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Association Between Periodontal Diseases and Adverse Gestation Outcomes: a Review of the Current Literature

  • Davi da Silva BarbiratoEmail author
  • Monique Oliveira Rodrigues
  • Julianna Peres Alves
  • Heric Pinheiro de Castro
  • Mariana Fampa Fogacci
Systemic Diseases (N Buduneli, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Systemic Diseases

Abstract

Purpose of Review

Miller (Dent Cosmos 1891:698–713, 1999) and Hunter (Br Med J 2:215–216, 1900) suggested the hypothesis that oral infections could spread throughout the body causing sepsis or be related to other pathologies in other systems or parts of the human body. In the 1990s, some research groups investigated possible associations between periodontal diseases and systemic diseases, such as prematurity and low birth weight. However, although there were theoretical bases related to the hypotheses tested, the experimental models indicated to explore the biological bases of this process (biological plausibility) were limited, and great part had essential limitations related to the experimental design (artificial models incompatible or not similar to the periodontal diseases which affect humans). Observational and interventional clinical studies have been developed since then, with considerable difficulties and limitations inherent in the proposal of the studies. Prematurity and low birth weight present approximately 40 associated risk factors, and periodontal diseases are multifactorial and extremely complex either. Each research carried out and published represents a new scientific contribution and the critical construction of new knowledge, the formulation of new hypotheses, and the evolution to study models closer to a definitive answer on the cause and effect relationship between periodontal diseases and adverse effects of pregnancy. Thus, the present study aims to review articles published in the last 3 years that approached this possible association.

Recent Findings

This review had a total of 14 scientific papers of the following types: observational studies, interventional studies, and experimental studies.

Summary

The present study shows controversial results, with a greater number of cases of non-association between periodontal diseases and adverse pregnancy events, especially with prematurity and/or low birth weight. However, it is biologically possible that there is a relationship between diseases that affect the oral cavity and gestation in humans; more studies are necessary to have a conclusion in this regard.

Keywords

Adverse outcomes of pregnancy Preterm Low birth weight Preterm and low birth weight Periodontal diseases Periodontitis 

Notes

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.

