Review: Maternal health and the placental microbiome

Placenta

Volumn 54, Issue , 2017, Pages 30-37

  Pelzer, Elise ^a   Gomez Arango, Luisa F ^b,c   Barrett, Helen L ^b,c,d   Nitert, Marloes Dekker ^b,c  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Microbiome; Placenta; Pregnancy; Preterm delivery; Probiotics

Indexed keywords

ANTIBIOTIC AGENT; PROBIOTIC AGENT;

CHORIOAMNIONITIS; HUMAN; MATERNAL OBESITY; MATERNAL WELFARE; MICROBIOME; NONHUMAN; PLACENTA; PREECLAMPSIA; PREGNANCY; PREGNANCY DIABETES MELLITUS; PREGNANCY OUTCOME; PREMATURE LABOR; PRIORITY JOURNAL; REVIEW; FEMALE; MICROBIOLOGY; MICROFLORA; PREGNANCY COMPLICATION;

FEMALE; HUMANS; MATERNAL HEALTH; MICROBIOTA; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 85009223250     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2016.12.003     Document Type: Review

References (97)

1. Gilbert, S.F., Bosch, T.C.G., Ledon-Rettig, C., Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat. Rev. Genet. 16:10 (2015), 611–622.
2. Del Chierico, F., Vernocchi, P., Dallapiccola, B., Putignani, L., Mediterranean diet and health: food effects on gut microbiota and disease control. Int. J. Mol. Sci., 15(7), 2014.
3. Bull, M.J., Plummer, N.T., Part 1: the human gut microbiome in health and disease. Integr. Med. A Clinician's J. 13:6 (2014), 17–22.
4. Parfrey, L.W., Knight, R., Spatial and temporal variability of the human microbiota, Clinical Microbiology and Infection 18. Supplement 4 (2012), 5–7.
5. Estrela, S., Whiteley, M., Brown, S.P., The demographic determinants of human microbiome health. Trends Microbiol. 23:3 (2015), 134–141.
6. Koren, O., Goodrich, J.K., Cullender, T.C., Spor, A., Laitinen, K., Kling Backhed, H., Gonzalez, A., Werner, J.J., Angenent, L.T., Knight, R., Backhed, F., Isolauri, E., Salminen, S., Ley, R.E., Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150:3 (2012), 470–480.
7. Gomez-Arango, L.F., Barrett, H.L., McIntyre, H.D., Callaway, L.K., Morrison, M., Dekker Nitert, M., Group, S.T., Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes 65:8 (2016), 2214–2223.
8. Gomez-Arango, L.F., Barrett, H.L., McIntyre, H.D., Callaway, L.K., Morrison, M., Nitert, M.D., Group, S.T., Increased systolic and diastolic blood pressure is associated with altered gut microbiota composition and butyrate production in early pregnancy. Hypertension 68:4 (2016), 974–981.
9. Franasiak, J.M., Scott, R.T. Jr., Reproductive tract microbiome in assisted reproductive technologies. Fertil. Steril. 104:6 (2015), 1364–1371.
10. Kovalovszki, L., Villanyi, Z., Pataki, I., Veszelowvsky, I., Nagy, Z.B., Isolation of aerobic bacteria from the placenta. Acta Paediatr. Acad. Sci. Hung. 23:3 (1982), 357–360.
11. DiGiulio, D.B., Gervasi, M., Romero, R., Mazaki-Tovi, S., Vaisbuch, E., Kusanovic, J.P., Seok, K.S., Gomez, R., Mittal, P., Gotsch, F., Chaiworapongsa, T., Oyarzun, E., Kim, C.J., Relman, D.A., Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J. Perinat. Med. 38:5 (2010), 503–513.
12. Cao, B., Stout, M.J., Lee, I., Mysorekar, I.U., Placental microbiome and its role in preterm birth. Neoreviews 15:12 (2014), e537–e545.
13. Prince, A.L., Ma, J., Kannan, P.S., Alvarez, M., Gisslen, T., Harris, R.A., Sweeney, E.L., Knox, C.L., Lambers, D.S., Jobe, A.H., Chougnet, C.A., Kallapur, S.G., Aagaard, K.M., The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am. J. Obstet. Gynecol., 214(5), 2016, 627 e1 627 e16.
