A prospective study on maternal periodontal diseases and neonatal adverse outcomes

Authors

  • Ping Wen Division of Science & Education, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Huijun Li Division of Stomatology, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Xiaoyi Xu Division of Science & Education, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Feng Zhang Division of Stomatology, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Dan Zhao Beijing Stomatological Hospital, Capital Medical University, Beijing, China; Division of Periodontology & Implant Dentistry, Faculty of Dentistry, The University of Hong Kong, Hong Kong SAR, China
  • Rong Yu Division of Science & Education, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Tianfan Cheng Division of Periodontology & Implant Dentistry, Faculty of Dentistry, The University of Hong Kong, Hong Kong SAR, China
  • Hao Wang Division of Pediatrics, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Chuanzhong Yang Division of Neonatology, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Wei Qin Division of Obstetrics & Gynecology, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Xiuqiao Yang Division of Science & Education, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Jilong Yao Division of Obstetrics & Gynecology, Shenzhen Maternity & Child Healthcare Hospital, Shenzhen, China
  • Lijian Jin Division of Periodontology & Implant Dentistry, Faculty of Dentistry, The University of Hong Kong, Hong Kong SAR, China

DOI:

https://doi.org/10.2340/aos.v83.40836

Keywords:

Periodontal diseases, probing depth, pregnancy, neonatal adverse outcomes, small-for-gestational age

Abstract

Objective: It is evident that periodontitis is linked to various adverse pregnancy outcomes. This prospective study explored the potential link of maternal periodontal diseases to neonatal adverse outcomes.

Materials and Methods: A total of 193 generally healthy females in their third trimester (34–36 weeks) of pregnancy were enrolled. All subjects received full-mouth periodontal assessment, and the periodontal inflamed surface area (PISA) was calculated. Demographic data, lifestyles and anthropometric measurements of the neonates (e.g., body length and head circumference) were recorded. Herein, small-for-gestational age (SGA) referred to gender- and age-adjusted birth weight below the 10th percentile in line with the standard reference. Multivariable logistic regression analysis and restricted cubic spline were performed for examining the association of periodontal parameters with SGA. 

Results: There were 8.3% (16/193) of neonates with SGA. Significantly positive correlation existed between the percentage of tooth sites with increased probing depth and an elevated risk of SGA (OR: 1.052;
P < 0.05). Yet, the PISA was positively associated with the risk of SGA (OR: 1.002; P < 0.05) as well. No significant link occurred between maternal periodontal status and other neonatal outcome measures.

Conclusion: Within the limitations of this study, the findings suggest that there could be a link between maternal periodontal diseases and neonatal adverse outcomes like SGA. Further investigation is required to clarify the current findings and potential implications for promoting maternal oral/periodontal health and newborn health.

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References

Genco RJ, Sanz M. Clinical and public health implications of periodontal and systemic diseases: an overview. Periodontol 2000. 2020;83(1):7–13. https://doi.org/10.1111/prd.12344 DOI: https://doi.org/10.1111/prd.12344

Potempa J, Mydel P, Koziel J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13(10):606–20. https://doi.org/10.1038/nrrheum.2017.132 DOI: https://doi.org/10.1038/nrrheum.2017.132

Acharya C, Sahingur SE, Bajaj JS. Microbiota, cirrhosis, and the emerging oral-gut-liver axis. JCI Insight. 2017;2(19):e94416. https://doi.org/10.1172/jci.insight.94416 DOI: https://doi.org/10.1172/jci.insight.94416

Schenkein HA, Papapanou PN, Genco R, Sanz M. Mechanisms underlying the association between periodontitis and atherosclerotic disease. Periodontol 2000. 2020;83(1):90–106. https://doi.org/10.1111/prd.12304 DOI: https://doi.org/10.1111/prd.12304

Anand PS, Jadhav P, Kamath KP, Kumar SR, Vijayalaxmi S, Anil S. A case-control study on the association between periodontitis and coronavirus disease (COVID-19). J Periodontol. 2022;93(4):584–90. https://doi.org/10.1002/JPER.21-0272 DOI: https://doi.org/10.1002/JPER.21-0272

Wang Y, Deng H, Pan Y, Jin L, Hu R, Lu Y, et al. Periodontal disease increases the host susceptibility to COVID-19 and its severity: a Mendelian randomization study. J Transl Med. 2021;19(1):528. https://doi.org/10.1186/s12967-021-03198-2 DOI: https://doi.org/10.1186/s12967-021-03198-2

Marouf N, Cai W, Said KN, Daas H, Diab H, Chinta VR, et al. Association between periodontitis and severity of COVID-19 infection: a case-control study. J Clin Periodontol. 2021;48(4):483–91. https://doi.org/10.1111/jcpe.13435 DOI: https://doi.org/10.1111/jcpe.13435

