Abstract
Purpose
To elucidate plausible associations between periodontal disease (PD) and pregnancy events through meta-analysis of original research published between 1998 and 2010.
Methods
One hundred and twenty-five randomized, case–control, matched-cohort studies on pregnancy and postpartum specifics in women with PD are identified through PubMed, LILACS, and Cochrane Register. Meta-study is performed on a sample of 992 births allocated from studies of level I-II-1 evidence. An oral inflammation score (OIS) is composed from parameteric and observational components of maternal PD. Pearson arrival process is modeled for exchangeable correlations.
Results
Women with preeclampsia and preterm birth have poor periodontal parameters in both, treatment and placebo groups (OR 1.94–2.9). In puerperae with severe periodontitis birth weight is negatively correlated with maternal probing depth (r = −0.368), and C-reactive protein (r = −0.416). Higher rates of tobacco use (RR 3.02), bacterial vaginosis (RR 2.7), clinical attachment level (OR 2.76), and fetal tyrosine kinase (OR 1.6) contribute in increased rates of preeclamsia (RR 1.68), and prematurity (RR 2.75). After adding confounders into the model OIS remains significantly associated with preterm birth (OR 2.3).
Conclusions
Maternal PD has strong associations with preeclampsia and prematurity.
Similar content being viewed by others
References
Adriaens LM, Alessandri R, Spörri S et al (2009) Does pregnancy have an impact on the subgingival microbiota? J Periodontol 80(1):72–81
Agueda A, Echeverría A, Manau C (2008) Association between periodontitis in pregnancy and preterm or low birth weight: review of the literature. Med Oral Patologia Oral Y Cirugia Bucal 13(9):E609–E615
Agueda A, Ramón JM, Manau C et al (2008) Periodontal disease as a risk factor for adverse pregnancy outcomes: a prospective cohort study. J Clin Periodontol 35(1):16–22
Akalin FA, Baltacioğlu E, Alver A et al (2009) Total antioxidant capacity and superoxide dismutaseactivity levels in serum and gingival crevicular fluid in pregnant women with chronic periodontitis. J Periodontol 80(3):457–467
Al-Habashneh R, Aljundi SH, Alwaeli HA (2008) Survey of medical doctors’ attitudes and knowledge of the association between oral health and pregnancy outcomes. Int J Dent Hyg 6(3):214–220
Alves RT, Ribeiro RA (2006) Relationship between maternal periodontal disease and birth of preterm low weight babies. Braz Oral Res 20(4):318–323
Anonymous (2006) Periodontal bacteria found in amniotic fluid. Br Dent J 203(2):65
Anonymous (2008) Periodontal disease may lead to gestational diabetes. J Am Dent Assoc 139(5):541
Betleja-Gromada K, Banach J, Kaczmarek A et al (2008) Anaerobic bacteria of periodontal pockets in course of periodontitis and premature labor. Med Dosw Mikrobiol 60(1):71–78
Bobetsis YA, Barros SP, Offenbacher S (2006) Exploring the relationship between periodontal disease and pregnancy complications. J Am Dent Assoc 137(suppl 2):7S–13S
Boggess KA (2005) Pathophysiology of preterm birth: emerging concepts of maternal infection. Clin Perinatol 32(3):561–569
Boggess KA, Lieff S, Murtha AP et al (2003) Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol 101(2):227–231
Bosnjak A, Relja T, Vucićević-Boras V et al (2006) Pre-term delivery and periodontal disease: a case–control study from Croatia. J Clin Periodontol 33(10):710–716
Boyarova TV, Dryankova MM, Bobeva AI et al (2001) Pregnancy and gingival hyperplasia. Folia Med 43(1–2):53–56
Canakci V, Canakci CF, Yildirim A et al (2007) Periodontal disease increases the risk of severe pre-eclampsia among pregnant women. J Clin Periodontol 34(8):639–645
Cappelli D, Steffen MJ, Holt SC et al (2009) Periodontitis in pregnancy: clinical and serum antibody observations from a baboon model of ligature-induced disease. J Periodontol 80(7):1154–1165
Carta G, Persia G, Falciglia K et al (2004) Periodontal disease and poor obstetrical outcome. Clin Exp Obstet Gynecol 31(1):47–49
