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Published in: Archives of Gynecology and Obstetrics 6/2019

01-12-2019 | Premature Birth | Maternal-Fetal Medicine

Periodontopathogenic microbiota, infectious mechanisms and preterm birth: analysis with structural equations (cohort—BRISA)

Authors: Elisa Miranda Costa, Camilla Silva de Araujo Figueiredo, Rafiza Félix Marão Martins, Cecília Claudia Costa Ribeiro, Claudia Maria Coelho Alves, Maria Lúcia Talarico Sesso, Ruchele Dias Nogueira, Maria da Conceição Saraiva, Marco Antônio Barbieri, Heloisa Bettiol, Antônio Augusto Moura da Silva, Erika Bárbara Abreu Fonseca Thomaz

Published in: Archives of Gynecology and Obstetrics | Issue 6/2019

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Abstract

Purpose

The association between periodontopathogenic microbiota and preterm birth (PTB) has been overly studied. However, the biological mechanisms involved are little known. The objective is to evaluate the effect of periodontopathogenic bacteria burden (PBB), periodontal disease and other infections during pregnancy on preterm birth (PTB), through Structural Equation Modeling.

Methods

This was a case–control study nested in a prospective cohort called BRISA, including 330 pregnant women, 110 cases and 220 controls. This study included the following variables: cytokines interleukin-10 (IL-10) and transforming growth factor beta (TGF-β), periodontal disease, PBB, age, socioeconomic status (SES), systemic infections and PTB. The correlations between variables were analyzed using Standardized Coefficient (SC).

Results

Greater PBB interfered positively with the occurrence of periodontal disease (SC: 0.027; p: 0.011), but these were not associated with the cytokines studied, nor with PTB. The lower serum levels of IL-10 (SC − 0.330; p 0.022) and TGF-β (SC − 0.612; p  < 0.001), and the presence of other systemic infections during pregnancy (SC 0.159; 0.049) explained the higher occurrence of PTB.