Hajishengallis G, Chavakis T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat Rev Immunol. 2021;21(7):426–40. https://doi.org/10.1038/s41577-020-00488-6 DOI: https://doi.org/10.1038/s41577-020-00488-6

Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44. https://doi.org/10.1038/nri3785 DOI: https://doi.org/10.1038/nri3785

D’Aiuto F, Gkranias N, Bhowruth D, Khan T, Orlandi M, Suvan J, et al. Systemic effects of periodontitis treatment in patients with type 2 diabetes: a 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol. 2018;6(12):954–65. https://doi.org/10.1016/S2213-8587(18)30038-X DOI: https://doi.org/10.1016/S2213-8587(18)30038-X

Bajaj JS, Matin P, White MB, Fagan A, Deeb JG, Acharya C, et al. Periodontal therapy favorably modulates the oral-gut-hepatic axis in cirrhosis. Am J Physiol Gastrointest Liver Physiol. 2018;315(5):G824–37. https://doi.org/10.1152/ajpgi.00230.2018 DOI: https://doi.org/10.1152/ajpgi.00230.2018

Genco RJ, Van Dyke TE. Prevention: reducing the risk of CVD in patients with periodontitis. Nat Rev Cardiol. 2010;7(9):479–80. https://doi.org/10.1038/nrcardio.2010.120 DOI: https://doi.org/10.1038/nrcardio.2010.120

Tonetti MS. Periodontitis and risk for atherosclerosis: an update on intervention trials. J Clin Periodontol. 2009;36(Suppl 10):15–19. https://doi.org/10.1111/j.1600-051X.2009.01417.x DOI: https://doi.org/10.1111/j.1600-051X.2009.01417.x

Raju K, Berens L. Periodontology and pregnancy: An overview of biomedical and epidemiological evidence. Periodontol 2000. 2021;87(1):132–42. https://doi.org/10.1111/prd.12394 DOI: https://doi.org/10.1111/prd.12394

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. https://doi.org/10.1111/j.2041-1626.2012.00137.x DOI: https://doi.org/10.1111/j.2041-1626.2012.00137.x

Manau C, Echeverria A, Agueda A, Guerrero A, Echeverria JJ. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. J Clin Periodontol. 2008;35(5):385–97. https://doi.org/10.1111/j.1600-051X.2008.01222.x DOI: https://doi.org/10.1111/j.1600-051X.2008.01222.x

Sanz M, Kornman K, working group 3 of the joint EFPAAP workshop. Periodontitis and adverse pregnancy outcomes: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol. 2013;84(4 Suppl):S164–9. https://doi.org/10.1902/jop.2013.1340016 DOI: https://doi.org/10.1902/jop.2013.1340016

Boggess KA, Beck JD, Murtha AP, Moss K, Offenbacher S. Maternal periodontal disease in early pregnancy and risk for a small-for-gestational-age infant. Am J Obstet Gynecol. 2006;194(5):1316–22. https://doi.org/10.1016/j.ajog.2005.11.059 DOI: https://doi.org/10.1016/j.ajog.2005.11.059

Chambrone L, Guglielmetti MR, Pannuti CM, Chambrone LA. Evidence grade associating periodontitis to preterm birth and/or low birth weight: I. A systematic review of prospective cohort studies. J Clin Periodontol. 2011;38(9):795–808. https://doi.org/10.1111/j.1600-051X.2011.01755.x DOI: https://doi.org/10.1111/j.1600-051X.2011.01755.x

Figuero E, Han YW, Furuichi Y. Periodontal diseases and adverse pregnancy outcomes: mechanisms. Periodontol 2000. 2020;83(1):175–88. https://doi.org/10.1111/prd.12295 DOI: https://doi.org/10.1111/prd.12295

Heo JS, Ahn KH, Park JS. Radiological screening of maternal periodontitis for predicting adverse pregnancy and neonatal outcomes. Sci Rep. 2020;10(1):21266. https://doi.org/10.1038/s41598-020-78385-0 DOI: https://doi.org/10.1038/s41598-020-78385-0

Ide M, Papapanou PN. Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes – systematic review. J Periodontol. 2013;84(4 Suppl):S181–94. DOI: https://doi.org/10.1902/jop.2013.134009

Iheozor-Ejiofor Z, Middleton P, Esposito M, Glenny AM. Treating periodontal disease for preventing adverse birth outcomes in pregnant women. Cochrane Database Syst Rev. 2017;6:CD005297. https://doi.org/10.1002/14651858.CD005297.pub3 DOI: https://doi.org/10.1002/14651858.CD005297.pub3

