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Published in: Clinical Oral Investigations 12/2020

01-12-2020 | Preterm Labor | Original Article

The periodontopathic bacteria in placenta, saliva and subgingival plaque of threatened preterm labor and preterm low birth weight cases: a longitudinal study in Japanese pregnant women

Authors: Changchang Ye, Sayaka Katagiri, Naoyuki Miyasaka, Hiroaki Kobayashi, Thatawee Khemwong, Toshiyuki Nagasawa, Yuichi Izumi

Published in: Clinical Oral Investigations | Issue 12/2020

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Abstract

Objectives

This study determined the quantity of periodontopathic bacteria in saliva, subgingival plaque, and placenta on the threatened preterm labor (TPL) and preterm low birth weight (PLBW) subjects in order to identify specific periodontal pathogens with high association to adverse pregnancy outcomes.

Methods

We used real-time PCR with TaqMan probe and ELISA to detect the amount of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia, Treponema denticola, Fusobacterium nucleatum, and Prevotella intermedia in subgingival plaque, saliva, and placenta tissue, in addition to serum IgG titers against these bacteria in 28 patients with TPL and 36 healthy pregnant women.

Results

Thirteen of 64 births delivered PLBW infants. All 6 periodontopathic bacteria were detected in the placenta samples. The amount of F. nucleatum and detection frequency of T. denticola in placental samples was significantly higher in the TPL group than in the healthy group. Meanwhile, the age, anti-P. gingival IgG in serum, amount of P. gingivalis and T. forsythia in plaque samples, detection frequency of P. intermedia in saliva, and percentage of pocket probing depth ≥ 5 mm were higher in TPL-PLBW births than those in TPL-Healthy delivery (HD) group and/or in H-HD group. Ordinal logistic regression analysis revealed that the presence of F. nucleatum in placental tissues was significantly associated with TPL, while the maternal age was significantly associated with PLBW in TPL.

Conclusion

Our findings suggested all 6 bacteria may access the placenta. The increased presence of F. nucleatum in placenta might be related to TPL, while advanced maternal age might be associated with PLBW in TPL.