References

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

  1. 1.
    Chawanpaiboon S, Vogel JP, Moller A-B, Lumbiganon P, Petzold M, Hogan D, et al. Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health. 2018;109x(18):30451–0.Google Scholar
  2. 2.
    Kinney HC. The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review. Semin Perinatol. 2006;30:81–8.PubMedCrossRefGoogle Scholar
  3. 3.
    O’Connor AR, Wilson CM, Fielder AR. Ophthalmological problems associated with preterm birth. Eye. 2007;21:1254–60.PubMedCrossRefGoogle Scholar
  4. 4.
    Araujo BF, Zatti H, Madi JM, Coelho MB, Olmi FB, Canabarro CT. Analysis of neonatal morbidity and mortality in late-preterm newborn infants. J Pediatr. 2012;88:259–66.CrossRefGoogle Scholar
  5. 5.
    Mwaniki MK, Atieno M, Lawn JE, Newton CR. Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet. 2012;379:445–52.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008;371:261–9.PubMedCrossRefGoogle Scholar
  7. 7.
    Ramenghi LA. Late preterm babies and the risk of neurological damage. Acta Biomed. 2015;86(suppl 1):36–40.PubMedGoogle Scholar
  8. 8.
    van Dommelen P, Verkerk PH, van Straaten HL. Dutch neonatal intensive care unit neonatal hearing screening working group. J Pediatr. 2015;166:840–3.PubMedCrossRefGoogle Scholar
  9. 9.
    Singer LT, Salvator A, Guo S, Collin M, Lilien L, Baley J. Maternal psychological distress and parenting stress after the birth of a very low-birth-weight infant. JAMA. 1999;281:799–805.PubMedCrossRefGoogle Scholar
  10. 10.
    Petrou S, Abangma G, Johnson S, Wolke D, Marlow N. Costs and health utilities associated with extremely preterm birth: evidence from the EPICure study. Value Health. 2009;12:1124–34.PubMedCrossRefGoogle Scholar
  11. 11.
    Korvenranta E, Lehtonen L, Rautava L, et al. Impact of very preterm birth on health care costs at five years of age. Pediatrics. 2010;125:1109–14.CrossRefGoogle Scholar
  12. 12.
    Berard A, Le Tiec M, De Vera MA. Study of the costs and morbidities of late-preterm birth. Arch Dis Child Fetal Neonatal Ed. 2012;97:F329–34.PubMedCrossRefGoogle Scholar
  13. 13.
    WHO - World Health Organization. Optima feeding of low-birth-weight infants: Tecnal review. Genebra, 2006.Google Scholar
  14. 14.
    WHO World Health Organization. Preterm birth. Fact Sheet No 363, 2014.Google Scholar
  15. 15.
    Offenbacher S, Katz V, Fertik GJ. Periodontal infection as a possible risk factor for PTLBW. J Periodontol. 1996;67:1103–13.PubMedCrossRefGoogle Scholar
  16. 16.
    Vettore MV, Lamarca GA, Leão AT, Thomaz FB, Sheiham A, Leal MC. Periodontal infection and adverse pregnancy outcomes: a systematic review of epidemiological studies. Cad Saude Publica. 2006;22(10):2041–53.PubMedCrossRefGoogle Scholar
  17. 17.
    Polyzos NP, Polyzos IP, Zavos A, Valachis A, Mauri D, Papanikolau EG, et al. Obstetric outcomes after treatment of periodontal disease during pregnancy: systematic review and meta-analysis. BMJ. 2010;341:7017.CrossRefGoogle Scholar
  18. 18.
    • da Silva HEC, Stefani CM, de Santos Melo N, de Almeida de Lima A, Rösing CK, Porporatti AL, et al. Effect of intra-pregnancy nonsurgical periodontal therapy on inflammatory biomarkers and adverse pregnancy outcomes: a systematic review with meta-analysis. Syst Rev. 2017;6(1):197 This study is a systematic review that included the most recent studies on the subject, evaluating the effects of intra-pregnancy nonsurgical periodontal therapy on periodontal inflammatory biomarkers and adverse pregnancy outcomes. PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    • Corbella S, Taschieri S, Del Fabbro M, Francetti L, Weinstein R, Ferrazzi E. Adverse pregnancy outcomes and periodontitis: A systematic review and meta-analysis exploring potential association. Quintessence Int. 2016;47(3):193–204 This study is a systematic review that included the most recent studies on the subject, evaluating periodontal diseases as an independent risk factor for adverse pregnancy outcomes. PubMedGoogle Scholar
  20. 20.
    Moher D, Liberati A, Tetzlaff J, Altman DG. The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):1–6.CrossRefGoogle Scholar
