Gestational diabetes alters subgingival pathobiont composition
DOI:
https://doi.org/10.2340/aos.v85.45789Keywords:
pregnancy, gestational diabetes mellitus, subgingival pathobionts, periodontal inflammationAbstract
Objective: This cross-sectional study assesses the relationship between gestational diabetes mellitus (GDM) and periodontal dysbiosis by evaluating specific periodontal pathobionts (Porphyromonas gingivalis, Prevotella intermedia, Tannerella forsythia, and Treponema denticola), clinical periodontal parameters, and periodontal inflamed surface area (PISA).
Materials and methods: 101 GDM and 98 non-GDM women of 16–36 weeks gestation were included. Clinical periodontal parameters were measured, and PISA values calculated. Subgingival plaque samples, collected from the deepest pockets, were analyzed, to assess the amount of periodontopathogens. Associations were assessed using binary logistic regression and path analysis.
Results: The GDM group showed higher clinical parameters and PISA values (p < 0.001). While P. gingivalis levels were similar in both groups (p = 0.924) and unrelated to the presence of GDM in path analysis (p = 0.055), P. intermedia and T. denticola levels were found higher in the non-GDM group (p < 0.05, p < 0.001) and negatively associated with the presence of GDM (p < 0.001, p = 0.002). P. intermedia increased with gestation week (p = 0.044). Elevated T. forsythia levels were observed to increase GDM risk 1.208-fold in regression analysis (p = 0.002).
Conclusion: Increasing sex hormone levels accompanied by the presence of GDM may alter subgingival pathobiont composition. In patients with GDM, there is a heightened burden of T. forsythia in subgingival zones, where P. intermedia finds less favorable conditions.
Downloads
References
Hajishengallis G, Lamont RJ. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol. 2012;27(6):409–19.
https://doi.org/10.1111/j.2041-1014.2012.00663.x DOI: https://doi.org/10.1111/j.2041-1014.2012.00663.x
Suarez LJ, Garzon H, Arboleda S, Rodriguez A. Oral dysbiosis and autoimmunity: from local periodontal responses to an imbalanced systemic immunity. A review. Front Immunol. 2020;11:591255.
https://doi.org/10.3389/fimmu.2020.591255 DOI: https://doi.org/10.3389/fimmu.2020.591255
Bascones-Martinez A, Gonzalez-Febles J, Sanz-Esporrin J. Diabetes and periodontal disease. Review of the literature. Am J Dent. 2014;27(2):63–7.
Negrato CA, Tarzia O, Jovanovic L, Chinellato LE. Periodontal disease and diabetes mellitus. J Appl Oral Sci. 2013;21(1):1–12.
https://doi.org/10.1590/1678-7757201302106 DOI: https://doi.org/10.1590/1678-7757201302106
Sima C, Glogauer M. Diabetes mellitus and periodontal diseases. Curr Diab Rep. 2013;13(3):445–52.
https://doi.org/10.1007/s11892-013-0367-y DOI: https://doi.org/10.1007/s11892-013-0367-y
Buchanan TA, Xiang A, Kjos SL, Watanabe R. What is gestational diabetes? Diabetes Care. 2007;30 Suppl 2:S105–11. DOI: https://doi.org/10.2337/dc07-s201
Barbour LA, McCurdy CE, Hernandez TL, Kirwan JP, Catalano PM, Friedman JE. Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes. Diabetes Care. 2007;30 Suppl 2:S112–9.
https://doi.org/10.2337/dc07-s202 DOI: https://doi.org/10.2337/dc07-s202
Best LG, Saxena R, Anderson CM, Barnes MR, Hakonarson H, Falcon G, et al. Two variants of the C-reactive protein gene are associated with risk of pre-eclampsia in an American Indian population. PLoS One. 2013;8(8):e71231. DOI: https://doi.org/10.1371/journal.pone.0071231
Wang H, Li N, Chivese T, Werfalli M, Sun H, Yuen L, et al. IDF diabetes atlas: estimation of global and regional gestational diabetes mellitus prevalence for 2021 by International Association of Diabetes in Pregnancy Study Group’s Criteria. Diabetes Res Clin Pract. 2022;183:109050.
https://doi.org/10.1016/j.diabres.2021.109050 DOI: https://doi.org/10.1016/j.diabres.2021.109050
Zachariasen RD. Ovarian hormones and oral health: pregnancy gingivitis. Compendium. 1989;10(9):508–12.