14. Hillier, S.L., Krohn, M.A., Kiviat, N.B., Watts, D.H., Eschenbach, D.A., Microbiologic causes and neonatal outcomes associated with chorioamnion infection. Am. J. Obstet. Gynecol. 165:4 Pt 1 (1991), 955–961.
15. Onderdonk, A.B., Delaney, M.L., DuBois, A.M., Allred, E.N., Leviton, A., I. Extremely Low Gestational Age Newborns Study, Detection of bacteria in placental tissues obtained from extremely low gestational age neonates. Am. J. Obstet. Gynecol., 198(1), 2008, 110 e1 7.
16. Onderdonk, A.B., Hecht, J.L., McElrath, T.F., Delaney, M.L., Allred, E.N., Leviton, A., Investigators, E.S., Colonization of second-trimester placenta parenchyma. Am. J. Obstet. Gynecol., 199(1), 2008, 52 e1 52 e10.
17. Antony, K.M., Ma, J., Mitchell, K.B., Racusin, D.A., Versalovic, J., Aagaard, K., The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am. J. Obstetrics Gynecol., 212(5), 2015, 653.e1 653.e16.
18. DiGiulio, D.B., Gervasi, M.T., Romero, R., Vaisbuch, E., Mazaki-Tovi, S., Kusanovic, J.P., Seok, K.S., Gomez, R., Mittal, P., Gotsch, F., Chaiworapongsa, T., Oyarzun, E., Kim, C.J., Relman, D.A., Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J. Perinat. Med. 38:5 (2010), 495–502.
19. DiGiulio, D.B., Romero, R., Amogan, H.P., Kusanovic, J.P., Bik, E.M., Gotsch, F., Kim, C.J., Erez, O., Edwin, S., Relman, D.A., Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One, 3(8), 2008, e3056.
20. DiGiulio, D.B., Romero, R., Kusanovic, J.P., Gomez, R., Kim, C.J., Seok, K.S., Gotsch, F., Mazaki-Tovi, S., Vaisbuch, E., Sanders, K., Bik, E.M., Chaiworapongsa, T., Oyarzun, E., Relman, D.A., Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am. J. Reprod. Immunol. 64:1 (2010), 38–57.
21. Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J., Versalovic, J., The placenta harbors a unique microbiome. Sci. Transl. Med., 6(237), 2014 237ra65.
22. Collado, M.C., Rautava, S., Aakko, J., Isolauri, E., Salminen, S., Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep., 6, 2016, 23129.
23. DiGiulio, D.B., Callahan, B.J., McMurdie, P.J., Costello, E.K., Lyell, D.J., Robaczewska, A., Sun, C.L., Goltsman, D.S.A., Wong, R.J., Shaw, G., Stevenson, D.K., Holmes, S.P., Relman, D.A., Temporal and spatial variation of the human microbiota during pregnancy. Proc. Natl. Acad. Sci. U. S. A. 112:35 (2015), 11060–11065.
24. McClure, E.M., Goldenberg, R.L., Infection and stillbirth. Semin. Fetal Neonatal Med. 14:4 (2009), 182–189.
25. Romero, R., Miranda, J., Chaiworapongsa, T., Korzeniewski, S.J., Chaemsaithong, P., Gotsch, F., Dong, Z., Ahmed, A.I., Yoon, B.H., Hassan, S.S., Kim, C.J., Yeo, L., Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am. J. Reprod. Immunol. 72:5 (2014), 458–474.
26. Romero, R., Miranda, J., Kusanovic, J.P., Chaiworapongsa, T., Chaemsaithong, P., Martinez, A., Gotsch, F., Dong, Z., Ahmed, A.I., Shaman, M., Lannaman, K., Yoon, B.H., Hassan, S.S., Kim, C.J., Korzeniewski, S.J., Yeo, L., Kim, Y.M., Clinical chorioamnionitis at term I: microbiology of the amniotic cavity using cultivation and molecular techniques. J. Perinat. Med. 43:1 (2015), 19–36.
27. Zheng, J., Xiao, X., Zhang, Q., Mao, L., Yu, M., Xu, J., The placental microbiome varies in association with low birth weight in full-term neonates. Nutrients 7:8 (2015), 6924–6937.