  21. 21.
    Khan FR, Ahmad T, Hussain R, Bhutta ZA. Relationship among hypovitaminosis D, maternal periodontal disease, and low birth weight. J Coll Physicians Surg Pak. 2018;28:36–9.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Ramfjord SP. Indices for prevalence and incidence of periodontal disease. J Periodontol. 1959;30:51–9.CrossRefGoogle Scholar
  23. 23.
    Löe H, Silness J. Periodontal disease in pregnance. Acta Odontol Scand. 1963;21:533–51.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Turton M, CWJ A. Further evidence for periodontal disease as a risk indicator for adverse pregnancy outcomes. Int Dent J. 2017;67(3):148–56.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Offenbacher S, Lieff S, Boggess KA, Murtha AP, Madianos PN, Champagne CME, et al. Maternal periodontitis and prematurity. Part I: obstetric outcome of prematurity and growth restriction. Ann Periodontol. 2001;6:164–74.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    WHO – World Health Organization. Oral health survey-basics methods, 4th edn. World Health Organization. Geneva, 1997.Google Scholar
  27. 27.
    Silness J, Löe H. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–35.PubMedCrossRefGoogle Scholar
  28. 28.
    Tilakarantne A, Soory M, Ranasinghe AW, et al. Periodontal disease status during pregnancy and 3 months postpartum, in a rural population of Sri-Lankan women. J Clin Periodontol. 2000;27:787–92.CrossRefGoogle Scholar
  29. 29.
    Mumghamba EG, Pitiphat W, Matee MI, et al. The usefulness of using Ramfjord teeth in predicting periodontal status of a Tanzanian adult population. J Clin Periodontol. 2004;31:16–8.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Najah A, Seham S, Fadhil R. The usefulness of Ramfjord teeth to represent the full-mouth pocket depth in epidemiological study. MDJ. 2010;7:272–5.Google Scholar
  31. 31.
    Lee HJ, Ha JE, Bae KH. Synergistic effect of maternal obesity and periodontitis on preterm birth in women with pre-eclampsia: a prospective study. J Clin Periodontol. 2016:1–6.Google Scholar
  32. 32.
    Kopelman PG. Obesity as a medical problem. Nature. 2000;404:635–43.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    WHO Expert Consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157–63.CrossRefGoogle Scholar
  34. 34.
    Offenbacher S, Jared HL, O’Reilly PG, Wells SR, Salvi GE, Lawrence HP, et al. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Annals of Periodontology. 1998;3:233–50.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Boggess KA, Lieff S, Murtha AP, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol. 2003;101:227–31.PubMedGoogle Scholar
  36. 36.
    Kumar A, Basra M, Begum N, Rani V, Prasad S, Lamba AK, et al. Association of maternal periodontal health with adverse pregnancy outcome. J Obstet Gynaecol Res. 2013;39:40–5.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Torloni MR, Betran AP, Dager S, Widmer M, Dolan SM, Menon R, et al. Maternal BMI and preterm birth: a systematic review of the literature with meta-analysis. J Matern Fetal Neonatal Med. 2009;22:957–70.PubMedCrossRefGoogle Scholar
  38. 38.
    Cnattingius S, Villamor E, Johansson S, Edstedt Bonamy AK, Persson M, Wikström AK, et al. Maternal obesity and risk of preterm delivery. JAMA. 2012;309:2362–70.CrossRefGoogle Scholar
  39. 39.
    Berkowitz GS, Blackmore-Prince C, Lapinski RH, Savitz DA. Risk factors for preterm birth subtypes. Epidemiology. 1998;9:279–85.PubMedCrossRefGoogle Scholar
  40. 40.
    Goldenberg RL, Culhane JF, Lams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371:75–84.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Ehrenberg HM, Iams JD, Goldenberg RL, Newman RB, Weiner SJ, Sibai BM, et al. Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) Maternal-Fetal Medicine Units Net- work (MFMU) Maternal obesity, uterine activity, and the risk of spontaneous preterm birth. Obstet Gynecol. 2009;113:48–52.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Goldenberg RL, Culhane JF. Pre-pregnancy health status and the risk of preterm delivery. Archives of Pediatrics & Adolescent Medicine. 2005;159:89–90.CrossRefGoogle Scholar
