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Obstetrics and Gynegology2022№4
Periodontal diseases and their association...

Periodontal diseases and their association with unwanted pregnancy outcomes

DOI
https://dx.doi.org/10.18565/aig.2022.4.26-33

Burduli A.G., Balmasova I.P., Tsarev V.N., Arutyunov S.D.

1) Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology, and Perinatology, Ministry of Health of the Russian Federation, Moscow, Russia; 2) A.I. Evdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of the Russian Federation,Moscow, Russia; 3) Peoples’ Friendship University of Russia, Ministry of Science and Higher Education of the Russian Federation (RUDN University), Moscow, Russia
Periodontal diseases are among the most common in the world and are a risk factor for a large number of systemic pathological processes. These systemic conditions currently include unwanted pregnancy outcomes. This review is devoted to the analysis of the etiopathogenetic mechanisms of a relationship between periodontal diseases and unwanted pregnancy outcomes.
Publications in recent years on a given topic were analyzed.
Most researchers currently consider that the key factor that links periodontal diseases with systemic disease is the ability of a number of periodontal pathogenic bacteria to persist in the body, which reach distant organs and tissues, inducing a pronounced inflammatory response not only at the local, but also at the systemic level. In pregnant women, the incidence of periodontal diseases amounts to as much as 40% and is accompanied by a significant increase in that of preterm birth, premature rupture of membranes, low fetal weight, preeclampsia, and other adverse events. The basis for these impairments in the course of the gestational process is the development of inflammatory reactions that accompany periodontitis and become systemic with time. Inflammation in turn provokes birth activity. In addition, the appearance of periodontal pathogenic bacteria in the placenta and amniotic fluid was recorded in periodontitis diseases, which affects fetal development. Among the periodontal pathogens in these cases, Porphyromonas gingivalis prevails with its unique set of virulence factors, the ability to affect macrophages intracellularly and to induce the autoimmune processes accompanied by the production of specific cardiolipin antibodies.
Conclusion: The investigation has found a relationship between periodontal diseases and adverse pregnancy outcomes due to the unity of a number of etiopathogenetic mechanisms. The presence of these phenomena creates a prospect for prevention of unwanted pregnancy outcomes through measures aimed at treating periodontal diseases.

Keywords

pregnancy
unwanted pregnancy outcomes
periodontal diseases
periodontal pathogenic bacteria
inflammation
Full text (in Russian)