Castaldi JL, Bertin MS, Giménez F et al (2006) Periodontal disease: is it a risk factor for premature labor, low birth weight or preeclampsia? Rev Panam Salud Publica 19(4):253–258
Clothier B, Stringer M, Jeffcoat MK (2007) Periodontal disease and pregnancy outcomes: exposure, risk and intervention. Best Pract Res Clin Obstet Gynecol 21(3):451–466
Cruz SS, Costa Mda C, Gomes-Filho IS et al (2009) Contribution of periodontal disease in pregnant women as a risk factor for low birth weight. Community Dent Oral Epidemiol 37(6):527–533
Dasanayake AP, Russell S, Boyd D et al (2003) Preterm low birth weight and periodontal disease among African Americans. Dent Clin N Am 47(1):115–125
Dasanayake AP, Chhun N, Tanner AC et al (2008) Periodontal pathogens and gestational diabetes mellitus. J Dent Res 87(4):328–333
Davenport ES (2004) Does periodontal disease affect pregnancy outcome? Br Dent J 197(5)
Davenport ES, Williams CE, Sterne JA et al (1998) The East London study of maternal chronic periodontal disease and preterm low birth weight infants: study design and prevalence data. Ann Periodontol 3(1):213–221
Durand R, Gunselman EL, Hodges JS et al (2009) A pilot study of the association between cariogenic oral bacteria and preterm birth. Oral Dis 15(6):400–406
Ebersole JL, Novak MJ, Michalowicz BS et al (2009) Systemic immune responses in pregnancy and periodontitis: relationship to pregnancy outcomes in the Obstetrics and Periodontal Therapy (OPT) study. J Periodontol 80(6):953–960
Fogacci MF, Leão A, Vettore MV et al (2010) Periodontal treatment completed before the 35th week of pregnancy appeared to have a beneficial effect on birth weight and time of delivery. Letter to the editor. J Dent Res 89(2):101; author reply 101–2
Gazolla CM, Ribeiro A, Moyses MR et al (2007) Evaluation of the incidence of preterm low birth weight in patients undergoing periodontal therapy. J Periodontol 78(5):842–848
Giglio JA, Lanni SM, Laskin DM et al (2009) Oral health care for the pregnant patient. J Can Dent Assoc 75(1):43–48
Gomes-Filho IS, Cruz SS, Rezende EJ et al (2007) Exposure measurement in the association between periodontal disease and prematurity/low birth weight. J Clin Periodontol 34(11):957–963
Grant WB (2008) High vitamin D and calcium requirements during pregnancy and tooth loss. Am J Public Health 98(11):1931–1932
Goldenberg RL, Culhane JF, Iams JD et al (2008) Epidemiology and causes of preterm birth. Lancet 371(9606):75–84
Guilbeau JR, Hurst H (2009) Brush up: periodontal disease and pregnancy. Nurs Womens Health 13(6):496–499
Güncü GN, Tözüm TF, Cağlayan F (2005) Effects of endogenous sex hormones on the periodontium—review of literature. Aust Dent J 50(3):138–145
Gürsoy M, Haraldsson G, Hyvönen M et al (2009) Does the frequency of Prevotella intermedia increase during pregnancy? Oral Microbiol Immunol 24(4):299–303
Heimonen A, Janket SJ, Kaaja R et al (2009) Oral inflammatory burden and preterm birth. J Periodontol 80(6):884–891
Heimonen A, Rintamäki H, Furuholm J et al (2008) Postpartum oral health parameters in women with preterm birth. Acta Odontol Scand 66(6):334–341
Herrera JA, Parra B, Herrera E et al (2007) Periodontal disease severity is related to high levels of C-reactive protein in pre-eclampsia. J Hypertens 25(7):1459–1464
Horton AL, Boggess KA, Moss KL et al (2008) Periodontal disease early in pregnancy is associated with maternal systemic inflammation among African American women. J Periodontol 79(7):1127–1132
Horton AL, Boggess KA, Moss KL et al (2009) Maternal periodontal disease and soluble fms-like tyrosine kinase-1 expression. J Periodontol 80(9):1506–1510
Indelicato F, Greco S, Messina G (1989) Periodontal disease during pregnancy. Stomatologica Mediterranea 9(1):49–55
Jared H, Boggess KA, Moss K et al (2009) Fetal exposure to oral pathogens and subsequent risk for neonatal intensive care admission. J Periodontol 80(6):878–883
Jarjoura K, Devine PC, Perez-Delboy A et al (2005) Markers of periodontal infection and preterm birth. Am J Obstet Gynecol 192(2):513–519
Katz J, Chegini N, Shiverick KT et al (2009) Localization of Porphyromonas gingivalis in preterm delivery placenta. J Dent Res 88(6):575–578