  43. 43.
    Martínez-Martínez RE, Moreno-Castillo DF, Loyola-Rodríguez JP, Sánchez-Medrano AG, Miguel-Hernández JHS, Olvera-Delgado JH, Domínguez-Pérez RA. Association between periodontitis, periodontopathogens and preterm birth: is it real? Arch Gynecol Obstet 2016;249(1):47-54.Google Scholar
  44. 44.
    Armitage G. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4:1–6.PubMedCrossRefGoogle Scholar
  45. 45.
    Jeffcoat MK, Geurs NC, Reddy MS, Cliver SP, Goldenberg RL, Hauth JC. Periodontal infection and preterm birth: results of a prospective study. J Am Dent Assoc. 2001;184:2005–18.Google Scholar
  46. 46.
    Radnai M, Gorzo I, Urban E, Eller J, Novak T, Pal A. Possible association between mother’s periodontal status and preterm delivery. J Clin Periodontol. 2006;33:791–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Macedo JF, Ribeiro RA, Machado FC, et al. Periodontal disease and oral health-related behavior as factors associated with preterm birth: a case–control study in south-eastern Brazil. J Pe- riodont Res. 2014;49:458–64.CrossRefGoogle Scholar
  48. 48.
    Löe H. The gingival index, plaque index, and the retention index systems. J Periodontol. 1967;38:610–6.CrossRefGoogle Scholar
  49. 49.
    Greene JC, Vermilon JR. The oral hygiene index: a method for classifying oral hygiene status. J Am Dent Assoc. 1960;61:172–9.CrossRefGoogle Scholar
  50. 50.
    Martínez-Martínez RE, Abud-Mendoza C, Patinõ-Marín N, Rizo-Rodríguez JC, Little JW, Loyola-Rodriguez JP. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol. 2009;36:1004–10.PubMedCrossRefGoogle Scholar
  51. 51.
    Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res. 1991;26:230–42.PubMedCrossRefGoogle Scholar
  52. 52.
    Buduneli N, Baylas H, Budunneli E, Türkoglu O, Köse T, Dahlen G. Periodontal infections and pre-term low birth weight: a case control study. J Clin Periodontol. 2005;32:174–81.PubMedCrossRefGoogle Scholar
  53. 53.
    Bassani DG, Olinto MTA, Kreiger N. Periodontal disease and perinatal outcomes: a case-control study. J Clin Periodontol. 2007;34:31–9.PubMedCrossRefGoogle Scholar
  54. 54.
    Lieff S, Boggess KA, Murtha AP, Jared H, Madianos PM, Moss K, et al. The Oral conditions and pregnancy study: periodontal status of a cohort of pregnant women. J Periodontol. 2004;75:116–26.PubMedCrossRefGoogle Scholar
  55. 55.
    Tellapragada C, Eshwara VK, Bhat P, Acharya S, Kamath A, Bhat S, et al. Risk factors for preterm birth and low birth weight among pregnant Indian women: a hospital-based prospective study. J Prev Med Public Health. 2016;49:165–75.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Vogel JP, Lee AC, Souza JP. Maternal morbidity and preterm birth in 22 low- and middle-income countries: a secondary analysis of the WHO Global Survey dataset. BMC Pregnancy Childbirth. 2014;14:56.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Mumbare SS, Maindarkar G, Darade R, Yenge S, Tolani MK, Patole K. Maternal risk factors associated with term low birth weight neonates: a matched-pair case control study. Indian Pediatr. 2012;49(1):25–8.PubMedCrossRefGoogle Scholar
  58. 58.
    Thomre PS, Borle AL, Naik JD, Rajderkar SS. Maternal risk factors determining birth weight of newborns: a tertiary care hospital based study. Int J Recent Trends Sci Technol. 2012;5(1):3–8.Google Scholar
  59. 59.
    Nair NS, Rao RS, Chandrashekar S, Acharya D, Bhat HV. Socio- demographic and maternal determinants of low birth weight: a multivariate approach. Indian J Pediatr. 2000;67(1):9–14.PubMedCrossRefGoogle Scholar
  60. 60.
    Kimura S, Ooshima T, Takiguchi M, Sasaki Y, Amano A, Morisaki I, et al. Periodontopathic bacterial infection in childhood. J Periodontol. 2002;73(1):20–6.PubMedCrossRefGoogle Scholar
  61. 61.
    Murthy S, Mubashir A, Kodkany BS, Mallapur MD. Pregnancy periodontitis and low birth weight: a cohort study in rural Belgaum, India. Glob J Med Public Health. 2012;1(4):42–8.Google Scholar
  62. 62.