Conclusion

It is possible that only the more severe periodontal disease and other systemic infections are capable of altering the cascade of cytokines regulating the inflammatory process and have an effect on the occurrence of PTB.
Literature
1.
go back to reference Chawanpaiboon S, Vogel JP, Moller AB, Lumbiganon P, Petzold M, Hogan D et al (2019) Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health. 7:37–46 Chawanpaiboon S, Vogel JP, Moller AB, Lumbiganon P, Petzold M, Hogan D et al (2019) Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health. 7:37–46
2.
go back to reference Silveira MF, Victora CG, Horta BL, da Silva BGC, Matijasevich A, Barros FC (2019) Low birthweight and preterm birth: trends and inequalities in four population-based birth cohorts in Pelotas, Brazil, 1982–2015. Int J Epidemiol 48:46–53 Silveira MF, Victora CG, Horta BL, da Silva BGC, Matijasevich A, Barros FC (2019) Low birthweight and preterm birth: trends and inequalities in four population-based birth cohorts in Pelotas, Brazil, 1982–2015. Int J Epidemiol 48:46–53
3.
go back to reference Stylianou-Riga P, Kouis P, Kinni P, Rigas A, Papadouri T, Yiallouros PK et al (2018) Maternal socioeconomic factors and the risk of premature birth and low birth weight in Cyprus: a case-control study. Reprod Health. 15:157PubMedPubMedCentral Stylianou-Riga P, Kouis P, Kinni P, Rigas A, Papadouri T, Yiallouros PK et al (2018) Maternal socioeconomic factors and the risk of premature birth and low birth weight in Cyprus: a case-control study. Reprod Health. 15:157PubMedPubMedCentral
4.
go back to reference Pizzo G, La Cara M, Conti Nibali M, Guiglia R (2005) Periodontitis and preterm delivery. A review of the literature. Minerva Stomatol. 54:1–14PubMed Pizzo G, La Cara M, Conti Nibali M, Guiglia R (2005) Periodontitis and preterm delivery. A review of the literature. Minerva Stomatol. 54:1–14PubMed
5.
go back to reference Xiong X, Buekens P, Fraser WD, Beck J, Offenbacher S (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 113:135–143 Xiong X, Buekens P, Fraser WD, Beck J, Offenbacher S (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 113:135–143
6.
go back to reference Pretorius C, Jagatt A, Lamont RF (2007) The relationship between periodontal disease, bacterial vaginosis, and preterm birth. J Perinat Med 35:93–99PubMed Pretorius C, Jagatt A, Lamont RF (2007) The relationship between periodontal disease, bacterial vaginosis, and preterm birth. J Perinat Med 35:93–99PubMed
7.
go back to reference HEC da Silva CM Stefani MN Santos de Almeida de Lima A Rosing CK Porporatti AL et al 2017 Effect of intra-pregnancy nonsurgical periodontal therapy on inflammatory biomarkers and adverse pregnancy outcomes: a systematic review with meta-analysis Syst Rev. 6 197 HEC da Silva CM Stefani MN Santos de Almeida de Lima A Rosing CK Porporatti AL et al 2017 Effect of intra-pregnancy nonsurgical periodontal therapy on inflammatory biomarkers and adverse pregnancy outcomes: a systematic review with meta-analysis Syst Rev. 6 197
8.
go back to reference Cobb CM, Kelly PJ, Williams KB, Babbar S, Angolkar M, Derman RJ (2017) The oral microbiome and adverse pregnancy outcomes. Int J Womens Health. 9:551–559PubMedPubMedCentral Cobb CM, Kelly PJ, Williams KB, Babbar S, Angolkar M, Derman RJ (2017) The oral microbiome and adverse pregnancy outcomes. Int J Womens Health. 9:551–559PubMedPubMedCentral
9.
go back to reference Corbella S, Taschieri S, Francetti L, De Siena F, Del Fabbro M (2012) Periodontal disease as a risk factor for adverse pregnancy outcomes: a systematic review and meta-analysis of case–control studies. Odontology. 100:232–240PubMed Corbella S, Taschieri S, Francetti L, De Siena F, Del Fabbro M (2012) Periodontal disease as a risk factor for adverse pregnancy outcomes: a systematic review and meta-analysis of case–control studies. Odontology. 100:232–240PubMed
10.
go back to reference Rosa MI, Pires PD, Medeiros LR, Edelweiss MI, Martinez-Mesa J (2012) Periodontal disease treatment and risk of preterm birth: a systematic review and meta-analysis. Cad Saude Publica. 28:1823–1833PubMed Rosa MI, Pires PD, Medeiros LR, Edelweiss MI, Martinez-Mesa J (2012) Periodontal disease treatment and risk of preterm birth: a systematic review and meta-analysis. Cad Saude Publica. 28:1823–1833PubMed