Khader YS, Jibreal M, Al-Omiri M et al (2006) Lack of association between periodontal parameters and preeclampsia. J Periodontol 77(10):1681–1687
Klebanoff M, Searle K (2006) The role of inflammation in preterm birth—focus on periodontitis. BJOG 113(Suppl 3):43–45
Konopka T (2004) Periodontitis and preterm low birth weight. Ginekol Pol 75(5):397–403
Konopka T, Rutkowska M, Hirnle L et al (2003) The secretion of prostaglandin E2 and interleukin 1-beta in women with periodontal diseases and preterm low-birth-weight. Bull Group Int Rech Sci Stomatol Odontol 45(1):18–28
Kugahara T, Shosenji Y, Ohashi K (2008) Screening for periodontitis in pregnant women with salivary enzymes. J Obstet Gynaecol Res 34(1):40–46
Kumar J, Samelson R (2009) Oral health care during pregnancy recommendations for oral health professionals. N Y State Dent J 75(6):29–33
Laine MA (2002) Effect of pregnancy on periodontal and dental health. Acta Odontol 60(5):257–264
Lang CT, Iams JD (2009) Goals and strategies for prevention of preterm birth: an obstetric perspective. Pediatr Clin North Am 56(3):537–563
Lohsoonthorn V, Kungsadalpipob K, Chanchareonsook P et al (2009) Maternal periodontal disease and risk of preeclampsia: a case–control study. Am J Hypertens 22(4):457–463
Lohsoonthorn V, Kungsadalpipob K, Chanchareonsook P et al (2009) Is maternal periodontal disease a risk factor for preterm delivery? Am J Epidemiol 169(6):731–739
Looney SW (2008) Re: treatment of periodontal disease and the risk of preterm birth. J Periodontol 79(1):1–2; author reply 2–3
López R (2008) Periodontal disease and adverse pregnancy outcomes. Evid Based Dent 9(2):48
Lopez NJ, Smith PC, Gutierrez J (2002) Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res 81(1):58–63
Louro PM, Fiori HH, Filho PL et al (2001) Periodontal disease in pregnancy and low birth weight. J Pediatr 77(1):23–28
Machtei EE, Mahler D, Sanduri H et al (2004) The effect of menstrual cycle on periodontal health. J Periodontol 75(3):408–412
Macones GA, Parry S, Nelson DB et al (2010) 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 202(2):147.e1–8
Manau C, Echeverria A, Agueda A et al (2008) Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. J Clin Periodontol 35(5):385–397
Marakoglu I, Gursoy UK, Marakoglu K et al (2008) Periodontitis as a risk factor for preterm low birth weight. Yonsei Med J 49(2):200–203
Marin C, Segura-Egea JJ, Martínez-Sahuquillo A et al (2005) Correlation between infant birth weight and mother’s periodontal status. J Clin Periodontol 32(3):299–304
Mariotti A (1994) Sex steroid hormones and cell dynamics in the periodontium. Crit Rev Oral Biol Med 5(1):27–53
Mayer Y, Levin L, Oettinger-Barak O et al (2008) Pregnancy and periodontal disease—is there a relation? Refuat Hapeh Vehashinayim 25(1):24–33, 82
McGaw T (2002) Periodontal disease and preterm delivery of low-birth-weight infants. J Can Dent Assoc 68(3):165–169
McElrath TF, Hecht JL, Dammann O et al (2008) Pregnancy disorders that lead to delivery before the 28th week of gestation: an epidemiologic approach to classification. Am J Epidemiol 168(9):980–989
Meijer van Putten JB (1998) Female hormones and oral health. Ned Tijdschr Tandheelkd 105(11):416–418
Meisel P, Reifenberger J, Haase R et al (2007) Women are periodontally healthier than men, but why don’t they have more teeth than men? Menopause 15(2):270–275
Menezes EV, Yakoob MY, Soomro T et al (2009) Reducing stillbirths: prevention and management of medical disorders and infections during pregnancy. BMC Pregnancy Childbirth 9 (Suppl 1):S4
Michalowicz BS, Novak MJ, Hodges JS et al (2009) Serum inflammatory mediators in pregnancy: changes after periodontal treatment and association with pregnancy outcomes. J Periodontol 80(11):1731–1741
Minozzi F, Chipaila N, Unfer V et al (2008) Odontostomatological approach to the pregnant patient. Eur Rev Med Pharmacol Sci 12(6):397–409
Moore S, Ide M, Coward PY et al (2004) A prospective study to investigate the relationship between periodontal disease and adverse pregnancy outcome. Br Dent J 197(5):251–258