References

  1. Hajishengallis G., Darveau R.P., Curtis M.A. The keystone-pathogen hypothesis. Nat. Rev. Microbiol. 2012; 10(10): 717-25. https://dx.doi.org/10.1038/nrmicro2873.
  2. Лепеева Н.А., Ермолаева Л.А., Шишкин А.Н. Состояние тканей пародонта у больных метаболическим синдромом. Вестник Санкт-Петербургского университета. 2012; 11(3): 145-52. [Lepeeva N.A., Ermolaeva L.A., Shishkin A.N. The state of periodontal tissues in patients with metabolic syndrome. Bulletin of St. Petersburg University. 2012; 11(3): 145-52. (in Russian)].
  3. Балмасова И.П., Царёв В.Н., Янушевич О.О., Маев И.В., Мкртумян А.М., Арутюнов С.Д. Микроэкология пародонта. Взаимосвязь локальных и системных эффектов. М.: Практическая медицина; 2021.264 с. [Balmasova I.P., Tsarev V.N., Yanushevich O.O. et al. Microecology of periodontal disease. The relationship of local and systemic effects. M.: Practical Medicine; 2021. 264 p. (in Russian)].
  4. Bui F.Q., Almeida-da-Silva C.L.C., Huynh B., Trinh A., Liu J., Woodward J. et al. Association between periodontal pathogens and systemic disease. Biomed. J. 2019; 42(1): 27-35. https://dx.doi.org/10.1016/j.bj.2018.12.001.
  5. Bostanci N., Belibasakis G.N. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol. Lett. 2012; 331(1): 1-9. https://dx.doi.org/10.1111/j.1574-6968.2012.02579.x.
  6. Cullinan M.P., Seymour G.J. Periodontal disease and systemic illness: will the evidence ever be enough? Periodontol 2000. 2013; 62(1): 271-86. https://dx.doi.org/10.1111/prd.12007.
  7. Goldenberg R.L., Culhane J.F., Iams J.D., Romero R. Epidemiology and causes of preterm birth. Lancet. 2008; 371(9606): 75-84. https://dx.doi.org/10.1016/S0140-6736(08)60074-4.
  8. Dasanayake A. Poor periodontal health of the pregnant woman as a risk factor for low birth weight. Ann. Periodontol. 1998; 3(1): 206-12. https://dx.doi.org/10.1902/annals.1998.3.1.206.
  9. Mercer B.M. Preterm premature rupture of the membranes: diagnosis and management. Obstet. Gynecol. 2003; 101(1): 178-93. https://dx.doi.org/10.1016/j.clp.2004.06.004.
  10. Figuero E., Carrillo‐de‐Albornoz A., Martín C., Tobías A., Herrera D. Effect of pregnancy on gingival inflammation in systematically healthy women: a systematic review. J. Clin. Periodontol. 2013; 40(5): 457‐73. https://dx.doi.org/10.1111/jcpe.12053.
  11. Lopez N.J., Smith P.C., Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. J. Periodontol. 2002; 73(8): 911-24. https://dx.doi.org/10.1902/jop.2002.73.8.911.
  12. Ide M., Papapanou P.N. Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes – systematic review. J. Clin. Periodontol. 2013; 84(4, Suppl.): 181‐94. https://dx.doi.org/10.1902/jop.2013.134009.
  13. Boggess K.A., Lieff S., Murtha A.P., Moss K., Beck J., Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet. Gynecol. 2003; 101(2): 227‐31. https://dx.doi.org/10.1016/s0029-7844(02)02314-1.
  14. Xiong X., Buekens P., Vastardis S., Yu S.M. Periodontal disease and pregnancy outcomes: state-of‐the‐science. Obstet. Gynecol. Surv. 2007; 62(9): 605‐15. https://dx.doi.org/10.1097/01.ogx.0000279292.63435.40.
  15. Swamy G., Murtha A., Jared H., Boggess K., Lieff S., Heine P. et al. Post‐cesarean infection in women with periodontal disease. Am. J. Obstet. Gynecol. 2002; 187(6, Suppl. 1): 225. (A610).
  16. Mohr S., Amylidi-Mohr S.K., Stadelmann P., Sculean A., Persson R., Eick S., Surbek D.V. Systemic inflammation in pregnant women with periodontitis and preterm prelabor rupture of membranes: A prospective case-control study. Front. Immunol. 2019; 10: 2624. https://dx.doi.org/10.3389/fimmu.2019.02624.
  17. Boggess K.A., Edelstein B.L. Oral health in women during preconception and pregnancy: implications for birth outcomes and infant oral health. Matern. Child Health J. 2006; 10(5, Suppl.): S169-74. https://dx.doi.org/10.1007/s10995-006-0095-x.
  18. Dortbudak O., Eberhardt R., Ulm M., Persson G.R. Periodontitis, a marker of risk in pregnancy for preterm birth. J. Clin. Periodontol. 2005; 32(1): 45-52. https://dx.doi.org/10.1111/j.1600-051X.2004.00630.x.