Clinical relevance

Periodontal therapy should be applied to reduce the deep periodontal pocket sites and the colonization of periodontal pathogens in high-risk population.
Literature
1.
go back to reference Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366(9499):1809–1820PubMed Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366(9499):1809–1820PubMed
2.
go back to reference Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27(6):409–419PubMedPubMedCentral Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27(6):409–419PubMedPubMedCentral
3.
go back to reference Lamont RJ, Hajishengallis G (2015) Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 21(3):172–183PubMed Lamont RJ, Hajishengallis G (2015) Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 21(3):172–183PubMed
4.
go back to reference Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, McKaig R, Beck J (1996) Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67(10 Suppl):1103–1113PubMed Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, McKaig R, Beck J (1996) Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67(10 Suppl):1103–1113PubMed
5.
go back to reference Ye C, Katagiri S, Miyasaka N, Bharti P, Kobayashi H, Takeuchi Y, Momohara Y, Sekiguchi M, Takamine S, Nagasawa T, Izumi Y (2013) The anti-phospholipid antibody-dependent and independent effects of periodontopathic bacteria on threatened preterm labor and preterm birth. Arch Gynecol Obstet 288(1):65–72PubMed Ye C, Katagiri S, Miyasaka N, Bharti P, Kobayashi H, Takeuchi Y, Momohara Y, Sekiguchi M, Takamine S, Nagasawa T, Izumi Y (2013) The anti-phospholipid antibody-dependent and independent effects of periodontopathic bacteria on threatened preterm labor and preterm birth. Arch Gynecol Obstet 288(1):65–72PubMed
6.
go back to reference Khader YS, Ta'ani Q (2005) Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis. J Periodontol 76(2):161–165PubMed Khader YS, Ta'ani Q (2005) Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis. J Periodontol 76(2):161–165PubMed
7.
go back to reference Lohsoonthorn V, Qiu C, Williams MA (2007) Maternal serum C-reactive protein concentrations in early pregnancy and subsequent risk of preterm delivery. Clin Biochem 40(5–6):330–335PubMedPubMedCentral Lohsoonthorn V, Qiu C, Williams MA (2007) Maternal serum C-reactive protein concentrations in early pregnancy and subsequent risk of preterm delivery. Clin Biochem 40(5–6):330–335PubMedPubMedCentral
8.
go back to reference Sugita N, Kobayashi T, Kikuchi A, Shimada Y, Hirano E, Sasahara J, Tanaka K, Yoshie H (2012) Immunoregulatory gene polymorphisms in Japanese women with preterm births and periodontitis. J Reprod Immunol 93(2):94–101PubMed Sugita N, Kobayashi T, Kikuchi A, Shimada Y, Hirano E, Sasahara J, Tanaka K, Yoshie H (2012) Immunoregulatory gene polymorphisms in Japanese women with preterm births and periodontitis. J Reprod Immunol 93(2):94–101PubMed
9.
go back to reference Leon R, Silva N, Ovalle A, Chaparro A, Ahumada A, Gajardo M, Martinez M, Gamonal J (2007) Detection of Porphyromonas gingivalis in the amniotic fluid in pregnant women with a diagnosis of threatened premature labor. J Periodontol 78(7):1249–1255PubMed Leon R, Silva N, Ovalle A, Chaparro A, Ahumada A, Gajardo M, Martinez M, Gamonal J (2007) Detection of Porphyromonas gingivalis in the amniotic fluid in pregnant women with a diagnosis of threatened premature labor. J Periodontol 78(7):1249–1255PubMed
10.
go back to reference Han YW, Fardini Y, Chen C, Iacampo KG, Peraino VA, Shamonki JM, Redline RW Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115(2 Pt 2):442–445 Han YW, Fardini Y, Chen C, Iacampo KG, Peraino VA, Shamonki JM, Redline RW Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115(2 Pt 2):442–445
11.