Marquez-Corona ML, Tellez-Giron-Valdez A, Pontigo-Loyola AP, Islas-Zarazua R, Robles-Bermeo NL, Gonzalez-Lopez BS, Medina-Solis CE. Preterm birth associated with periodontal and dental indicators: a pilot case-control study in a developing country. J Matern Fetal Neonatal Med. 2021;34(5):690–5. DOI: https://doi.org/10.1080/14767058.2019.1613363

Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol. 1996;67(10 Suppl):1103–13. https://doi.org/10.1902/jop.1996.67.10.1103 DOI: https://doi.org/10.1902/jop.1996.67.10.1103

Jung E, Romero R, Yeo L, Gomez-Lopez N, Chaemsaithong P, Jaovisidha A, et al. The etiology of preeclampsia. Am J Obstet Gynecol. 2022;226(2S):S844–66. DOI: https://doi.org/10.1016/j.ajog.2021.11.1356

Spivakovsky S. Periodontal treatment for the prevention of adverse birth outcomes. Evid Based Dent. 2018;19(1):12–13. https://doi.org/10.1038/sj.ebd.6401286 DOI: https://doi.org/10.1038/sj.ebd.6401286

Komine-Aizawa S, Aizawa S, Hayakawa S. Periodontal diseases and adverse pregnancy outcomes. J Obstet Gynaecol Res. 2019;45(1):5–12. DOI: https://doi.org/10.1111/jog.13782

Rijken MJ, De Livera AM, Lee SJ, Boel ME, Rungwilailaekhiri S, Wiladphaingern J, et al. Quantifying low birth weight, preterm birth and small-for-gestational-age effects of malaria in pregnancy: a population cohort study. PLoS One. 2014;9(7):e100247. https://doi.org/10.1371/journal.pone.0100247 DOI: https://doi.org/10.1371/journal.pone.0100247

Zhang Y, Feng W, Li J, Cui L, Chen ZJ. Periodontal disease and adverse neonatal outcomes: a systematic review and meta-analysis. Front Pediatr. 2022;10:799740. https://doi.org/10.3389/fped.2022.799740 DOI: https://doi.org/10.3389/fped.2022.799740

World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191–4. DOI: https://doi.org/10.1001/jama.2013.281053

Zhao D, Cheng T, Hu D, Xu X, Zhang F, Yu R, et al. Maternal periodontal diseases affect the leukocyte profiles of umbilical cord blood: A cohort study. Oral Dis. 2024;30:2533–45. https://doi.org/10.1111/odi.14683 DOI: https://doi.org/10.1111/odi.14683

Miki K, Kitamura M, Hatta K, Kamide K, Gondo Y, Yamashita M, et al. Periodontal inflamed surface area is associated with hs-CRP in septuagenarian Japanese adults in cross-sectional findings from the SONIC study. Sci Rep. 2021;11(1):14436. DOI: https://doi.org/10.1038/s41598-021-93872-8

Huang XY, Liu HL, Lei M, Mai HF, Lian CH, Li YC. Intrauterine growth curves for body weight, body length, head circumference, chest circumference, and crown-rump length in 16 887 neonates with a gestational age of 27–42 weeks in Shenzhen, China. Zhongguo Dang Dai Er Ke Za Zhi. 2017;19(8):877–86. [Chinese]

Wu M, Chen SW, Su WL, Zhu HY, Ouyang SY, Cao YT, et al. Sex hormones enhance gingival inflammation without affecting IL-1beta and TNF-alpha in periodontally healthy women during pregnancy. Mediators Inflamm. 2016;2016:4897890. DOI: https://doi.org/10.1155/2016/4897890

Kumar PS. Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria? Periodontol 2000. 2013;61(1):103–24. https://doi.org/10.1111/j.1600-0757.2011.00398.x DOI: https://doi.org/10.1111/j.1600-0757.2011.00398.x

Nuriel-Ohayon M, Neuman H, Koren O. Microbial changes during pregnancy, birth, and infancy. Front Microbiol. 2016;7:1031. DOI: https://doi.org/10.3389/fmicb.2016.01031

Fujiwara N, Tsuruda K, Iwamoto Y, Kato F, Odaki T, Yamane N, et al. Significant increase of oral bacteria in the early pregnancy period in Japanese women. J Investig Clin Dent. 2017;8(1):e12189. https://doi.org/10.1111/jicd.12189 DOI: https://doi.org/10.1111/jicd.12189

Balan P, Chong YS, Umashankar S, Swarup S, Loke WM, Lopez V, et al. Keystone species in pregnancy gingivitis: a snapshot of oral microbiome during pregnancy and postpartum period. Front Microbiol. 2018;9:2360. https://doi.org/10.3389/fmicb.2018.02360 DOI: https://doi.org/10.3389/fmicb.2018.02360

Mascarenhas P, Gapski R, Al-Shammari K, Wang HL. Influence of sex hormones on the periodontium. J Clin Periodontol. 2003;30(8):671–81. https://doi.org/10.1034/j.1600-051X.2003.00055.x DOI: https://doi.org/10.1034/j.1600-051X.2003.00055.x

Bobetsis YA, Graziani F, Gursoy M, Madianos PN. Periodontal disease and adverse pregnancy outcomes. Periodontol 2000. 2020;83(1):154–74. DOI: https://doi.org/10.1111/prd.12294

Pockpa ZAD, Soueidan A, Koffi-Coulibaly NT, Limam A, Badran Z, Struillou X. Periodontal diseases and adverse pregnancy outcomes: review of two decades of clinical research. Oral Health Prev Dent. 2021;19(1):77–83.