Mariotti A. Sex steroid hormones and cell dynamics in the periodontium. Crit Rev Oral Biol Med. 1994;5(1):27–53.
https://doi.org/10.1177/10454411940050010201 DOI: https://doi.org/10.1177/10454411940050010201
Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand. 1963;21:533–51.
https://doi.org/10.3109/00016356309011240 DOI: https://doi.org/10.3109/00016356309011240
Miyazaki H, Yamashita Y, Shirahama R, Goto-Kimura K, Shimada N, Sogame A, et al. Periodontal condition of pregnant women assessed by CPITN. J Clin Periodontol. 1991;18(10):751–4.
https://doi.org/10.1111/j.1600-051X.1991.tb00067.x DOI: https://doi.org/10.1111/j.1600-051X.1991.tb00067.x
Carrillo-de-Albornoz A, Figuero E, Herrera D, Cuesta P, Bascones-Martinez A. Gingival changes during pregnancy: III. Impact of clinical, microbiological, immunological and socio-demographic factors on gingival inflammation. J Clin Periodontol. 2012;39(3):272–83.
https://doi.org/10.1111/j.1600-051X.2011.01800.x DOI: https://doi.org/10.1111/j.1600-051X.2011.01800.x
Offenbacher S, Jared HL, O’Reilly PG, Wells SR, Salvi GE, Lawrence HP, et al. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Ann Periodontol. 1998;3(1):233–50.
https://doi.org/10.1902/annals.1998.3.1.233 DOI: https://doi.org/10.1902/annals.1998.3.1.233
Cassini MA, Pilloni A, Condo SG, Vitali LA, Pasquantonio G, Cerroni L. Periodontal bacteria in the genital tract: are they related to adverse pregnancy outcome? Int J Immunopathol Pharmacol. 2013;26(4):931–9.
https://doi.org/10.1177/039463201302600411 DOI: https://doi.org/10.1177/039463201302600411
Ercan E, Eratalay K, Deren O, Gur D, Ozyuncu O, Altun B, et al. Evaluation of periodontal pathogens in amniotic fluid and the role of periodontal disease in pre-term birth and low birth weight. Acta Odontol Scand. 2013;71(3–4):553–9.
https://doi.org/10.3109/00016357.2012.697576 DOI: https://doi.org/10.3109/00016357.2012.697576
Kornman KS, Loesche WJ. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun. 1982;35(1):256–63.
https://doi.org/10.1128/iai.35.1.256-263.1982 DOI: https://doi.org/10.1128/iai.35.1.256-263.1982
Gursoy M, Haraldsson G, Hyvonen M, Sorsa T, Pajukanta R, Kononen E. Does the frequency of Prevotella intermedia increase during pregnancy? Oral Microbiol Immunol. 2009;24(4):299–303. DOI: https://doi.org/10.1111/j.1399-302X.2009.00509.x
Borgo PV, Rodrigues VA, Feitosa AC, Xavier KC, Avila-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.
https://doi.org/10.1590/1678-775720140164 DOI: https://doi.org/10.1590/1678-775720140164
Jelihovschi I, Dorneanu O, Badescu A, Serban R, Ursu RG, Martu IA, et al. Increased detection rate of Prevotella Intermedia among pregnant periodontitis patients in Romania. Biomed J Sci Tech Res. 2018;2(10.26717).
https://doi.org/10.26717/BJSTR.2017.01.000646 DOI: https://doi.org/10.26717/BJSTR.2017.01.000646
Raber-Durlacher JE, Leene W, Palmer-Bouva CC, Raber J, Abraham-Inpijn L. Experimental gingivitis during pregnancy and post-partum: immunohistochemical aspects. J Periodontol. 1993;64(3):211–8.
https://doi.org/10.1902/jop.1993.64.3.211 DOI: https://doi.org/10.1902/jop.1993.64.3.211
Sharma A. Virulence mechanisms of Tannerella forsythia. Periodontol 2000. 2010;54(1):106–16.