go back to reference Swati P, Thomas B, Vahab SA, Kapaettu S, Kushtagi P (2012) Simultaneous detection of periodontal pathogens in subgingival plaque and placenta of women with hypertension in pregnancy. Arch Gynecol Obstet 285(3):613–619PubMed Swati P, Thomas B, Vahab SA, Kapaettu S, Kushtagi P (2012) Simultaneous detection of periodontal pathogens in subgingival plaque and placenta of women with hypertension in pregnancy. Arch Gynecol Obstet 285(3):613–619PubMed
12.
go back to reference Daly CG, Mitchell DH, Highfield JE, Grossberg DE, Stewart D (2001) Bacteremia due to periodontal probing: a clinical and microbiological investigation. J Periodontol 72(2):210–214PubMed Daly CG, Mitchell DH, Highfield JE, Grossberg DE, Stewart D (2001) Bacteremia due to periodontal probing: a clinical and microbiological investigation. J Periodontol 72(2):210–214PubMed
13.
go back to reference Champagne CM, Madianos PN, Lieff S, Murtha AP, Beck JD, Offenbacher S (2000) Periodontal medicine: emerging concepts in pregnancy outcomes. J Int Acad Periodontol 2(1):9–13PubMed Champagne CM, Madianos PN, Lieff S, Murtha AP, Beck JD, Offenbacher S (2000) Periodontal medicine: emerging concepts in pregnancy outcomes. J Int Acad Periodontol 2(1):9–13PubMed
14.
go back to reference Uehara R, Miura F, Itabashi K, Fujimura M, Nakamura Y (2011) Distribution of birth weight for gestational age in Japanese infants delivered by cesarean section. J Epidemiol 21(3):217–222PubMedPubMedCentral Uehara R, Miura F, Itabashi K, Fujimura M, Nakamura Y (2011) Distribution of birth weight for gestational age in Japanese infants delivered by cesarean section. J Epidemiol 21(3):217–222PubMedPubMedCentral
15.
go back to reference O'Leary TJ, Drake RB, Naylor JE (1972) The plaque control record. J Periodontol 43(1):38PubMed O'Leary TJ, Drake RB, Naylor JE (1972) The plaque control record. J Periodontol 43(1):38PubMed
16.
go back to reference Ramfjord SP (1959) Indices for prevalence and incidence of periodontal disease. J Periodontol 30(1):51–59 Ramfjord SP (1959) Indices for prevalence and incidence of periodontal disease. J Periodontol 30(1):51–59
17.
go back to reference Amodini Rajakaruna G, Umeda M, Uchida K, Furukawa A, Yuan B, Suzuki Y, Noriko E, Izumi Y, Eishi Y (2012) Possible translocation of periodontal pathogens into the lymph nodes draining the oral cavity. J Microbiol 50(5):827–836PubMed Amodini Rajakaruna G, Umeda M, Uchida K, Furukawa A, Yuan B, Suzuki Y, Noriko E, Izumi Y, Eishi Y (2012) Possible translocation of periodontal pathogens into the lymph nodes draining the oral cavity. J Microbiol 50(5):827–836PubMed
18.
go back to reference Yoshida A, Kawada M, Suzuki N, Nakano Y, Oho T, Saito T, Yamashita Y (2004) TaqMan real-time polymerase chain reaction assay for the correlation of Treponema denticola numbers with the severity of periodontal disease. Oral Microbiol Immunol 19(3):196–200PubMed Yoshida A, Kawada M, Suzuki N, Nakano Y, Oho T, Saito T, Yamashita Y (2004) TaqMan real-time polymerase chain reaction assay for the correlation of Treponema denticola numbers with the severity of periodontal disease. Oral Microbiol Immunol 19(3):196–200PubMed
19.
go back to reference Khemwong T, Kobayashi H, Ikeda Y, Matsuura T, Sudo T, Kano C, Mikami R, Izumi Y (2019) Fretibacterium sp. human oral taxon 360 is a novel biomarker for periodontitis screening in the Japanese population. PLoS One 14(6):e0218266PubMedPubMedCentral Khemwong T, Kobayashi H, Ikeda Y, Matsuura T, Sudo T, Kano C, Mikami R, Izumi Y (2019) Fretibacterium sp. human oral taxon 360 is a novel biomarker for periodontitis screening in the Japanese population. PLoS One 14(6):e0218266PubMedPubMedCentral
20.
go back to reference Ishikawa I, Watanabe H, Horibe M, Izumi Y (1988) Diversity of IgG antibody responses in the patients with various types of periodontitis. Adv Dent Res 2(2):334–338PubMed Ishikawa I, Watanabe H, Horibe M, Izumi Y (1988) Diversity of IgG antibody responses in the patients with various types of periodontitis. Adv Dent Res 2(2):334–338PubMed