11.
go back to reference Corbella S, Taschieri S, Del Fabbro M, Francetti L, Weinstein R, Ferrazzi E (2016) Adverse pregnancy outcomes and periodontitis: A systematic review and meta-analysis exploring potential association. Quintessence Int. 47:193–204PubMed Corbella S, Taschieri S, Del Fabbro M, Francetti L, Weinstein R, Ferrazzi E (2016) Adverse pregnancy outcomes and periodontitis: A systematic review and meta-analysis exploring potential association. Quintessence Int. 47:193–204PubMed
12.
go back to reference Perunovic ND, Rakic MM, Nikolic LI, Jankovic SM, Aleksic ZM, Plecas DV et al (2016) The Association Between Periodontal Inflammation and Labor Triggers (Elevated Cytokine Levels) in Preterm Birth: A Cross-Sectional Study. J. Periodontol. 87:248–256PubMed Perunovic ND, Rakic MM, Nikolic LI, Jankovic SM, Aleksic ZM, Plecas DV et al (2016) The Association Between Periodontal Inflammation and Labor Triggers (Elevated Cytokine Levels) in Preterm Birth: A Cross-Sectional Study. J. Periodontol. 87:248–256PubMed
13.
go back to reference Tellapragada C, Eshwara VK, Bhat P, Acharya S, Kamath A, Bhat S et al (2016) Risk Factors for Preterm Birth and Low Birth Weight Among Pregnant Indian Women: A Hospital-based Prospective Study. J Prev Med Public Health 49:165–175PubMedPubMedCentral Tellapragada C, Eshwara VK, Bhat P, Acharya S, Kamath A, Bhat S et al (2016) Risk Factors for Preterm Birth and Low Birth Weight Among Pregnant Indian Women: A Hospital-based Prospective Study. J Prev Med Public Health 49:165–175PubMedPubMedCentral
14.
go back to reference Mesa F, Pozo E, Blanc V, Puertas A, Bravo M, O'Valle F (2013) Are periodontal bacterial profiles and placental inflammatory infiltrate in pregnancy related to birth outcomes? J Periodontol 84:1327–1336PubMed Mesa F, Pozo E, Blanc V, Puertas A, Bravo M, O'Valle F (2013) Are periodontal bacterial profiles and placental inflammatory infiltrate in pregnancy related to birth outcomes? J Periodontol 84:1327–1336PubMed
15.
go back to reference Iheozor-Ejiofor Z, Middleton P, Esposito M, Glenny AM (2017). Treating periodontal disease for preventing adverse birth outcomes in pregnant women. Cochrane Database Syst Rev. 6:CD005297. Iheozor-Ejiofor Z, Middleton P, Esposito M, Glenny AM (2017). Treating periodontal disease for preventing adverse birth outcomes in pregnant women. Cochrane Database Syst Rev. 6:CD005297.
16.
go back to reference Kline RB (2015). Principles and practice of structural equation modeling: Guilford publications. Kline RB (2015). Principles and practice of structural equation modeling: Guilford publications.
17.
go back to reference Kruse AB, Kuerschner AC, Kunze M, Woelber JP, Al-Ahmad A, Wittmer A et al (2018) Association between high risk for preterm birth and changes in gingiva parameters during pregnancy—a prospective cohort study. Clinical Oral Investig. 22:1263–1271 Kruse AB, Kuerschner AC, Kunze M, Woelber JP, Al-Ahmad A, Wittmer A et al (2018) Association between high risk for preterm birth and changes in gingiva parameters during pregnancy—a prospective cohort study. Clinical Oral Investig. 22:1263–1271
18.
go back to reference Lohana MH, Suragimath G, Patange RP, Varma S, Zope SA (2017) A Prospective Cohort Study to Assess and Correlate the Maternal Periodontal Status with Their Pregnancy Outcome. J Obstet Gynaecol India. 67:27–32PubMed Lohana MH, Suragimath G, Patange RP, Varma S, Zope SA (2017) A Prospective Cohort Study to Assess and Correlate the Maternal Periodontal Status with Their Pregnancy Outcome. J Obstet Gynaecol India. 67:27–32PubMed
19.
go back to reference Basha S, Swamy HS, Mohamed RN, Shivalinga Swamy H, Noor Mohamed R (2015) Maternal Periodontitis as a Possible Risk Factor for Preterm Birth and Low Birth Weight–A Prospective Study. Oral health Prev Dent. 13:537–544PubMed Basha S, Swamy HS, Mohamed RN, Shivalinga Swamy H, Noor Mohamed R (2015) Maternal Periodontitis as a Possible Risk Factor for Preterm Birth and Low Birth Weight–A Prospective Study. Oral health Prev Dent. 13:537–544PubMed