https://doi.org/10.1111/j.1600-0757.2009.00332.x DOI: https://doi.org/10.1111/j.1600-0757.2009.00332.x
Wang Y, Cupul-Uicab LA, Rogan WJ, Eggesbo M, Travlos G, Wilson R, et al. Recreational exercise before and during pregnancy in relation to plasma C-reactive protein concentrations in pregnant women. J Phys Act Health. 2015;12(6):770–5.
https://doi.org/10.1123/jpah.2013-0390 DOI: https://doi.org/10.1123/jpah.2013-0390
Fardini Y, Chung P, Dumm R, Joshi N, Han YW. Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect Immun. 2010;78(4):1789–96.
https://doi.org/10.1128/IAI.01395-09 DOI: https://doi.org/10.1128/IAI.01395-09
Tellapragada C, Eshwara VK, Acharya S, Bhat P, Kamath A, Vishwanath S, et al. Prevalence of clinical periodontitis and putative periodontal pathogens among south indian pregnant women. Int J Microbiol. 2014;2014:420149.
https://doi.org/10.1155/2014/420149 DOI: https://doi.org/10.1155/2014/420149
Carta G, Persia G, Falciglia K, Iovenitti P. Periodontal disease and poor obstetrical outcome. Clin Exp Obstet Gynecol. 2004;31(1):47–9.
Garcia-Martos JM, Valverde-Bolivar FJ, Campillo-Lopez MT, Delgado-Rodriguez M. Association between periodontal disease and gestational diabetes: systematic review and meta-analysis. Prim Care Diabetes. 2025;19(1):1–6.
https://doi.org/10.1016/j.pcd.2024.11.003 DOI: https://doi.org/10.1016/j.pcd.2024.11.003
von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370(9596):1453–7.
https://doi.org/10.1016/S0140-6736(07)61602-X DOI: https://doi.org/10.1016/S0140-6736(07)61602-X
O’Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol. 1972;43(1):38.
https://doi.org/10.1902/jop.1972.43.1.38 DOI: https://doi.org/10.1902/jop.1972.43.1.38
Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975;25(4):229–35.
Nesse W, Abbas F, van der Ploeg I, Spijkervet FK, Dijkstra PU, Vissink A. Periodontal inflamed surface area: quantifying inflammatory burden. J Clin Periodontol. 2008;35(8):668–73.
https://doi.org/10.1111/j.1600-051X.2008.01249.x DOI: https://doi.org/10.1111/j.1600-051X.2008.01249.x
Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Periodontol. 2018;89 Suppl 1:S159–72. DOI: https://doi.org/10.1002/JPER.18-0006
Gogeneni H, Buduneli N, Ceyhan-Ozturk B, Gumus 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.
https://doi.org/10.1111/jcpe.12418 DOI: https://doi.org/10.1111/jcpe.12418
Ganiger K, Sridharan S, Rahul A, Satyanarayana A. Quantitative analysis of key periodontopathic bacteria in gestational diabetic and non-diabetic women. J Diabetes Metab Disord. 2019;18(2):363–9.
https://doi.org/10.1007/s40200-019-00420-3 DOI: https://doi.org/10.1007/s40200-019-00420-3
Figuero E, Carrillo-de-Albornoz A, Herrera D, Bascones-Martinez A. Gingival changes during pregnancy: I. Influence of hormonal variations on clinical and immunological parameters. J Clin Periodontol. 2010;37(3):220–9.
https://doi.org/10.1111/j.1600-051X.2009.01516.x DOI: https://doi.org/10.1111/j.1600-051X.2009.01516.x
Carrillo-de-Albornoz A, Figuero E, Herrera D, Bascones-Martinez A. Gingival changes during pregnancy: II. Influence of hormonal variations on the subgingival biofilm. J Clin Periodontol. 2010;37(3):230–40.
https://doi.org/10.1111/j.1600-051X.2009.01514.x DOI: https://doi.org/10.1111/j.1600-051X.2009.01514.x
Li Y, Ren X, He L, Li J, Zhang S, Chen W. Maternal age and the risk of gestational diabetes mellitus: a systematic review and meta-analysis of over 120 million participants. Diabetes Res Clin Pract. 2020;162:108044. DOI: https://doi.org/10.1016/j.diabres.2020.108044
Lappe V, Greiner GG, Linnenkamp U, Viehmann A, Adamczewski H, Kaltheuner M, et al. Gestational diabetes in Germany-prevalence, trend during the past decade and utilization of follow-up care: an observational study. Sci Rep. 2023;13(1):16157.