Moore S, Randhawa M, Ide M (2005) A case–control study to investigate an association between adverse pregnancy outcome and periodontal disease. J Clin Periodontol 32(1):1–5
Moreu G, Tellez L, Gonzalez JM (2005) Relationship between maternal periodontal disease and low-birth-weight pre-term infants. J Clin Periodontol 32(6):622–627
Morgan MA, Crall J, Goldenberg RL et al (2009) Oral health during pregnancy. J Matern Fetal Neonatal Med 22(9):733–739
Murphey C, Rew L (2009) Three intervention models for exploring oral health in pregnant minority adolescents. J Spec Pediat Nurs 14(2):132–141
Newnham JP, Newnham IA, Ball CM et al (2009) Treatment of periodontal disease during pregnancy: a randomized controlled trial. Obstet Gynecol 114(6):1239–1248
Novák T, Radnai M, Gorzó I et al (2009) Prevention of preterm delivery with periodontal treatment. Fetal Diagn Ther 25(2):230–233
Offenbacher S, Boggess K, Murtha AP et al (2006) Progressive periodontal disease and risk of very preterm delivery. Obstet Gynecol 107(1):29–36
Offenbacher S, Beck JD, Jared HL et al (2009) Effects of periodontal therapy on rate of preterm delivery: a randomized controlled trial. Obstet Gynecol 114(3):551–559
Persson R, Hitti J, Verhelst R et al (2009) The vaginal microflora in relation to gingivitis. BMC Infect Dis 9:6
Persson GR, Hitti J, Paul K et al (2008) Tannerella forsythia and Pseudomonas aeruginosa in subgingival bacterial samples from parous women. J Periodontol 79(3):508–516
Pitiphat W, Joshipura KJ, Gillman MW et al (2008) Maternal periodontitis and adverse pregnancy outcomes. Community Dent Oral Epidemiol 36(1):3–11
Polyzos NP, Polyzos IP, Mauri D et al (2009) Effect of periodontal disease treatment during pregnancy on preterm birth incidence: a meta analysis of randomized trials. Am J Obstet Gynecol 200(3):225–232
Radnai M, Gorzó I, Nagy E et al (2007) The oral health status of postpartum mothers in South-East Hungary. Community Dent Health 24(2):111–116
Radnai M, Pál A, Novák T et al (2009) Benefits of periodontal therapy when preterm birth threatens. J Dent Res 88(3):280–284
Ressler-Maerlender J, Krishna R, Robison V (2005) Oral health during pregnancy: current research. J Womens Health (Larchmt) 14(10):):880–882
Ruma M, Boggess K, Moss K et al (2008) Maternal periodontal disease, systemic inflammation, and risk for preeclampsia. Am J Obstet Gynecol 198(4):389.e1–5
Sacco G, Carmagnola D, Abati S et al (2008) Periodontal disease and preterm birth relationship: a review of the literature. Minerva Stomatol 57(5):233–46, 246–50
Saddki N, Bachok N, Hussain NH et al (2008) The association between maternal periodontitis and low birth weight infants among Malay women. Community Dent Oral Epidemiol 36(4):296–304
Samant A, Chabra SK, Devi PK (1977) Gingivitis and periodontal disease in pregnancy. Obstet Gynecol Surv 32(3):140–141
Sánchez AR, Bagniewski S, Weaver AL et al (2007) Correlations between maternal periodontal conditions and preterm low birth weight infants. J Int Acad Periodontol 9(2):34–41
Sasahara J, Kikuchi A, Takakuwa K et al (2009) Antibody responses to Porphyromonas gingivalis outer membrane protein in the first trimester. Aust N Z J Obstet Gynaecol 49(2):137–141
Scannapieco FA, Bush RB (2003) Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Ann Periodontol 8(1):70–78
Sha YQ, Huang Z, Chen ZB et al (2009) Association between periodontitis and preterm low birth weight. Beijing Da Xue Xue Bao 41(1):117–120
Sharma R, Maimanuku LR, Morse Z et al (2007) Preterm low birth weights associated with periodontal disease in the Fiji Islands. Int Dent J 57(4):257–260
Shenoy RP, Nayak DG, Sequeira PS et al (2009) Periodontal disease as a risk factor in pre-term low birth weight—an assessment of gynecologists’ knowledge: a pilot study. Indian J Dent Res 20(1):13–16
Shub A, Wong C, Jennings B et al (2009) Maternal periodontal disease and perinatal mortality. Aust N Z J Obstet Gynecol 49(2):130–136