20.
go back to reference da Silva AA, Simoes VM, Barbieri MA, Cardoso VC, Alves CM, Thomaz EB et al (2014) A protocol to identify non-classical risk factors for preterm births: the Brazilian Ribeirao Preto and Sao Luis prenatal cohort (BRISA). Reprod Health. 11:79PubMedPubMedCentral da Silva AA, Simoes VM, Barbieri MA, Cardoso VC, Alves CM, Thomaz EB et al (2014) A protocol to identify non-classical risk factors for preterm births: the Brazilian Ribeirao Preto and Sao Luis prenatal cohort (BRISA). Reprod Health. 11:79PubMedPubMedCentral
21.
go back to reference Pesquisa ABdEd. Códigos e guias: CCEB-Critério de Classificação Econômica Brasil.: ABEP; 2009 [cited 2018]. Pesquisa ABdEd. Códigos e guias: CCEB-Critério de Classificação Econômica Brasil.: ABEP; 2009 [cited 2018].
22.
go back to reference Adriaens LM, Alessandri R, Spörri S, Lang NP, Persson GR (2009) Does pregnancy have an impact on the subgingival microbiota? J. Periodontol. 80:72–81PubMed Adriaens LM, Alessandri R, Spörri S, Lang NP, Persson GR (2009) Does pregnancy have an impact on the subgingival microbiota? J. Periodontol. 80:72–81PubMed
23.
go back to reference Carmo CDS, Ribeiro MRC, Teixeira JXP, Alves CMC, Franco MM, Franca A et al (2018) Added Sugar Consumption and Chronic Oral Disease Burden among Adolescents in Brazil. J Dent Res. 97:508–514PubMed Carmo CDS, Ribeiro MRC, Teixeira JXP, Alves CMC, Franco MM, Franca A et al (2018) Added Sugar Consumption and Chronic Oral Disease Burden among Adolescents in Brazil. J Dent Res. 97:508–514PubMed
24.
go back to reference Pereira TB, Thomaz EB, Nascimento FR, Santos AP, Batista RL, Bettiol H et al (2016) Regulatory Cytokine Expression and Preterm Birth: Case-Control Study Nested in a Cohort. PLoS ONE 11:e0158380PubMedPubMedCentral Pereira TB, Thomaz EB, Nascimento FR, Santos AP, Batista RL, Bettiol H et al (2016) Regulatory Cytokine Expression and Preterm Birth: Case-Control Study Nested in a Cohort. PLoS ONE 11:e0158380PubMedPubMedCentral
25.
go back to reference Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. 29:297–301PubMedPubMedCentral Nugent RP, Krohn MA, Hillier SL (1991) Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. 29:297–301PubMedPubMedCentral
27.
go back to reference Sood G, Argani C, Ghanem KG, Perl TM, Sheffield JS (2018) Infections complicating cesarean delivery. Curr Opin Infect Dis. 31:368–376PubMed Sood G, Argani C, Ghanem KG, Perl TM, Sheffield JS (2018) Infections complicating cesarean delivery. Curr Opin Infect Dis. 31:368–376PubMed
28.
go back to reference Barak S, Oettinger-Barak O, Machtei EE, Sprecher H, Ohel G (2007) Evidence of periodonpathogenic microorganisms in placentas of women with preeclampsia. J Periodontol. 78:670–676PubMed Barak S, Oettinger-Barak O, Machtei EE, Sprecher H, Ohel G (2007) Evidence of periodonpathogenic microorganisms in placentas of women with preeclampsia. J Periodontol. 78:670–676PubMed
29.
go back to reference Borgo PV, Rodrigues VA, Feitosa AC, Xavier KC, Avila-Campos MJ (2014) Association between periodontal condition and subgingival microbiota in women during pregnancy: a longitudinal study. J Appl Oral Sci. 22:528–533PubMedPubMedCentral Borgo PV, Rodrigues VA, Feitosa AC, Xavier KC, Avila-Campos MJ (2014) Association between periodontal condition and subgingival microbiota in women during pregnancy: a longitudinal study. J Appl Oral Sci. 22:528–533PubMedPubMedCentral
30.
go back to reference Machado FC, Cesar DE, Apolônio ACM, Ribeiro LC, Ribeiro RA (2016) Longitudinal study on clinical and microbial analysis of periodontal status in pregnancy. Braz. Oral Res. 30:1–8 Machado FC, Cesar DE, Apolônio ACM, Ribeiro LC, Ribeiro RA (2016) Longitudinal study on clinical and microbial analysis of periodontal status in pregnancy. Braz. Oral Res. 30:1–8
31.
go back to reference Armitage GC (2013) Bi-directional relationship between pregnancy and periodontal disease. Periodontol 2000(61):160–176 Armitage GC (2013) Bi-directional relationship between pregnancy and periodontal disease. Periodontol 2000(61):160–176
32.