21.
go back to reference Yano-Higuchi K, Takamatsu N, He T, Umeda M, Ishikawa I (2000) Prevalence of Bacteroides forsythus, Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in subgingival microflora of Japanese patients with adult and rapidly progressive periodontitis. J Clin Periodontol 27(8):597–602PubMed Yano-Higuchi K, Takamatsu N, He T, Umeda M, Ishikawa I (2000) Prevalence of Bacteroides forsythus, Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in subgingival microflora of Japanese patients with adult and rapidly progressive periodontitis. J Clin Periodontol 27(8):597–602PubMed
22.
go back to reference Takeuchi Y, Guggenheim B, Filieri A, Baehni P (2007) Effect of chlorhexidine/thymol and fluoride varnishes on dental biofilm formation in vitro. Eur J Oral Sci 115(6):468–472PubMed Takeuchi Y, Guggenheim B, Filieri A, Baehni P (2007) Effect of chlorhexidine/thymol and fluoride varnishes on dental biofilm formation in vitro. Eur J Oral Sci 115(6):468–472PubMed
23.
go back to reference Koseki T, Benno Y, Zhang-Koseki YJ, Umeda M, Ishikawa I (1996) Detection frequencies and the colony-forming unit recovery of oral treponemes by different cultivation methods. Oral Microbiol Immunol 11(3):203–208PubMed Koseki T, Benno Y, Zhang-Koseki YJ, Umeda M, Ishikawa I (1996) Detection frequencies and the colony-forming unit recovery of oral treponemes by different cultivation methods. Oral Microbiol Immunol 11(3):203–208PubMed
24.
go back to reference Vergnes JN, Sixou M (2007) Preterm low birth weight and maternal periodontal status: a meta-analysis. Am J Obstet Gynecol 196(2):135 e131–135 e137 Vergnes JN, Sixou M (2007) Preterm low birth weight and maternal periodontal status: a meta-analysis. Am J Obstet Gynecol 196(2):135 e131–135 e137
25.
go back to reference Ide M, Papapanou PN (2013) Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes--systematic review. J Clin Periodontol 40(Suppl 14):S181–S194PubMed Ide M, Papapanou PN (2013) Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes--systematic review. J Clin Periodontol 40(Suppl 14):S181–S194PubMed
26.
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(2):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(2):232–240PubMed
27.
go back to reference Lin D, Smith MA, Elter J, Champagne C, Downey CL, Beck J, Offenbacher S (2003) Porphyromonas gingivalis infection in pregnant mice is associated with placental dissemination, an increase in the placental Th1/Th2 cytokine ratio, and fetal growth restriction. Infect Immun 71(9):5163–5168PubMedPubMedCentral Lin D, Smith MA, Elter J, Champagne C, Downey CL, Beck J, Offenbacher S (2003) Porphyromonas gingivalis infection in pregnant mice is associated with placental dissemination, an increase in the placental Th1/Th2 cytokine ratio, and fetal growth restriction. Infect Immun 71(9):5163–5168PubMedPubMedCentral
28.
go back to reference Udagawa S, Katagiri S, Maekawa S, Takeuchi Y, Komazaki R, Ohtsu A, Sasaki N, Shiba T, Watanabe K, Ishihara K, Sato N, Miyasaka N, Izumi Y (2018) Effect of Porphyromonas gingivalis infection in the placenta and umbilical cord in pregnant mice with low birth weight. Acta Odontol Scand 76(6):433–441PubMed Udagawa S, Katagiri S, Maekawa S, Takeuchi Y, Komazaki R, Ohtsu A, Sasaki N, Shiba T, Watanabe K, Ishihara K, Sato N, Miyasaka N, Izumi Y (2018) Effect of Porphyromonas gingivalis infection in the placenta and umbilical cord in pregnant mice with low birth weight. Acta Odontol Scand 76(6):433–441PubMed
29.
go back to reference Ao M, Miyauchi M, Furusho H, Inubushi T, Kitagawa M, Nagasaki A, Sakamoto S, Kozai K, Takata T (2015) Dental infection of Porphyromonas gingivalis induces preterm birth in mice. PLoS One 10(8):e0137249PubMedPubMedCentral Ao M, Miyauchi M, Furusho H, Inubushi T, Kitagawa M, Nagasaki A, Sakamoto S, Kozai K, Takata T (2015) Dental infection of Porphyromonas gingivalis induces preterm birth in mice. PLoS One 10(8):e0137249PubMedPubMedCentral