28. Perez, P.F., Dore, J., Leclerc, M., Levenez, F., Benyacoub, J., Serrant, P., Segura-Roggero, I., Schiffrin, E.J., Donnet-Hughes, A., Bacterial imprinting of the neonatal immune system: lessons from maternal cells?. Pediatrics, 119(3), 2007, e724 32.
29. Jimenez, E., Marin, M.L., Martin, R., Odriozola, J.M., Olivares, M., Xaus, J., Fernandez, L., Rodriguez, J.M., Is meconium from healthy newborns actually sterile?. Res. Microbiol. 159:3 (2008), 187–193.
30. Han, Y.W., Redline, R.W., Li, M., Yin, L., Hill, G.B., McCormick, T.S., Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect. Immun. 72:4 (2004), 2272–2279.
31. Romero, R., Hassan, S.S., Gajer, P., Tarca, A.L., Fadrosh, D.W., Bieda, J., Chaemsaithong, P., Miranda, J., Chaiworapongsa, T., Ravel, J., The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome, 2, 2014, 18.
32. MacIntyre, D.A., Chandiramani, M., Lee, Y.S., Kindinger, L., Smith, A., Angelopoulos, N., Lehne, B., Arulkumaran, S., Brown, R., Teoh, T.G., Holmes, E., Nicoholson, J.K., Marchesi, J.R., Bennett, P.R., The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci. Rep., 5, 2015, 8988.
33. Romero, R., Hassan, S.S., Gajer, P., Tarca, A.L., Fadrosh, D.W., Nikita, L., Galuppi, M., Lamont, R.F., Chaemsaithong, P., Miranda, J., Chaiworapongsa, T., Ravel, J., The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome, 2(1), 2014, 4.
34. Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T.A., Coarfa, C., Raza, S., Rosenbaum, S., Van den Veyver, I., Milosavljevic, A., Gevers, D., Huttenhower, C., Petrosino, J., Versalovic, J., A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One, 7(6), 2012, e36466.
35. Petricevic, L., Domig, K.J., Nierscher, F.J., Sandhofer, M.J., Fidesser, M., Krondorfer, I., Husslein, P., Kneifel, W., Kiss, H., Characterisation of the vaginal Lactobacillus microbiota associated with preterm delivery. Sci. Rep., 4, 2014, 5136.
36. Petricevic, L., Domig, K.J., Nierscher, F.J., Krondorfer, I., Janitschek, C., Kneifel, W., Kiss, H., Characterisation of the oral, vaginal and rectal Lactobacillus flora in healthy pregnant and postmenopausal women. Eur. J. Obstet. Gynecol. Reprod. Biol. 160:1 (2012), 93–99.
37. Andrews, W.W., Goldenberg, R.L., Hauth, J.C., Cliver, S.P., Conner, M., Goepfert, A.R., Endometrial microbial colonization and plasma cell endometritis after spontaneous or indicated preterm versus term delivery. Am. J. Obstet. Gynecol. 193:3 Pt 1 (2005), 739–745.
38. Andrews, W.W., Klebanoff, M.A., Thom, E.A., Hauth, J.C., Carey, J.C., Meis, P.J., Caritis, S.N., Leveno, K.J., Wapner, R.J., Varner, M.W., Iams, J.D., Moawad, A., Miodovnik, M., Sibai, B., Dombrowski, M., Langer, O., O'Sullivan, M.J., H. National Institute of Child, N. Human Development Maternal-Fetal Medicine Units, Midpregnancy genitourinary tract infection with Chlamydia trachomatis: association with subsequent preterm delivery in women with bacterial vaginosis and Trichomonas vaginalis. Am. J. Obstet. Gynecol. 194:2 (2006), 493–500.
39. Mitchell, C.M., Haick, A., Nkwopara, E., Garcia, R., Rendi, M., Agnew, K., Fredricks, D.N., Eschenbach, D., Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women. Am. J. Obstet. Gynecol., 212(5), 2015, 611 e1 9.
40. Fang, R.L., Chen, L.X., Shu, W.S., Yao, S.Z., Wang, S.W., Chen, Y.Q., Barcoded sequencing reveals diverse intrauterine microbiomes in patients suffering with endometrial polyps. Am. J. Transl. Res. 8:3 (2016), 1581–1592.
41. Korn, A.P., Bolan, G., Padian, N., Ohm-Smith, M., Schachter, J., Landers, D.V., Plasma cell endometritis in women with symptomatic bacterial vaginosis. Obstet. Gynecol. 85:3 (1995), 387–390.