go back to reference Shao H, Demuth DR (2010) Quorum sensing regulation of biofilm growth and gene expression by oral bacteria and periodontal pathogens. Periodontol 2000(52):53–67 Shao H, Demuth DR (2010) Quorum sensing regulation of biofilm growth and gene expression by oral bacteria and periodontal pathogens. Periodontol 2000(52):53–67
33.
go back to reference Scannapieco FA, Bush RB, Paju S (2003) Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Annals of Periodontology. 8:70–78PubMed Scannapieco FA, Bush RB, Paju S (2003) Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Annals of Periodontology. 8:70–78PubMed
34.
go back to reference Nugent JL, Baker PN (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 113:135–143 Nugent JL, Baker PN (2006) Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 113:135–143
35.
go back to reference Chambrone L, Pannuti CM, Guglielmetti MR, Chambrone LA (2011) Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: a systematic review of randomized trials evaluating the effects of periodontal treatment. J Clin Periodontol. 38:902–914PubMed Chambrone L, Pannuti CM, Guglielmetti MR, Chambrone LA (2011) Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: a systematic review of randomized trials evaluating the effects of periodontal treatment. J Clin Periodontol. 38:902–914PubMed
36.
go back to reference Martínez-Martínez RE, Moreno-Castillo DF, Loyola-Rodríguez JP, Sánchez-Medrano AG, San Miguel-Hernández JH, Olvera-Delgado JH et al (2016) Association between periodontitis, periodontopathogens and preterm birth: is it real? Arch Gynecol Obstet 294:47–54PubMed Martínez-Martínez RE, Moreno-Castillo DF, Loyola-Rodríguez JP, Sánchez-Medrano AG, San Miguel-Hernández JH, Olvera-Delgado JH et al (2016) Association between periodontitis, periodontopathogens and preterm birth: is it real? Arch Gynecol Obstet 294:47–54PubMed
37.
go back to reference Gargano JW, Holzman C, Senagore P, Thorsen P, Skogstrand K, Hougaard DM et al (2008) Mid-pregnancy circulating cytokine levels, histologic chorioamnionitis and spontaneous preterm birth. J Reprod Immunol. 79:100–110PubMedPubMedCentral Gargano JW, Holzman C, Senagore P, Thorsen P, Skogstrand K, Hougaard DM et al (2008) Mid-pregnancy circulating cytokine levels, histologic chorioamnionitis and spontaneous preterm birth. J Reprod Immunol. 79:100–110PubMedPubMedCentral
38.
go back to reference Denney JM, Nelson EL, Wadhwa PD, Waters TP, Mathew L, Chung EK et al (2011) Longitudinal modulation of immune system cytokine profile during pregnancy. Cytokine 53:170–177PubMed Denney JM, Nelson EL, Wadhwa PD, Waters TP, Mathew L, Chung EK et al (2011) Longitudinal modulation of immune system cytokine profile during pregnancy. Cytokine 53:170–177PubMed
39.
go back to reference Shigeru S, Akitoshi N, Subaru M-H, Shiozaki A (2008) The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy. J Reprod Immunol 77:14–22PubMed Shigeru S, Akitoshi N, Subaru M-H, Shiozaki A (2008) The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy. J Reprod Immunol 77:14–22PubMed
40.
go back to reference Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF 3rd, Petraglia F (2009) Inflammation and pregnancy. Reprod Sci. 16:206–215PubMed Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF 3rd, Petraglia F (2009) Inflammation and pregnancy. Reprod Sci. 16:206–215PubMed
41.
go back to reference Alijotas-Reig J, Llurba E, Gris JM (2014) Potentiating maternal immune tolerance in pregnancy: a new challenging role for regulatory T cells. Placenta 35:241–248PubMed Alijotas-Reig J, Llurba E, Gris JM (2014) Potentiating maternal immune tolerance in pregnancy: a new challenging role for regulatory T cells. Placenta 35:241–248PubMed
42.
go back to reference Schumacher A, Costa SD, Zenclussen AC (2014) Endocrine factors modulating immune responses in pregnancy. Front Immunol 5:196PubMedPubMedCentral Schumacher A, Costa SD, Zenclussen AC (2014) Endocrine factors modulating immune responses in pregnancy. Front Immunol 5:196PubMedPubMedCentral
43.