30.
go back to reference Hasegawa-Nakamura K, Tateishi F, Nakamura T, Nakajima Y, Kawamata K, Douchi T, Hatae M, Noguchi K (2011) The possible mechanism of preterm birth associated with periodontopathic Porphyromonas gingivalis. J Periodontal Res 46(4):497–504PubMed Hasegawa-Nakamura K, Tateishi F, Nakamura T, Nakajima Y, Kawamata K, Douchi T, Hatae M, Noguchi K (2011) The possible mechanism of preterm birth associated with periodontopathic Porphyromonas gingivalis. J Periodontal Res 46(4):497–504PubMed
31.
go back to reference Katz J, Chegini N, Shiverick KT, Lamont RJ (2009) Localization of P. gingivalis in preterm delivery placenta. J Dent Res 88(6):575–578PubMedPubMedCentral Katz J, Chegini N, Shiverick KT, Lamont RJ (2009) Localization of P. gingivalis in preterm delivery placenta. J Dent Res 88(6):575–578PubMedPubMedCentral
32.
go back to reference Vanterpool SF, Been JV, Houben ML, Nikkels PG, De Krijger RR, Zimmermann LJ, Kramer BW, Progulske-Fox A, Reyes L (2016) Porphyromonas gingivalis within placental villous mesenchyme and umbilical cord Stroma is associated with adverse pregnancy outcome. PLoS One 11(1):e0146157PubMedPubMedCentral Vanterpool SF, Been JV, Houben ML, Nikkels PG, De Krijger RR, Zimmermann LJ, Kramer BW, Progulske-Fox A, Reyes L (2016) Porphyromonas gingivalis within placental villous mesenchyme and umbilical cord Stroma is associated with adverse pregnancy outcome. PLoS One 11(1):e0146157PubMedPubMedCentral
33.
go back to reference Cobe HM (1954) Transitory bacteremia. Oral Surg Oral Med Oral Pathol 7(6):609–615PubMed Cobe HM (1954) Transitory bacteremia. Oral Surg Oral Med Oral Pathol 7(6):609–615PubMed
34.
go back to reference Kinane DF, Riggio MP, Walker KF, MacKenzie D, Shearer B (2005) Bacteraemia following periodontal procedures. J Clin Periodontol 32(7):708–713PubMed Kinane DF, Riggio MP, Walker KF, MacKenzie D, Shearer B (2005) Bacteraemia following periodontal procedures. J Clin Periodontol 32(7):708–713PubMed
35.
go back to reference Lineberger LT, De Marco TJ (1973) Evaluation of transient bacteremia following routine periodontal procedures. J Periodontol 44(12):757–762PubMed Lineberger LT, De Marco TJ (1973) Evaluation of transient bacteremia following routine periodontal procedures. J Periodontol 44(12):757–762PubMed
36.
go back to reference Lockhart PB, Brennan MT, Sasser HC, Fox PC, Paster BJ, Bahrani-Mougeot FK (2008) Bacteremia associated with toothbrushing and dental extraction. Circulation 117(24):3118–3125PubMedPubMedCentral Lockhart PB, Brennan MT, Sasser HC, Fox PC, Paster BJ, Bahrani-Mougeot FK (2008) Bacteremia associated with toothbrushing and dental extraction. Circulation 117(24):3118–3125PubMedPubMedCentral
37.
go back to reference LaPorte DM, Waldman BJ, Mont MA, Hungerford DS (1999) Infections associated with dental procedures in total hip arthroplasty. J Bone Joint Surg (Br) 81(1):56–59 LaPorte DM, Waldman BJ, Mont MA, Hungerford DS (1999) Infections associated with dental procedures in total hip arthroplasty. J Bone Joint Surg (Br) 81(1):56–59
38.
go back to reference Cassini MA, Pilloni A, Condo SG, Vitali LA, Pasquantonio G, Cerroni L (2013) Periodontal bacteria in the genital tract: are they related to adverse pregnancy outcome? Int J Immunopathol Pharmacol 26(4):931–939PubMed Cassini MA, Pilloni A, Condo SG, Vitali LA, Pasquantonio G, Cerroni L (2013) Periodontal bacteria in the genital tract: are they related to adverse pregnancy outcome? Int J Immunopathol Pharmacol 26(4):931–939PubMed
39.
go back to reference Lannon SMR, Adams Waldorf KM, Fiedler T, Kapur RP, Agnew K, Rajagopal L, Gravett MG, Fredricks DN (2019) Parallel detection of lactobacillus and bacterial vaginosis-associated bacterial DNA in the chorioamnion and vagina of pregnant women at term. J Matern Fetal Neonatal Med 32(16):2702–2710PubMed Lannon SMR, Adams Waldorf KM, Fiedler T, Kapur RP, Agnew K, Rajagopal L, Gravett MG, Fredricks DN (2019) Parallel detection of lactobacillus and bacterial vaginosis-associated bacterial DNA in the chorioamnion and vagina of pregnant women at term. J Matern Fetal Neonatal Med 32(16):2702–2710PubMed