    Vogt M, Sallum AW, Cecatti JG, Morais SS. Factors associated with the prevalence of periodontal disease in low-risk pregnant women. Reprod Health. 2012;9:3–11.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Donati L, Di Vico A, Nucci M, Quagliozzi L, Spagnuolo T, Labianca A, et al. Vaginal microbial flora and outcome of pregnancy. Arch Gynecol Obstet. 2010;281(4):589–600.PubMedCrossRefGoogle Scholar
  64. 64.
    Goldenberg RL, Goepfert AR, Ramsey PS. Biochemical markers for the prediction of preterm birth. Am J Obstet Gynecol. 2005;192(5 Suppl):S36–46.PubMedCrossRefGoogle Scholar
  65. 65.
    Kim BJ, Romero R, Mi Lee S, Park CW, Shin Park J, Jun JK, et al. Clinical significance of oligohydramnios in patients with pre-term labor and intact membranes. J Perinat Med. 2011;39(2):131–6.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Zhang YP, Liu XH, Gao SH, Wang JM, Gu YS, Zhang JY, et al. Risk factors for preterm birth in five maternal and child health hospitals in Beijing. PLoS One. 2012;7(12):e52780.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Blencowe H, Lawn JE, Vazquez T, Fielder A, Gilbert C. Preterm-associated visual impairment and estimates of retinopathy of prematurity at regional and global levels for 2010. Pediatr Res. 2013;74(suppl 1):35–49.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Yadav H, Lee N. Maternal factors in predicting low birth weight babies. Med J Malaysia. 2013;68(1):44–7.PubMedGoogle Scholar
  69. 69.
    Smaill F, Vazquez JC. Antibiotics for asymptomatic bacteriuria in pregnancy. Cochrane Database Syst Rev. 2007;2:CD000490.Google Scholar
  70. 70.
    Jain V, Das V, Agarwal A, Pandey A. Asymptomatic bacteriuria & obstetric outcome following treatment in early versus late pregnancy in north Indian women. Indian J Med Res. 2013;137(4):753–8.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Soucy-Giguère L, Tétu A, Gauthier S, Morand M, Chandad F, Giguère Y, et al. Periodontal disease and adverse pregnancy outcomes: a porspective study in a low-risk population. J Obstet Gynaecol Can. 2016;38(4):346–50.PubMedCrossRefGoogle Scholar
  72. 72.
    Perunovic ND, Rakic MM, Nikolic LI, Jankovic SM, Aleksic ZM, Plecas DV, et al. The association between periodontal inflammation and labor triggers elevated cytokine levels in pre-term birth: a cross-sectional study. J Periodontol. 2016;87(3):248–56.PubMedCrossRefGoogle Scholar
  73. 73.
    Pozo E, Mesa F, Ikram MH, Puertas A, Torrecillas-Marínez L, Ortega-Oller I, et al. Preterm birth and/or low birth weight are associated with periodontal disease and the increased placental immunohistochemical expression of inflammatory markers. Histol Histopathol. 2016;31(2):231–7.PubMedGoogle Scholar
  74. 74.
    Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J. 1975;25:229–35.PubMedGoogle Scholar
  75. 75.
    López NJ, Smith PC, Gutierrez J. Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res. 2002;81:58–63.PubMedCrossRefGoogle Scholar
  76. 76.
    Nigro G, Mazzocco M, Mattia E, Di Renzo GC, Carta G, Anceschi MM. Role of the infections in recurrent spontaneous abortion. J Matern Fetal Neonatal Med. 2011;24:983–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Kitsantas P, Christopher KE. Smoking and respiratory conditions in pregnancy: associations with adverse pregnancy outcomes. South Med J. 2013;106:310–5.PubMedCrossRefGoogle Scholar
  78. 78.
    Hasegawa-Nakamura K, Tateishi F, Nakamura T, Nakajima Y, Kawamata K, Douchi T, et al. The possible mechanism of preterm birth associated with periodontopathic Porphyromonas gingivalis. J Periodontal Res. 2011;46:497–504.PubMedCrossRefGoogle Scholar
  79. 79.
    Tateishi F, Hasegawa-Nakamura K, Nakamura T, Oogai Y, Komatsuzawa H, Kawamata K, et al. Detection of fusobacterium nucleatum in chorionic tissues of high-risk pregnant women. J Clin Periodontol. 2012;39:417–24.PubMedCrossRefGoogle Scholar
  80. 80.
    Mesa F, Pozo E, Blanc V, Puertas A, Bravo M, O'Valle F. Are periodontal bacterial profiles and placental inflammatory infiltrate in pregnancy related to birth outcomes? J Periodontol. 2013;84:1327–36.PubMedCrossRefGoogle Scholar
  81. 81.
    Pawelec M, Pałczyński B, Krzemieniewska J, Karmowski M, Koryś J, Lątkowski K, et al. Initiation of preterm labor. Adv Clin Exp Med. 2013;22:283–8.PubMedGoogle Scholar