42. Prince, A.L., Antony, K.M., Ma, J., Aagaard, K.M., The microbiome and development: a mother's perspective. Semin. Reprod. Med. 32:1 (2014), 14–22.
43. Prince, A.L., Antony, K.M., Chu, D.M., Aagaard, K.M., The microbiome, parturition, and timing of birth: more questions than answers. J. Reprod. Immunol. 104–105 (2014), 12–19.
44. Goldenberg, R.L., Iams, J.D., Das, A., Mercer, B.M., Meis, P.J., Moawad, A.H., Miodovnik, M., VanDorsten, J.P., Caritis, S.N., Thurnau, G.R., Dombrowski, M.P., Roberts, J.M., McNellis, D., The preterm prediction study: sequential cervical length and fetal fibronectin testing for the prediction of spontaneous preterm birth. National institute of child health and human development maternal-fetal medicine units network. Am. J. Obstet. Gynecol. 182:3 (2000), 636–643.
45. Martin, R., Makino, H., Cetinyurek Yavuz, A., Ben-Amor, K., Roelofs, M., Ishikawa, E., Kubota, H., Swinkels, S., Sakai, T., Oishi, K., Kushiro, A., Knol, J., Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut microbiota. PLoS One, 11(6), 2016, e0158498.
46. Jimenez, E., Fernandez, L., Marin, M.L., Martin, R., Odriozola, J.M., Nueno-Palop, C., Narbad, A., Olivares, M., Xaus, J., Rodriguez, J.M., Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 51:4 (2005), 270–274.
47. Steel, J.H., Malatos, S., Kennea, N., Edwards, A.D., Miles, L., Duggan, P., Reynolds, P.R., Feldman, R.G., Sullivan, M.H., Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor. Pediatr. Res. 57:3 (2005), 404–411.
48. Gomez de Aguero, M., Ganal-Vonarburg, S.C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., McCoy, K.D., Macpherson, A.J., The maternal microbiota drives early postnatal innate immune development. Science 351:6279 (2016), 1296–1302.
49. Lawn, J.E., Cousens, S., Zupan, J., T. Lancet neonatal survival steering, 4 million neonatal deaths: when? Where? why?. Lancet 365:9462 (2005), 891–900.
50. Solt, I., The human microbiome and the great obstetrical syndromes: a new frontier in maternal-fetal medicine. Best. Pract. Res. Clin. Obstet. Gynaecol. 29:2 (2015), 165–175.
51. Fortner, K.B., Grotegut, C.A., Ransom, C.E., Bentley, R.C., Feng, L., Lan, L., Heine, R.P., Seed, P.C., Murtha, A.P., Bacteria localization and chorion thinning among preterm premature rupture of membranes. PLoS One, 9(1), 2014, e83338.
52. Watts, D.H., Krohn, M.A., Hillier, S.L., Eschenbach, D.A., The association of occult amniotic fluid infection with gestational age and neonatal outcome among women in preterm labor. Obstet. Gynecol. 79:3 (1992), 351–357.
53. Brocklehurst, P., Hannah, M., McDonald, H., Interventions for treating bacterial vaginosis in pregnancy. Cochrane Database Syst. Rev.(2), 2000, CD000262.
54. Myntti, T., Rahkonen, L., Tikkanen, M., Paavonen, J., Stefanovic, V., Vaginally obtained amniotic fluid samples in the diagnosis of subclinical chorioamnionitis. Acta Obstet. Gynecol. Scand. 95:2 (2016), 233–237.
55. Mysorekar, I.U., Cao, B., Microbiome in parturition and preterm birth. Semin. Reprod. Med. 32:1 (2014), 50–55.
56. Jefferson, K.K., The bacterial etiology of preterm birth. Adv. Appl. Microbiol. 80 (2012), 1–22.
57. Amarasekara, R., Jayasekara, R.W., Senanayake, H., Dissanayake, V.H., Microbiome of the placenta in pre-eclampsia supports the role of bacteria in the multifactorial cause of pre-eclampsia. J. Obstet. Gynaecol. Res. 41:5 (2015), 662–669.