40.
go back to reference Liu CJ, Liang X, Niu ZY, Jin Q, Zeng XQ, Wang WX, Li MY, Chen XR, Meng HY, Shen R, Sun SY, Luo YY, Yang E, Geng JW, Li XR (2019) Is the delivery mode a critical factor for the microbial communities in the meconium? EBioMedicine 49:354–363PubMedPubMedCentral Liu CJ, Liang X, Niu ZY, Jin Q, Zeng XQ, Wang WX, Li MY, Chen XR, Meng HY, Shen R, Sun SY, Luo YY, Yang E, Geng JW, Li XR (2019) Is the delivery mode a critical factor for the microbial communities in the meconium? EBioMedicine 49:354–363PubMedPubMedCentral
41.
go back to reference Doyle RM, Alber DG, Jones HE, Harris K, Fitzgerald F, Peebles D, Klein N (2014) Term and preterm labour are associated with distinct microbial community structures in placental membranes which are independent of mode of delivery. Placenta 35(12):1099–1101PubMed Doyle RM, Alber DG, Jones HE, Harris K, Fitzgerald F, Peebles D, Klein N (2014) Term and preterm labour are associated with distinct microbial community structures in placental membranes which are independent of mode of delivery. Placenta 35(12):1099–1101PubMed
42.
go back to reference Gonzales-Marin C, Spratt DA, Allaker RP (2013) Maternal oral origin of Fusobacterium nucleatum in adverse pregnancy outcomes as determined using the 16S-23S rRNA gene intergenic transcribed spacer region. J Med Microbiol 62(Pt 1):133–144PubMed Gonzales-Marin C, Spratt DA, Allaker RP (2013) Maternal oral origin of Fusobacterium nucleatum in adverse pregnancy outcomes as determined using the 16S-23S rRNA gene intergenic transcribed spacer region. J Med Microbiol 62(Pt 1):133–144PubMed
43.
go back to reference Wang X, Buhimschi CS, Temoin S, Bhandari V, Han YW, Buhimschi IA Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLoS One 8(2):e56131 Wang X, Buhimschi CS, Temoin S, Bhandari V, Han YW, Buhimschi IA Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLoS One 8(2):e56131
44.
go back to reference Blanc V, O'Valle F, Pozo E, Puertas A, Leon R, Mesa F (2015) Oral bacteria in placental tissues: increased molecular detection in pregnant periodontitis patients. Oral Dis 21(7):905–912PubMed Blanc V, O'Valle F, Pozo E, Puertas A, Leon R, Mesa F (2015) Oral bacteria in placental tissues: increased molecular detection in pregnant periodontitis patients. Oral Dis 21(7):905–912PubMed
45.
go back to reference Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS (2004) Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun 72(4):2272–2279PubMedPubMedCentral Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS (2004) Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun 72(4):2272–2279PubMedPubMedCentral
46.
go back to reference Laopaiboon M, Lumbiganon P, Intarut N, Mori R, Ganchimeg T, Vogel JP, Souza JP, Gulmezoglu AM (2014) Network WHOMSoMNHR: advanced maternal age and pregnancy outcomes: a multicountry assessment. BJOG 121(Suppl 1):49–56PubMed Laopaiboon M, Lumbiganon P, Intarut N, Mori R, Ganchimeg T, Vogel JP, Souza JP, Gulmezoglu AM (2014) Network WHOMSoMNHR: advanced maternal age and pregnancy outcomes: a multicountry assessment. BJOG 121(Suppl 1):49–56PubMed
Metadata
Title
The periodontopathic bacteria in placenta, saliva and subgingival plaque of threatened preterm labor and preterm low birth weight cases: a longitudinal study in Japanese pregnant women
Authors
Changchang Ye
Sayaka Katagiri
Naoyuki Miyasaka
Hiroaki Kobayashi
Thatawee Khemwong
Toshiyuki Nagasawa
Yuichi Izumi
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 12/2020
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-020-03287-4

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