  82. 82.
    Padmini E, Uthra V, Lavanya S. Effect of HSP70 and 90 in modulation of JNK, ERK expression in preeclamptic placental endothelial cell. Cell Biochem Biophys. 2012;64:187–95.PubMedCrossRefGoogle Scholar
  83. 83.
    Molvarec A, Rigó J Jr, Lázár L, Balogh K, Makó V, Cervenak L, et al. Increased serum heat-shock protein 70 levels reflect systemic inflammation, oxidative stress and hepatocellular injury in preeclampsia. Cell Stress Chaperones. 2009;14:151–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Chaiworapongsa T, Erez O, Kusanovic JP, Vaisbuch E, Mazaki-Tovi S, Gotsch F, et al. Amniotic fluid heat shock protein 70 concentration in histologic chorioamnionitis, term and preterm parturition. J Matern Fetal Neonatal Med. 2008;21:449–61.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Souza LM, da Cruz SS, Gomes-Filho IS, Barreto ML, Passos-Soares JS, Trindade SC, et al. Effect of maternal periodontitis and low birth weight – a case control study. Acta Odontol Scand. 2016:1–8.Google Scholar
  86. 86.
    Vettore MV, Leal M, Leão AT, da Silva AM, Lamarca GA, Sheiham A. The relationship between periodontitis and pre- term low birthweight. J Dent Res. 2008b;87:73–8.PubMedCrossRefGoogle Scholar
  87. 87.
    Vettore MV, Leão AT, Leal Mdo C, Feres M, Sheiham A. The relationship between periodontal disease and preterm low birthweight: clinical and microbiological results. J Periodontal Res. 2008a;43:615–26.PubMedCrossRefGoogle Scholar
  88. 88.
    Michalowicz BS, Hodges JS, DiAngelis AJ, Lupo VR, Novak MJ, Ferguson JE, et al. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med. 2006;355:1885–94.PubMedCrossRefGoogle Scholar
  89. 89.
    Ebersole JL, Novak MJ, Michalowicz BS, Hodges JS, Steffen MJ, Ferguson JE, et al. Systemic immune responses in pregnancy and periodontitis: relationship to pregnancy outcomes in the obstetrics and periodontal therapy (OPT) study. J Periodontol. 2009;80:953–60.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Michalowicz BS, Hodges JS, Novak MJ, Buchanan W, DiAngelis AJ, Papapanou PN, et al. Change in periodontitis during pregnancy and the risk of pre-term birth and low birth weight. J Clin Periodontol. 2009;36:308–14.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Offenbacher S, Beck JD, Jared HL, Mauriello SM, Mendoza LC, Couper DJ, et al. Effects of periodontal therapy on rate of preterm delivery: a randomized controlled trial. Obstet Gynecol. 2009;114:551–9.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Macones GA, Parry S, Nelson DB, Strauss JF, Ludmir J, Cohen AW, et al. Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: results from the periodontal infections and prematurity study (PIPS). Am J Obstet Gynecol. 2010;202:147–8.PubMedGoogle Scholar
  93. 93.
    Usin MM, Menso J, Rodríguez VI, González A, Tabares S, Parodi R, et al. Association between maternal periodontitis and preterm and/or low birth weight infants in normal pregnancies. J Matern Fetal Neonatal Med. 2014:1–5.Google Scholar
  94. 94.
    Scannapieco FA, Bush RB, Paju S. Periodontal disease as a risk factor for adverse pregnancy outcomes: a systematic review. Ann Periodontol. 2003;8:70–8.PubMedCrossRefGoogle Scholar
  95. 95.
    Castaldi JL, Bertin MS, Giménez F, Lede R. Periodontal disease: is it a risk factor for premature labor, low birth weight or preeclampsia? Rev Panam Salud Publica. 2006;19:253–8.PubMedCrossRefGoogle Scholar
  96. 96.
    Léon R, Silva N, Ovalle A, Chaparro A, Ahumada A, Gajardo M, et al. Detection of Porphyromonas gingivalis in the amniotic fluid in pregnant women with a diagnosis of threatened premature labor. J Periodontol. 2007;78:1249–55.PubMedCrossRefGoogle Scholar
  97. 97.
    Ali TB, Abidin KZ. Relationship of periodontal disease to preterm low birth weight infants in a selected population – a prospective study. Community Dent Health. 2012;29:100–5.PubMedGoogle Scholar
  98. 98.
    Miyoshi J, Onba T, Ohkuma M, Katoh T, Tanoue D, Katabuchi H. Efficacy of a prospective community-based intervention to prevent preterm birth. J Perinat Med. 2016:1–7.Google Scholar