https://doi.org/10.1038/s41598-023-43382-6 DOI: https://doi.org/10.1038/s41598-023-43382-6
World Health Organization. A healthy lifestyle – WHO recommendations. 2010. Available from: https://www.who.int/europe/news-room/fact-sheets/item/a-healthy-lifestyle---who-recommendations
Yilmaz D, Altas A. Evaluation of gingival microcirculation in patients with gestational diabetes mellitus. Microvasc Res. 2021;138:104222.
https://doi.org/10.1016/j.mvr.2021.104222 DOI: https://doi.org/10.1016/j.mvr.2021.104222
Hajishengallis G. The inflammophilic character of the periodontitis-associated microbiota. Mol Oral Microbiol. 2014;29(6):248–57.
https://doi.org/10.1111/omi.12065 DOI: https://doi.org/10.1111/omi.12065
Dasanayake AP, Chhun N, Tanner AC, Craig RG, Lee MJ, Moore AF, et al. Periodontal pathogens and gestational diabetes mellitus. J Dent Res. 2008;87(4):328–33.
https://doi.org/10.1177/154405910808700421 DOI: https://doi.org/10.1177/154405910808700421
Keshavarz M, Cheung NW, Babaee GR, Moghadam HK, Ajami ME, Shariati M. Gestational diabetes in Iran: incidence, risk factors and pregnancy outcomes. Diabetes Res Clin Pract. 2005;69(3):279–86. DOI: https://doi.org/10.1016/j.diabres.2005.01.011
Xiong X, Elkind-Hirsch KE, Vastardis S, Delarosa RL, Pridjian G, Buekens P. Periodontal disease is associated with gestational diabetes mellitus: a case-control study. J Periodontol. 2009;80(11):1742–9.
https://doi.org/10.1902/jop.2009.090250 DOI: https://doi.org/10.1902/jop.2009.090250
Jensen J, Liljemark W, Bloomquist C. The effect of female sex hormones on subgingival plaque. J Periodontol. 1981;52(10):599–602.
https://doi.org/10.1902/jop.1981.52.10.599 DOI: https://doi.org/10.1902/jop.1981.52.10.599
Muramatsu Y, Takaesu Y. Oral health status related to subgingival bacterial flora and sex hormones in saliva during pregnancy. Bull Tokyo Dent Coll. 1994;35(3):139–51.
Akherati M, Shafaei E, Salehiniya H, Abbaszadeh H. Comparison of the frequency of periodontal pathogenic species of diabetics and non-diabetics and its relation to periodontitis severity, glycemic control and body mass index. Clin Exp Dent Res. 2021;7(6):1080–8.
https://doi.org/10.1002/cre2.453 DOI: https://doi.org/10.1002/cre2.453
Sakallioglu EE, Lutfioglu M, Sakallioglu U, Diraman E, Keskiner I. Fluid dynamics of gingiva in diabetic and systemically healthy periodontitis patients. Arch Oral Biol. 2008;53(7):646–51.
https://doi.org/10.1016/j.archoralbio.2007.12.013 DOI: https://doi.org/10.1016/j.archoralbio.2007.12.013
BieleckiM, Antonyuk S, Strange RW, Smalley JW, Mackiewicz P, Smiga M, et al. Tannerella forsythia Tfo belongs to Porphyromonas gingivalis HmuY-like family of proteins but differs in heme-binding properties. Biosci Rep. 2018;38(5):BSR20181325
https://doi.org/10.1042/BSR20181325 DOI: https://doi.org/10.1042/BSR20181325
Chaparro A, Zuniga E, Varas-Godoy M, Albers D, Ramirez V, Hernandez M, et al. Periodontitis and placental growth factor in oral fluids are early pregnancy predictors of gestational diabetes mellitus. J Periodontol. 2018;89(9):1052–60.
https://doi.org/10.1002/JPER.17-0497 DOI: https://doi.org/10.1002/JPER.17-0497

Acta Odontologica Scandinavica publishes original research papers as well as critical reviews relevant to the diagnosis, epidemiology, health service, prevention, aetiology, pathogenesis, pathology, physiology, microbiology, development and treatment of diseases affecting tissues of the oral cavity and associated structures including papers on cause and effect or explanatory/associative relationships for experimental or observational studies.