  19. Escobar-Arregoces F., Latorre-Uriza C., Velosa-Porras J., Roa-Molina N., Ruiz A.J., Silva J. et al. Inflamatory response in pregnant women with high risk of preterm delivery and its relationship with periodontal disease: a pilot study. Acta Odontol. Latinoam. 2018; 31(1): 53-7.
  20. Challis J.R., Lockwood C.J., Myatt L., Norman J.E., Strauss J.F. 3rd, Petraglia F. Inflammation and pregnancy. Reprod. Sci. 2009; 16(2): 206-15. https://dx.doi.org/10.1177/1933719108329095.
  21. Stadelmann P., Alessandri R., Eick S., Salvi G.E., Surbek D., Sculean A. The potential association between gingival crevicular fluid inflammatory mediators and adverse pregnancy outcomes: a systematic review. Clin. Oral Investig. 2013; 17(6): 1453-63. https://dx.doi.org/10.1007/s00784-013-0952-0.
  22. Cetin I., Pileri P., Villa A., Calabrese S., Ottolenghi L., Abati S. Pathogenic mechanisms linking periodontal diseases with adverse pregnancy outcomes. Reprod. Sci. 2012; 19(6): 633-41. https://dx.doi.org/10.1177/1933719111432871.
  23. Palm M., Axelsson O., Wernroth L., Larsson A., Basu S. Involvement of inflammation in normal pregnancy. Acta Obstet. Gynecol. Scand. 2013; 92(5): 601-5. https://dx.doi.org/10.1111/aogs.12093.
  24. Green E.S., Arck P.C. Pathogenesis of preterm birth: bidirectional inflammation in mother and fetus. Semin. Immunopathol. 2020; 42(4): 413-29. https://dx.doi.org/10.1007/s00281-020-00807-y.
  25. Saito S., Nakashima A., Shima T., Ito M. Th-1/Th2/Th-17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 2010; 63(6): 601-10. https://dx.doi.org/10.1111/j.1600-0897.2010.00852.x.
  26. Хаматова А.А., Чеботарева Т.А., Балмасова И.П. Тканерезидентные натуральные киллеры: особенности функционирования в матке и децидуальной оболочке. Иммунология. 2021; 42(5): 574-80. https://dx.doi.org/10.33029/0206-4952-2021-42-5-574-580.
  27. Bardou M., Hadi T., Mace G., Pesant M., Debermont J., Barrichon M. et al. Systemic increase in human maternal circulating CD14+CD16-MCP-1+ monocytes as a marker of labor. Am. J. Obstet. Gynecol. 2014; 210(1): 70. e1-70. e9. https://dx.doi.org/10.1016/j.ajog.2013.08.031.
  28. Fukui A., Ntrivalas E., Fukuhara R., Fujii S., Mizunuma H., Gilman-Sachs A. et al. Correlation between natural cytotoxicity receptors and intracellular cytokine expression of peripheral blood NK cells in women with recurrent pregnancy losses and implantation failures. Am. J. Reprod. Immunol. 2009; 62(6): 371-80. https://dx.doi.org/10.1111/j.1600-0897.2009.00750.x.
  29. Zheng Y., Dong C., Yang J., Jin Y., Zheng W., Zhou Q. et al. Exosomal microRNA-155-5p from PDLSCs regulated Th17/Treg balance by targeting sirtuin-1 in chronic periodontitis. J. Cell. Physiol. 2019; 234(11): 20662-74. https://dx.doi.org/10.1zz002/jcp.28671.
  30. Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. The placenta harbors a unique microbiome. Sci. Transl. Med. 2014; 6(237): 237ra65. https://dx.doi.org/10.1126/scitranslmed.3008599.
  31. Parris K.M., Amabebe E., Cohen M.C., Anumba D.O. Placental microbial-metabolite profiles and inflammatory mechanisms associated with preterm birth. J. Clin. Pathol. 2021; 74(1): 10-8. https://dx.doi.org/10.1136/jclinpath-2020-206536.
  32. Stinson L.F., Boyce M.C., Payne M.S., Keelan J.A. The not-so-sterile womb: evidence that the human fetus is exposed to bacteria prior to birth. Front. Microbiol. 2019; 10: 1124. https://dx.doi.org/10.3389/fmicb.2019.01124.
  33. Mendelson C.R. Minireview: fetal-maternal hormonal signaling in pregnancy and labor. Mol. Endocrinol. 2009; 23(7): 947-54. https://dx.doi.org/10.1210/me.2009-0016.
  34. Morgan T.K. Role of the placenta in preterm birth: a review. Am. J. Perinatol. 2016; 33(3): 258-66. https://dx.doi.org/10.1055/s-0035-1570379.
  35. DiGiulio D.B., Romero R., Amogan H.P., Kusanovic J.P., Bik E.M., Gotsch F. et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-¬based investigation. PLoS One. 2008; 3(8): e3056. https://dx.doi.org/10.1371/journal.pone.0003056.