  99. 99.
    Ainamo J, Brames D, Beagrie G, Cutress T, Martin J, Sardo-Infirri J. Development of World Health Organization (WHO) community periodontal index of treatment needs (CPITN). Int Dent J. 1982;32:281–91.PubMedGoogle Scholar
  100. 100.
    Jiang H, Xiong X, Su Y, Peng J, Zhu X, Wang J, et al. Use of antiseptic mouthrinse during pregnancy and pregnancy outcomes: a randomized controlled clinical trial in rural China. An Intern J Obst Gynaec. 2016;123:39–47.CrossRefGoogle Scholar
  101. 101.
    Jeffcoat M, Parry S, Gerlach RW, Doyle MJ. Use of alcohol-free antimicrobial mouthrinse is associated with decreased incidence of preterm birth in a high-risk population. Am J Obstet Gynecol. 2011;205:382 e381–6.CrossRefGoogle Scholar
  102. 102.
    McDonald HM, O’Loughlin JA, Jolley PT, Vigneswaran R, McDonald PJ. Changes in vaginal flora during pregnancy and association with preterm birth. J Infect Dis. 1994;170:724–8.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Parry S, Strauss JF 3rd. Premature rupture of the fetal membranes. N Engl J Med. 1998;338:663–70.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Locksmith G, Duff P. Infection, antibiotics, and preterm delivery. Semin Perinatol. 2001;25:295–309.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Fogacci MF, Barbirato DS, Amaral CSF, da Silva PG, Coelho MO, Bertozi G, et al. No association between periodontitis, preterm birth, or intrauterine growth restriction: experimental study in Wistar rats. Am J Obstet Gynecol. 2016;214(749e):1–11.Google Scholar
  106. 106.
    Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Investig. 1976;34:235–49.PubMedPubMedCentralGoogle Scholar
  107. 107.
    Ohlrich EJ, Cullinam MP, Seymour GJ. The immunopathogenesis of periodontal disease. Aust Dent J. 2009;54(suppl1):S2–10.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Isogai E, Isogai H, Sawada H, Kaneko H, Ito N. Microbial ecology of plaque in rats with naturally occurring gingivitis. Infect Immun. 1985;48:520–7.PubMedPubMedCentralGoogle Scholar
  109. 109.
    Duarte PM, Tezolin KR, Figueiredo LC, Feres M, Bastos MF. Microbial profile of ligature- induced periodontitis in rats. Arch Oral Biol. 2010;55:142–7.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Rovin S, Costich ER, Gordon HA. The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J Periodontal Res. 1966;1:193–204.PubMedCrossRefGoogle Scholar
  111. 111.
    Györfi A, Fazekas A, Suba Z, Ender F, Rosivall L. Neurogenic component in ligature- induced periodontitis in the rat. J Clin Periodontol. 1994;21:601–5.PubMedCrossRefGoogle Scholar
  112. 112.
    Donesky BW, deMoura MD, Tedeschi C, Hurwitz A, Adashi EY, Payne DW. Interleukin- 1 inhibits steroidogenic bioactivity in cultured rat ovarian granulosa cells by stimulation of progesterone degradation and inhibition of estrogen formation. Biol Reprod. 1998;58:1108–16.PubMedCrossRefGoogle Scholar
  113. 113.
    Martoriati A, Gérard N. Interleukin-1 (IL-1) system gene expression in granulosa cells: kinetics during terminal preovulatory follicle maturation in the mare. Reprod Biol Endocrinol. 2003;1:42.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Sirivelu MP, Shin AC, Perez GI, MohanKumar PS, MohanKumar SMJ. Effect of L-dopa on interleukin-1b-induced sup- pression of luteinizing hormone secretion in intact female rats. Hum Reprod. 2009;24:718–25.PubMedCrossRefGoogle Scholar
  115. 115.
    Montrezor LH, Rosa e Silva AAM. Efeitos da endotelina-1 sobre a esteroidogênese e o crescimento celular em cultura de células da granulosa de bovinos. Braz J Vet Res Anim Sci. 2007;44:103–14.CrossRefGoogle Scholar
  116. 116.
    Collins JG, Windley HW, Arnold RR, Offenbacher S. Effects of a Porphyromonas gingivalis infection on inflammatory mediator response and pregnancy outcomes in ham- sters. Infect Immun. 1994a;62:4356–61.PubMedPubMedCentralGoogle Scholar
  117. 117.
    Collins JG, Smith MA, Arnold RR, Offenbacher S. Effects of E coli and P gingivalis lipopolysaccharide on pregnancy outcome in the golden hamster. Infect Immun. 1994b;62:4652–5.PubMedPubMedCentralGoogle Scholar