Simonson LG, Goodman CH, Bial JJ et al (1988) Quantitative relationship of Treponema denticola to severity of periodontal disease. Infect Immun 56(4):726–728
Silk H, Douglass AB, Douglass JM, Silk L (2008) Oral health during pregnancy. Am Fam Physician 77(8):1139–1144
Siqueira FM, Cota LO, Costa JE et al (2008) Maternal periodontitis as a potential risk variable for preeclampsia: a case–control study. J Periodontol 79(2):207–215
Srinivas SK, Sammel MD, Stamilio DM et al (2009) Periodontal disease and adverse pregnancy outcomes: is there an association? Am J Obstet Gynecol 200(5):497.e1–8
Tanaka K, Miyake Y, Sasaki S et al (2006) Magnesium intake is inversely associated with the prevalence of tooth loss in Japanese pregnant women: the Osaka Maternal and Child Health Study. Magnes Res 19(4):268–275
Tanaka K, Miyake Y, Sasaki S et al (2007) Relationship between intake of vegetables, fruit, and grains and the prevalence of tooth loss in Japanese women. J Nutr Sci Vitaminol (Tokyo) 53(6):522–528
Tandon S, D’Silva I (2003) Periodontal physiology during pregnancy. Indian J Physiol Pharmacol 47(4):367–372
Tarannum F, Faizuddin M (2007) Effect of periodontal therapy on pregnancy outcome in women affected by periodontitis. J Periodontol 78(11):2095–2103
Urbán E, Radnai M, Novák T et al (2006) Distribution of anaerobic bacteria among pregnant periodontitis patients who experience preterm delivery. Anaerobe 12(1):52–57
Vergnes JN (2008) Studies suggest an association between maternal periodontal disease and pre-eclampsia. Evid Based Dent 9(2):46–47
Vergnes JN, Sixou M (2007) Preterm low birth weight and maternal periodontal status: a meta-analysis. Am J Obstet Gynecol 196(2):135.e1–7
Vettore MV, Leão AT, Leal Mdo C et al (2008) The relationship between periodontal disease and preterm low birth weight: clinical and microbiological results. J Periodontal Res 43(6):615–626
Walker AR (1998) A tooth per child? Lancet 352(9137):1386
Wilder R, Robinson C, Jared HL et al (2007) Obstetricians’ knowledge and practice behaviors concerning periodontal health and preterm delivery and low birth weight. J Dent Hygiene 81(4):81
Williams RC (2008) Understanding and managing periodontal diseases: a notable past, a promising future. J Periodontol 79(8 Suppl):1552–1559
Wimmer G, Pihlstrom BL (2008) A critical assessment of adverse pregnancy outcome and periodontal disease. J Clin Periodontol 35(8 Suppl):380–397
Wood S, Frydman A, Cox S et al (2006) Periodontal disease and spontaneous preterm birth: a case–control study. BMC J Pregnancy Birth 6(24)
Wrzosek T, Einarson A (2009) Dental care during pregnancy. Can Fam Physician 55(6):598–599
Xiong X, Buekens P, Vastardis S, Wu T (2006) Periodontal disease as one possible explanation for the Mexican paradox. Med Hypotheses 67(6):1348–1354
Xiong X, Buekens P, Fraser WD et al (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. Obstet Gynecol Surv 61(5):307–309
Xiong X, Buekens P, Vastardis S, Yu SM (2007) Periodontal disease and pregnancy outcomes: state-of-the-science. Obstet Gynecol Surv 62(9):605–615
Yamoah KK, Lindow S, Karsai L (2009) A large epulis in pregnancy. J Obstet Gynecol 29(8):761–762
Yeo BK, Lim LP, Paquette DW et al (2005) Periodontal disease—the emergence of a risk for systemic conditions: pre-term low birth weight. Ann Acad Med Singap 34(1):111–116
Zachariasen RD (1989) Ovarian hormones and oral health: pregnancy gingivitis. Compendium 10(9):508–512
Zadeh-Modarres S, Amooian B, Bayat-Movahed S et al (2007) Periodontal health in mothers of preterm and term infants. Taiwan J Obstet Gynecol 46(2):157–161
Zanata RL, Fernandes KB, Navarro PS (2008) Prenatal dental care: evaluation of professional knowledge of obstetricians and dentists in the cities of Londrina/PR and Bauru/SP, Brazil. J Appl Oral Sci 16(3):194–200
Conflict of interest
None declared.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matevosyan, N.R. Periodontal disease and perinatal outcomes. Arch Gynecol Obstet 283, 675–686 (2011). https://doi.org/10.1007/s00404-010-1774-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00404-010-1774-9