  36. Leon L.J., Doyle R., Diez-Benavente E., Clark T.G., Klein N., Stanier P., Moore G.E. Enrichment of clinically relevant organisms in spontaneous preterm-delivered placentas and reagent contamination across all clinical groups in a large pregnancy cohort in the United Kingdom. Appl. Environ. Microbiol. 2018; 84(14): e00483-e00518. https://dx.doi.org/10.1128/AEM.00483-18.
  37. Bardos J., Fiorentino D., Longman R.E., Paidas M. Immunological role of the maternal uterine microbiome in pregnancy: pregnancies pathologies and alterated microbiota. Front. Immunol. 2020; 10: 2823. https://dx.doi.org/10.3389/fimmu.2019.02823.
  38. Prince A.L., Ma J., Kannan P.S., Alvarez M., Gisslen T., Harris R.A. et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with without chorioamnionitis. Am. J. Obstet. Gynecol. 2016; 214(5): 627. e1-627. e16. https://dx.doi.org/10.1016/j.ajog.2016.01.193.
  39. Romero R., Dey S.K., Fisher S.J. Preterm labor: one syndrome, many causes. Science. 2014; 345(6198): 760-5. https://dx.doi.org/10.1126/science.1251816.
  40. Witkin S.S. The vaginal microbiome, vaginal anti-microbial defence mechanisms and the clinical challenge of reducing infection-related preterm birth. BJOG. 2015; 122(2): 213-8. https://dx.doi.org/10.1111/1471-0528.13115.
  41. Goepfert A.R., Jeffcoat M.K., Andrews W.W., Faye-Petersen O., Cliver S.P., Goldenberg R.L., Hauth J.C. Periodontal disease and upper genital tract inflammation in early spontaneous preterm birth. Obstet. Gynecol. 2004; 104(4): 777-83. https://dx.doi.org/10.1097/01.AOG.0000139836.47777.6d.
  42. Hill G.B. Preterm birth: Associations with genital and possibly oral microflora. Ann. Periodontol. 1998; 3(1): 222-32. https://dx.doi.org/10.1902/annals.1998.3.1.222.
  43. Gomez L.A., De Avila J., Castillo D.M., Montenegro D.A., Trujillo T.G., Suárez L.J., Lafaurie G.I. Porphyromonas gingivalis placental atopobiosis and inflammatory responses in women with adverse pregnancy outcomes. Front. Microbiol. 2020; 11: 591626. https://dx.doi.org/10.3389/fmicb.2020.591626.
  44. Царев В.Н., Николаева Е.Н., Ипполитов В.Е. Пародонтопатогенные бактерии – основной фактор возникновения и развития пародонтита. Журнал микробиологии, эпидемиологии и иммунобиологии. 2017; 5: 101-12. [Tsarev V.N., Nikolaeva E.N., Ippolitov V.E. Periodontopathogenic baxcteria of the main factors of emergence and development of periodontitis. J Microbiol (Moscow). 2017; 5: 101-12. (in Russian)]. https://dx.doi.org/10.36233/0372-9311-2017-5-101-112.
  45. Bostanci N., Belibasakis G.N. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol. Lett. 2012; 333(1): 1-9. https://dx.doi.org/10.1111/j.1574-6968.2012.02579.x.
  46. Chopra A., Radhakrishnan R., Sharma M. Porphyromonas gingivalis and adverse pregnancy outcomes: a review on its intricate pathogenic mechanisms. Crit. Rev. Microbiol. 2020; 46(2): 213-36. https://dx.doi.org/10.1080/1040841X.2020.1747392.
  47. Inaba H., Amano A., Lamont R.J., Murakami Y., Matsumoto-Nakano M. Cell cycle arrest and apoptosis induced by Porphyromonas gingivalis require Jun N-terminal protein kinase- and p53-mediated p38 activation in human trophoblasts. Infect. Immun. 2018; 86(4): e00923-17. https://dx.doi.org/10.1128/IAI.00923-17.
  48. Han Y.W., Houcken W., Loos B.G., Schenkein H.A., Tezal M. Periodontal disease, atherosclerosis, adverse pregnancy outcomes, and head-and-neck cancer. Adv. Dent. Res. 2014; 26(1): 47-55. https://dx.doi.org/10.1177/0022034514528334.
  49. Schenkein H.A., Berry C.R., Burmeister J.A., Brooks C.N., Barbour S.E., Best A.M., Tew J.G. Anti-cardiolipin antibodies in sera from patients with periodontitis. J. Dent. Res. 2003; 82(11): 919-22. https://dx.doi.org/10.1177/154405910308201114.
  50. Schenkein H.A., Bradley J.L., Purkall D.B. Anticardiolipin in Porphyromonas gingivalis antisera causes fetal loss in mice. J. Dent. Res. 2013; 92(9): 814-8. https://dx.doi.org/10.1177/0022034513497959.

