone levels in body fluids are associated with chronic periodontitis. Am J Mens Health. 2017;11(2):443–53. Scholar
  65. 65.
    Edelman A, Micks E, Gallo MF, Jensen JT, Grimes DA. Continuous or extended cycle vs. cyclic use of combined hormonal contraceptives for contraception. Cochrane Database Syst Rev. 2014;68:CD004695.Google Scholar
  66. 66.
    Taichman LS, Eklund SA. Oral contraceptives and periodontal diseases: rethinking the association based upon analysis of National Health and Nutrition Examination Survey data. J Periodontol. 2005;76(8):1374–85. Scholar
  67. 67.
    Haerian-Ardakani A, Moeintaghavi A, Talebi-Ardakani MR, Sohrabi K, Bahmani S, Dargahi M. The association between current low-dose oral contraceptive pills and periodontal health: a matched-case-control study. J Contemp Dent Pract. 2010;11(3):033–40.PubMedGoogle Scholar
  68. 68.
    Brusca MI, Rosa A, Albaina O, Moragues MD, Verdugo F, Pontón J. The impact of oral contraceptives on women’s periodontal health and the subgingival occurrence of aggressive periodontopathogens and Candida species. J Periodontol. 2010;81(7):1010–8. Scholar
  69. 69.
    Domingues RS, Ferraz BFR, Greghi SLA, de Rezende MLR, Passanezi E, Sant'Ana ACP. Influence of combined oral contraceptives on the periodontal condition. J Appl Oral Sci. 2012;20(2):253–9. Scholar
  70. 70.
    Aminzadeh A, Sabeti Sanat A, Nik Akhtar S. Frequency of candidiasis and colonization of Candida albicans in relation to oral contraceptive pills. Iran Red Crescent Med J. 2016;18:e38909.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Preshaw PM. Oral contraceptives and the periodontium. Periodontol 2000. 2013;61(1):125–59. Scholar
  72. 72.
    Xu X, Zhao Q, Yang S, Fu G, Chen Y. A new approach to accelerate orthodontic tooth movement in women: orthodontic force application after ovulation. Med Hypotheses. 2010;75(4):405–7. Scholar
  73. 73.
    Akcalı A, Bostanci N, Özçaka Ö, Öztürk Ceyhan B, Gümüş P, Budunel İN, et al. Association between polycystic ovary syndrome, oral microbiota and systemic antibody responses. PLoS One. 2014;9(9):e108074. Scholar
  74. 74.
    Akcalı A, Bostanci N, Özçaka Ö, Gümüş P, Öztürk Ceyhan B, Tervahartiala T, et al. Gingival inflammation and salivary or serum granulocyte secreted enzymes in patients with polycystic ovary syndrome. J Periodontol. 2017;9:1–10.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Aliye Akcalı
    • 1
    • 2
    Email author
  • Zeynep Akcalı
    • 3
  • Fareeha Batool
    • 4
  • Catherine Petit
    • 4
    • 5
  • Olivier Huck
    • 4
    • 5
  1. 1.Department of Periodontology, School of DentistryUniversity of Witten/HerdeckeWittenGermany
  2. 2.Centre for Oral Clinical Research, Institute of Dentistry, Barts and The London School of Medicine and DentistryQueen Mary University of London (QMUL)LondonUK
  3. 3.Department of Internal MedicineHavran Government HospitalBalıkesirTurkey
  4. 4.Department of Periodontology, Faculté de Chirurgie DentaireUniversité de StrasbourgStrasbourgFrance
  5. 5.INSERM 1260 Regenerative NanomedicineFédération de Médecine Translationnelle de Strasbourg (FMTS)StrasbourgFrance

Personalised recommendations