58. Hecht, J.L., Onderdonk, A., Delaney, M., Allred, E.N., Kliman, H.J., Zambrano, E., Pflueger, S.M., Livasy, C.A., Bhan, I., Leviton, A., Investigators, E.S., Characterization of chorioamnionitis in 2nd-trimester C-section placentas and correlation with microorganism recovery from subamniotic tissues. Pediatr. Dev. Pathol. 11:1 (2008), 15–22.
59. Musilova, I., Andrys, C., Drahosova, M., Soucek, O., Stepan, M., Bestvina, T., Spacek, R., Jacobsson, B., Cobo, T., Kacerovsky, M., Intraamniotic inflammation and umbilical cord blood interleukin-6 concentrations in pregnancies complicated by preterm prelabor rupture of membranes. J. Matern. Fetal Neonatal Med., 2016, 1–11.
60. Kjaergaard, N., Helmig, R.B., Schonheyder, H.C., Uldbjerg, N., Hansen, E.S., Madsen, H., Chorioamniotic membranes constitute a competent barrier to group b streptococcus in vitro. Eur. J. Obstet. Gynecol. Reprod. Biol. 83:2 (1999), 165–169.
61. 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. 47:3 (2016), 193–204.
62. Han, Y.W., Fardini, Y., Chen, C., Iacampo, K.G., Peraino, V.A., Shamonki, J.M., Redline, R.W., Term stillbirth caused by oral Fusobacterium nucleatum. Obstet. Gynecol. 115:2 Pt 2 (2010), 442–445.
63. Shiozaki, A., Yoneda, S., Yoneda, N., Yonezawa, R., Matsubayashi, T., Seo, G., Saito, S., Intestinal microbiota is different in women with preterm birth: results from terminal restriction fragment length polymorphism analysis. PLoS One, 9(11), 2014, e111374.
64. Lopetuso, L.R., Scaldaferri, F., Franceschi, F., Gasbarrini, A., The gastrointestinal microbiome - functional interference between stomach and intestine, Best practice & research. Clin. Gastroenterol. 28:6 (2014), 995–1002.
65. Antonio, M.A., Rabe, L.K., Hillier, S.L., Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J. Infect. Dis. 192:3 (2005), 394–398.
66. Boskey, E.R., Cone, R.A., Whaley, K.J., Moench, T.R., Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Hum. Reprod. 16:9 (2001), 1809–1813.
67. Han, Y.W., Shen, T., Chung, P., Buhimschi, I.A., Buhimschi, C.S., Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J. Clin. Microbiol. 47:1 (2009), 38–47.
68. Bearfield, C., Davenport, E.S., Sivapathasundaram, V., Allaker, R.P., Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG 109:5 (2002), 527–533.
69. Agrawal, V., Hirsch, E., Intrauterine infection and preterm labor. Semin. Fetal Neonatal Med. 17:1 (2012), 12–19.
70. Nuriel-Ohayon, M., Neuman, H., Koren, O., Microbial changes during pregnancy, birth, and infancy. Front. Microbiol., 7, 2016, 1031.
71. Fichorova, R.N., Onderdonk, A.B., Yamamoto, H., Delaney, M.L., DuBois, A.M., Allred, E., Leviton, A., I. Extremely Low Gestation Age Newborns Study, Maternal microbe-specific modulation of inflammatory response in extremely low-gestational-age newborns. mBio, 2(1), 2011, e00280 10.
72. Romero, R., Espinoza, J., Goncalves, L.F., Kusanovic, J.P., Friel, L., Hassan, S., The role of inflammation and infection in preterm birth. Semin. Reprod. Med. 25:1 (2007), 21–39.
73. Goldenberg, R.L., Hauth, J.C., Andrews, W.W., Intrauterine infection and preterm delivery. N. Engl. J. Med. 342:20 (2000), 1500–1507.
74. Payne, M.S., Bayatibojakhi, S., Exploring preterm birth as a polymicrobial disease: an overview of the uterine microbiome. Front. Immunol., 5, 2014, 595.
75. Vermeulen, G.M., van Zwet, A.A., Bruinse, H.W., Changes in the vaginal flora after two percent clindamycin vaginal cream in women at high risk of spontaneous preterm birth. BJOG 108:7 (2001), 697–700.
76. Challier, J.C., Basu, S., Bintein, T., Minium, J., Hotmire, K., Catalano, P.M., Hauguel-de Mouzon, S., Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 29:3 (2008), 274–281.