Xu B, Han YW. Oral bacteria, oral health, and adverse pregnancy outcomes. Periodontol 2000. 2022;89(1):181–9. DOI: https://doi.org/10.1111/prd.12436

Lefizelier E, Misbert E, Brooks M, Thuaut AL, Winer N, Ducarme G. Preterm birth and small-for-gestational age neonates among prepregnancy underweight women: a case-controlled study. J Clin Med. 2021;10(24) https://doi.org/10.3390/jcm10245733 DOI: https://doi.org/10.3390/jcm10245733

Ruiz M, Goldblatt P, Morrison J, Kukla L, Švancara J, Riitta-Järvelin M, et al. Mother’s education and the risk of preterm and small for gestational age birth: a DRIVERS meta-analysis of 12 European cohorts. J Epidemiol Community Health. 2015;69(9):826–33. https://doi.org/10.1136/jech-2014-205387 DOI: https://doi.org/10.1136/jech-2014-205387

Kim SY, Lee SM, Kwon GE, Kim BJ, Koo JN, Oh IH, et al. Maternal dyslipidemia and altered cholesterol metabolism in early pregnancy as a risk factor for small for gestational age neonates. Sci Rep. 2021;11(1):21066. DOI: https://doi.org/10.1038/s41598-021-00270-1

Parra-Saavedra M, Crovetto F, Triunfo S, Savchev S, Peguero A, Nadal A, et al. Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta. 2013;34(12):1136–41. https://doi.org/10.1016/j.placenta.2013.09.018 DOI: https://doi.org/10.1016/j.placenta.2013.09.018

Lafaurie GI, Gómez LA, Montenegro DA, De Avila J, Tamayo MC, Lancheros MC, et al. Periodontal condition is associated with adverse perinatal outcomes and premature rupture of membranes in low-income pregnant women in Bogota, Colombia: a case-control study. J Matern Fetal Neonatal Med. 2020;33(1):16–23. DOI: https://doi.org/10.1080/14767058.2018.1484092

Takeuchi N, Ekuni D, Irie K, Furuta M, Tomofuji T, Morita M, Watanabe T. Relationship between periodontal inflammation and fetal growth in pregnant women: a cross-sectional study. Arch Gynecol Obstet. 2013;287(5):951–7. https://doi.org/10.1007/s00404-012-2660-4 DOI: https://doi.org/10.1007/s00404-012-2660-4

American Academy of Periodontology. American Academy of Periodontology statement regarding periodontal management of the pregnant patient. J Periodontol. 2004;75(3):495. https://doi.org/10.1902/jop.2004.75.3.495 DOI: https://doi.org/10.1902/jop.2004.75.3.495

Jiao J, Jing W, Si Y, Feng X, Tai B, Hu D, et al. The prevalence and severity of periodontal disease in Mainland China: data from the Fourth National Oral Health Survey (2015–2016). J Clin Periodontol. 2021;48(2):168–79. DOI: https://doi.org/10.1111/jcpe.13396

Erchick DJ, Rai B, Agrawal NK, Khatry SK, Katz J, LeClerq SC, et al. Oral hygiene, prevalence of gingivitis, and associated risk factors among pregnant women in Sarlahi District, Nepal. BMC Oral Health. 2019;19(1):2. https://doi.org/10.1186/s12903-018-0681-5 DOI: https://doi.org/10.1186/s12903-018-0681-5

Zhang F, Zhao D, Xu X, Wen P, Li H, Yu R, et al. Periodontitis links to concurrent metabolic disorders and abnormal liver function in pregnant women. Oral Dis. 2024; 30(2):697-709. https://doi.org/10.1111/odi.14364 DOI: https://doi.org/10.1111/odi.14364

Li HJ, Zhao D, Xu X, Yu R, Zhang F, Cheng T, et al. Diagnostic performance of the AAP/EFP classification and the CDC/AAP case definition among pregnant women and a practical screening tool for maternal periodontal diseases. J Periodontal Res. 2022;57(5):960–8. https://doi.org/10.1111/jre.13032 DOI: https://doi.org/10.1111/jre.13032

Published

2024-06-11