  118. 118.
    WHO: recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand. 1977;56:247–53.Google Scholar
  119. 119.
    WHO Health Organization. http://www.who.int/mediacentre/ factsheets/fs363/en/ (Accessed 4 Dec 2015).
  120. 120.
    WHO - World Health Organization, International statistical classification of diseases and related health problems, tenth revision. Geneva, 1992.Google Scholar
  121. 121.
    United Nations Children’s Fund; World Health Organization. Low birthweight: country, regional and global estimates; 2004 [cited 2016 May 28]. Available from: http://www.unicef. org/publications/files/low_birthweight_from_EY.pdf.
  122. 122.
    Miller WD. The human mouth as a focus of infection. Dent Cosmos. 1999;1891:698–713.Google Scholar
  123. 123.
    Hunter W. Oral sepsis as a cause of disease. Br Med J. 1900;2:215–6.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Galvão MP, Chapper A, Rösing CK, Ferreira MB, de Souza MA. Methodological considerations on descriptive studies of induced periodontal diseases in rats. Pesqui Odontol Bras. 2003;17:56–62.PubMedCrossRefGoogle Scholar
  125. 125.
    Lin D, Smith MA, Champagne C, Elter J, Beck J, Offenbacher S. Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect Immun. 2003;71:5156–62.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Yeo A, Smith MA, Lin D, Riché EL, Moore A, Elter J, et al. Campylobacter rectus mediates growth restriction in pregnant mice. J Periodontol. 2005;76:551–7.PubMedCrossRefGoogle Scholar
  127. 127.
    Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS. Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun. 2004;72:2272–9.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Liu H, Redline RW, Han YW. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol. 2007;179:2501–8.PubMedCrossRefGoogle Scholar
  129. 129.
    Newnham JP, Shub A, Jobe AH, Bird PS, Ikegami M, Nitsos I, et al. The effects of intra-amniotic injection of perio- dontopathic lipopolysaccharides in sheep. Am J Obstet Gynecol. 2005;193:313–21.PubMedCrossRefGoogle Scholar
  130. 130.
    Kramer MS. Determinants of low birth weight: methodological assessment and meta- analysis. Bull World Health Organ. 1987;65:663–737.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000. 1997;14:9–11.PubMedCrossRefGoogle Scholar
  132. 132.
    Borrell LN, Papapanou PN. Analytical epidemiology of periodontitis. J Clin Periodontol. 2005;32(suppl6):132–58.PubMedCrossRefGoogle Scholar
  133. 133.
    Slots J. and research, science and therapy committee. Systemic antibiotics in periodontics. J Periodontol. 2004;75:1553–65.PubMedCrossRefGoogle Scholar
  134. 134.
    López NJ, et al. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol. 2005;76:2144–53.PubMedCrossRefGoogle Scholar
  135. 135.
    Newnham JP, Newnham IA, Ball CM, Wright M, Pennell CE, Swain J, et al. Treatment of periodontal disease during pregnancy: a randomized controlled trial. Obstet Gynecol. 2009;114:1239–48.PubMedCrossRefGoogle Scholar
  136. 136.
    Rubenfire M, Grossman NS, Kaciroti N, Apsey DJ, Loesche WJ. Anaerobic dental flora and the acute coronary syndrome. Coron Artery Dis. 2007;18:111–6.PubMedCrossRefGoogle Scholar
  137. 137.
    Turton MS, Henkel RR, Africa CWJ. A simple point of care can indicate the need for periodontal therapy to reduce the risk for adverse pregnancy outcomes in mothers attending antenatal clinics. Biomarkers. 2017;22(8):740–6.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Davi da Silva Barbirato
    • 1
    Email author
  • Monique Oliveira Rodrigues
    • 2
  • Julianna Peres Alves
    • 3
  • Heric Pinheiro de Castro
    • 3
  • Mariana Fampa Fogacci
    • 4
  1. 1.Post-Doctorate, School of Dentistry of PernambucoFOP, University of PernambucoUFPE PEBrazil
  2. 2.Doctorate studentFederal University of Rio de Janeiro - UFRJRio de JaneiroBrazil
  3. 3.Graduate student, School of DentistryFaculdades Integradas Aparício Carvalho - FIMCAPorto VelhoBrazil
  4. 4.Professor, Department of Clinical and Preventive DentistryFederal University of PernambucoUFPE PEBrazil

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