77. Kristensen, J., Vestergaard, M., Wisborg, K., Kesmodel, U., Secher, N.J., Pre-pregnancy weight and the risk of stillbirth and neonatal death. BJOG Int. J. obstetrics Gynaecol. 112:4 (2005), 403–408.
78. Do Carmo, S., Forest, J.C., Giguere, Y., Masse, A., Lafond, J., Rassart, E., Modulation of Apolipoprotein D levels in human pregnancy and association with gestational weight gain. Reproductive Biol. Endocrinol. RB&E, 7, 2009, 92.
79. Gohir, W., Ratcliffe, E.M., Sloboda, D.M., Of the bugs that shape us: maternal obesity, the gut microbiome, and long-term disease risk. Pediatr. Res. 77:1–2 (2015), 196–204.
80. Kuperman, A.A., Koren, O., Antibiotic use during pregnancy: how bad is it?. BMC Med., 14(1), 2016, 91.
81. Peng, S.M., Wong, H.M., King, N.M., McGrath, C., Is dental caries experience associated with adiposity status in preschool children?. Int. J. Paediatr. Dent./Br. Paedodontic Soc. Int. Assoc. Dent. Child. 24:2 (2014), 122–130.
82. Shillitoe, E., Weinstock, R., Kim, T., Simon, H., Planer, J., Noonan, S., Cooney, R., The oral microflora in obesity and type-2 diabetes. J. oral Microbiol., 4, 2012.
83. Oh, H.Y., Seo, S.S., Kong, J.S., Lee, J.K., Kim, M.K., Association between obesity and cervical microflora dominated by Lactobacillus iners in korean women. J. Clin. Microbiol. 53:10 (2015), 3304–3309.
84. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., Egholm, M., Henrissat, B., Heath, A.C., Knight, R., Gordon, J.I., A core gut microbiome in obese and lean twins. Nature 457:7228 (2009), 480–484.
85. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R., Gordon, J.I., An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:7122 (2006), 1027–1031.
86. Blaut, M., Gut microbiota and energy balance: role in obesity. Proc. Nutr. Soc., 2014, 1–8.
87. Cani, P.D., Gut microbiota and obesity: lessons from the microbiome. Briefings Funct. genomics 12:4 (2013), 381–387.
88. Weinert, L.S., International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy: comment to the international association of diabetes and pregnancy study groups consensus panel. Diabetes care, 33(7), 2010 e97; author reply e98.
89. Prince, A.L., Ma, J., Kannan, P.S., Alvarez, M., Gisslen, T., Harris, R.A., Sweeney, E.L., Knox, C.L., Lambers, D.S., Jobe, A.H., Chougnet, C.A., Kallapur, S.G., Aagaard, K.M., The placental microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am. J. Obstet. Gynecol. 215:5 (2016), 627.e1–627.e16.
90. Bassols, J., Serino, M., Carreras-Badosa, G., Burcelin, R., Blasco-Baque, V., Lopez-Bermejo, A., Fernandez-Real, J.M., Gestational diabetes is associated with changes in placental microbiota and microbiome. Pediatr. Res. 80:6 (2016), 777–784.
91. Mshvildadze, M., Neu, J., Shuster, J., Theriaque, D., Li, N., Mai, V., Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J. Pediatr. 156:1 (2010), 20–25.
92. Langdon, A., Crook, N., Dantas, G., The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med., 8(1), 2016, 39.
93. Rautava, S., Collado, M.C., Salminen, S., Isolauri, E., Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102:3 (2012), 178–184.
94. Satokari, R., Gronroos, T., Laitinen, K., Salminen, S., Isolauri, E., Bifidobacterium and Lactobacillus DNA in the human placenta. Lett. Appl. Microbiol. 48:1 (2009), 8–12.
95. Voreades, N., Kozil, A., Weir, T.L., Diet and the development of the human intestinal microbiome. Front. Microbiol., 5, 2014, 494.
96. Martinez de Tejada, B., Antibiotic use and misuse during pregnancy and delivery: benefits and risks. Int. J. Environ. Res. public health 11:8 (2014), 7993–8009.
97. Bartosch, S., Fite, A., Macfarlane, G.T., McMurdo, M.E., Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl. Environ. Microbiol. 70:6 (2004), 3575–3581.