go back to reference Polliotti BM, Fry AG, Saller DN Jr, Mooney RA, Cox C, Miller RK (2003) Second-trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset preeclampsia. Obstet Gynecol 101:1266–1274PubMed Polliotti BM, Fry AG, Saller DN Jr, Mooney RA, Cox C, Miller RK (2003) Second-trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset preeclampsia. Obstet Gynecol 101:1266–1274PubMed
44.
go back to reference Harper M, Li L, Zhao Y, Klebanoff MA, Thorp JM Jr, Sorokin Y et al (2013) Change in mononuclear leukocyte responsiveness in midpregnancy and subsequent preterm birth. Obstet Gynecol. 121:805–811PubMed Harper M, Li L, Zhao Y, Klebanoff MA, Thorp JM Jr, Sorokin Y et al (2013) Change in mononuclear leukocyte responsiveness in midpregnancy and subsequent preterm birth. Obstet Gynecol. 121:805–811PubMed
45.
go back to reference Ferguson KK, McElrath TF, Chen YH, Mukherjee B, Meeker JD (2014) Longitudinal profiling of inflammatory cytokines and C-reactive protein during uncomplicated and preterm pregnancy. Am J Reprod Immunol. 72:326–336PubMedPubMedCentral Ferguson KK, McElrath TF, Chen YH, Mukherjee B, Meeker JD (2014) Longitudinal profiling of inflammatory cytokines and C-reactive protein during uncomplicated and preterm pregnancy. Am J Reprod Immunol. 72:326–336PubMedPubMedCentral
46.
go back to reference Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232PubMed Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232PubMed
47.
48.
go back to reference Shaarawy M, El Meleigy M, Rasheed K (2001) Maternal serum transforming growth factor beta-2 in preeclampsia and eclampsia, a potential biomarker for the assessment of disease severity and fetal outcome. J Soc Gynecol Investig. 8:27–31PubMed Shaarawy M, El Meleigy M, Rasheed K (2001) Maternal serum transforming growth factor beta-2 in preeclampsia and eclampsia, a potential biomarker for the assessment of disease severity and fetal outcome. J Soc Gynecol Investig. 8:27–31PubMed
49.
go back to reference Tsiartas P, Holst RM, Wennerholm UB, Hagberg H, Hougaard DM, Skogstrand K et al (2012) Prediction of spontaneous preterm delivery in women with threatened preterm labour: a prospective cohort study of multiple proteins in maternal serum. BJOG 119:866–873PubMed Tsiartas P, Holst RM, Wennerholm UB, Hagberg H, Hougaard DM, Skogstrand K et al (2012) Prediction of spontaneous preterm delivery in women with threatened preterm labour: a prospective cohort study of multiple proteins in maternal serum. BJOG 119:866–873PubMed
50.
go back to reference Miralles R, Hodge R, McParland PC, Field DJ, Bell SC, Taylor DJ, Grant WD, Kotecha S (2005) Relationship between antenatal inflammation and antenatal infection identified by detection of microbial genes by polymerase chain reaction. Pediatr Res. 57:473–474 Miralles R, Hodge R, McParland PC, Field DJ, Bell SC, Taylor DJ, Grant WD, Kotecha S (2005) Relationship between antenatal inflammation and antenatal infection identified by detection of microbial genes by polymerase chain reaction. Pediatr Res. 57:473–474
51.
go back to reference Vrachnis N, Vitoratos N, Iliodromiti Z, Sifakis S, Deligeoroglou E, Creatsas G (2010) Intrauterine inflammation and preterm delivery. Ann N Y Acad Sci. 1205:118–122PubMed Vrachnis N, Vitoratos N, Iliodromiti Z, Sifakis S, Deligeoroglou E, Creatsas G (2010) Intrauterine inflammation and preterm delivery. Ann N Y Acad Sci. 1205:118–122PubMed
52.
go back to reference Morris M, Nicoll A, Simms I, Wilson J, Catchpole M (2001) Bacterial vaginosis: a public health review. BJOG 108:439–450PubMed Morris M, Nicoll A, Simms I, Wilson J, Catchpole M (2001) Bacterial vaginosis: a public health review. BJOG 108:439–450PubMed
53.
go back to reference Sangkomkamhang US, Lumbiganon P, Prasertcharoensuk W, Laopaiboon M (2015) Antenatal lower genital tract infection screening and treatment programs for preventing preterm delivery (Review). Cochrane Database Syst Rev 2:1–27 Sangkomkamhang US, Lumbiganon P, Prasertcharoensuk W, Laopaiboon M (2015) Antenatal lower genital tract infection screening and treatment programs for preventing preterm delivery (Review). Cochrane Database Syst Rev 2:1–27
54.