Received 05.03.2022

Accepted 24.03.2022

About the Authors

Anna G. Burduli, MD, PhD, Senior Researcher, Professor B.V. Leonov Department of IVF, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, burdulianna@gmail.com, https://orcid.org/0000-0002-2849-5426,
117997, Russia, Moscow, Academician Oparin str., 4.
Irina P. Balmasova, Dr. Med. Sci., Professor, Head of the Laboratory of Pathogenesis and Methods of Infectious Diseases Treatment, SRMDI, A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia; Professor of Allergology and Immunology Chair, FCME of Medical Institute, RUDN University,
iri.balm@mail.ru, https://orcid.org/0000-0001-8194-2419, 117198, Russia, Moscow, Miklukho-Maklaya str., 21/3.
Viktor N. Tsarev, Dr. Med. Sci., Professor, Head of the Microbiology, Virology and Immunology Department, A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia, nikola777@ rambler.ru, https://orcid.org/0000-0002-3311-0367, 127473, Russia, Moscow, Delegatskaya str., 20-1.
Sergey D. Arutyunov, Dr. Med. Sci., Professor, Head of Department of Propedeutics of Dental Diseases, Dean of the Faculty of Secondary Professional Education,
A.I. Yevdokimov Moscow State University of Medicine and Dentistry, Ministry of Health of Russia, sd.arutyunov@mail.ru, https://orcid.org/0000-0001-6512-8724,
127473, Russia, Moscow, Delegatskaya str., 20-1.

Authors' contributions: Burduli A.G., Balmasova I.P., Tsarev V.N., Arutyunov S.D. – equal contribution to the review of publications on the topic of the article, analysis of the data obtained, writing the manuscript.
Conflicts of interest: The authors declare that there are no possible conflicts of interest.
Funding: The investigation has been conducted without additional third-party funding.
For citation: Burduli A.G., Balmasova I.P., Tsarev V.N., Arutyunov S.D.
Periodontal diseases and their association with unwanted pregnancy outcomes.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 4: 26-33 (in Russian)
https://dx.doi.org/10.18565/aig.2022.4.26-33

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