go back to reference Brocklehurst P, Gordon A, Heatley E, Milan SJ (2013). Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst Rev. 31:CD000262 Brocklehurst P, Gordon A, Heatley E, Milan SJ (2013). Antibiotics for treating bacterial vaginosis in pregnancy. Cochrane Database Syst Rev. 31:CD000262
55.
go back to reference Baccaglini L (2011) A meta-analysis of randomized controlled trials shows no evidence that periodontal treatment during pregnancy prevents adverse pregnancy outcomes. J Am Dent Assoc. 142:1192–1193PubMed Baccaglini L (2011) A meta-analysis of randomized controlled trials shows no evidence that periodontal treatment during pregnancy prevents adverse pregnancy outcomes. J Am Dent Assoc. 142:1192–1193PubMed
56.
go back to reference Rosa MI, Pires PD, Medeiros LR, Edelweiss MI, Martínez-Mesa J (2012) Periodontal disease treatment and risk of preterm birth: a systematic review and meta-analysis. Cad Saude Publica. 28:1823–1833PubMed Rosa MI, Pires PD, Medeiros LR, Edelweiss MI, Martínez-Mesa J (2012) Periodontal disease treatment and risk of preterm birth: a systematic review and meta-analysis. Cad Saude Publica. 28:1823–1833PubMed
57.
go back to reference Polyzos NP, Polyzos IP, Zavos A, Valachis A, Mauri D, Papanikolaou EG, Tzioras S, Weber D, Messinis IE (2010) Obstetric outcomes after treatment of periodontal disease during pregnancy: systematic review and meta-analysis. BMJ 341:c7017PubMedPubMedCentral Polyzos NP, Polyzos IP, Zavos A, Valachis A, Mauri D, Papanikolaou EG, Tzioras S, Weber D, Messinis IE (2010) Obstetric outcomes after treatment of periodontal disease during pregnancy: systematic review and meta-analysis. BMJ 341:c7017PubMedPubMedCentral
58.
go back to reference López NJ, Uribe S (2000) Martinez B (2015) Effect of periodontal treatment on preterm birth rate: a systematic review of meta-analyses. Periodontol 67:87–130 López NJ, Uribe S (2000) Martinez B (2015) Effect of periodontal treatment on preterm birth rate: a systematic review of meta-analyses. Periodontol 67:87–130
59.
go back to reference Thomaz ÉB, Alves CM, Ribeiro CC, Batista RF, Simões VM, Cavalli R, Saraiva Mda C, Cardoso VC, Bettiol H, Barbieri MA, da Silva AA (2015) Perinatal outcomes and changes in the oral cavity: Brazilian cohorts of Ribeirão Preto and São Luís. Rev Bras Epidemiol. 18:966–970PubMed Thomaz ÉB, Alves CM, Ribeiro CC, Batista RF, Simões VM, Cavalli R, Saraiva Mda C, Cardoso VC, Bettiol H, Barbieri MA, da Silva AA (2015) Perinatal outcomes and changes in the oral cavity: Brazilian cohorts of Ribeirão Preto and São Luís. Rev Bras Epidemiol. 18:966–970PubMed
60.
go back to reference Cavalcante NCN, Simões VMF, Ribeiro MRC, Lamy-Filho F, Barbieri MA, Bettiol H, Silva AAMD (2017) Maternal socioeconomic factors and adverse perinatal outcomes in two birth cohorts, 1997/98 and 2010, in São Luís. Brazil. Rev Bras Epidemiol. 20:676–687PubMed Cavalcante NCN, Simões VMF, Ribeiro MRC, Lamy-Filho F, Barbieri MA, Bettiol H, Silva AAMD (2017) Maternal socioeconomic factors and adverse perinatal outcomes in two birth cohorts, 1997/98 and 2010, in São Luís. Brazil. Rev Bras Epidemiol. 20:676–687PubMed
61.
go back to reference Figueredo ED, Lamy F, Lamy ZC, Silva AAM (2014) Maternal age and adverse perinatal outcomes in a birth cohort (BRISA) from a Northeastern Brazilian city. Rev. Bras. Ginecol. Obstet. 6:562–568 Figueredo ED, Lamy F, Lamy ZC, Silva AAM (2014) Maternal age and adverse perinatal outcomes in a birth cohort (BRISA) from a Northeastern Brazilian city. Rev. Bras. Ginecol. Obstet. 6:562–568
Metadata
Title
Periodontopathogenic microbiota, infectious mechanisms and preterm birth: analysis with structural equations (cohort—BRISA)
Authors
Elisa Miranda Costa
Camilla Silva de Araujo Figueiredo
Rafiza Félix Marão Martins
Cecília Claudia Costa Ribeiro
Claudia Maria Coelho Alves
Maria Lúcia Talarico Sesso
Ruchele Dias Nogueira
Maria da Conceição Saraiva
Marco Antônio Barbieri
Heloisa Bettiol
Antônio Augusto Moura da Silva
Erika Bárbara Abreu Fonseca Thomaz
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
Archives of Gynecology and Obstetrics / Issue 6/2019
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-019-05355-x

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