Microbial changes during pregnancy, birth, and infancy

Frontiers in Microbiology

Volumn 7, Issue JUL, 2016, Pages

  Nuriel Ohayon, Meital ^a   Neuman, Hadar ^a   Koren, Omry ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Gut; Infant; Microbiome; Microbiota; Newborn; Pregnancy

Indexed keywords

AMOXICILLIN; AZITHROMYCIN; CEFACLOR; TOLL LIKE RECEPTOR;

BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL LOAD; BODY MASS; BREAST FEEDING; DYSBIOSIS; FAECALIBACTERIUM; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MECONIUM; METABOLIC SYNDROME X; MICROFLORA; MOUTH FLORA; NONHUMAN; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL DEVELOPMENT; REVIEW; VAGINA FLORA; WEIGHT GAIN;

EID: 84983056926     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01031     Document Type: Review

References (102)

1. Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., and Versalovic, J. (2014). The placenta harbors a unique microbiome. Sci. Transl. Med. 6: 237ra65. doi: 10.1126/scitranslmed.3008599
2. Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T. A., Coarfa, C., et al. (2012). A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS ONE 7: e36466. doi: 10.1371/journal.pone.0036466
3. Abrahamsson, T. R., Wu, R. Y., and Jenmalm, M. C. (2015). Gut microbiota and allergy: the importance of the pregnancy period. Pediatr. Res. 77, 214-219. doi: 10.1038/pr.2014.165
4. Ardissone, A. N., de la Cruz, D. M., Davis-Richardson, A. G., Rechcigl, K. T., Li, N., Drew, J. C., et al. (2014). Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS ONE 9: e90784. doi: 10.1371/journal.pone.0090784
5. Backhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., et al. (2015). Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690-703. doi: 10.1016/j.chom.2015.05.012
6. Balmer, S. E., and Wharton, B. A. (1989). Diet and faecal flora in the newborn: breast milk and infant formula. Arch. Dis. Child. 64, 1672-1677. doi: 10.1136/adc.64.12.1672
7. Bezirtzoglou, E., Tsiotsias, A., and Welling, G. W. (2011). Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17, 478-482. doi: 10.1016/j.anaerobe.2011.03.009
8. Bode, L. (2012). Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22, 1147-1162. doi: 10.1093/glycob/cws074
9. Borgo, P. V., Rodrigues, V. A., Feitosa, A. C., Xavier, K. C., and Avila-Campos, M. J. (2014). Association between periodontal condition and subgingival microbiota in women during pregnancy: a longitudinal study. J. Appl. Oral Sci. 22, 528-533. doi: 10.1590/1678-775720140164
10. Cabrera-Rubio, R., Collado, M. C., Laitinen, K., Salminen, S., Isolauri, E., and Mira, A. (2012). The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 96, 544-551. doi: 10.3945/ajcn.112.037382
11. Centers for Disease Prevention (2006). Community-associated methicillin-resistant Staphylococcus aureus infection among healthy newborns-Chicago and Los Angeles County, 2004. MMWR Morb. Mortal Wkly. Rep. 55, 329-332. doi: 10.1097/01.inf.0000226977.41367.58
12. Collado, M. C., Isolauri, E., Laitinen, K., and Salminen, S. (2008). Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am. J. Clin. Nutr. 88, 894-899.
13. Decker, E., Engelmann, G., Findeisen, A., Gerner, P., Laass, M., Ney, D., et al. (2010). Cesarean delivery is associated with celiac disease but not inflammatory bowel disease in children. Pediatrics 125, e1433-e1440. doi: 10.1542/peds.2009-2260
14. Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C., Yu, W. H., et al. (2010). The human oral microbiome. J. Bacteriol. 192, 5002-5017. doi: 10.1128/jb.00542-10
15. DiGiulio, D. B., Callahan, B. J., McMurdie, P. J., Costello, E. K., Lyell, D. J., Robaczewska, A., et al. (2015). Temporal and spatial variation of the human microbiota during pregnancy. Proc. Natl. Acad. Sci. U.S.A. 112, 11060-11065. doi: 10.1073/pnas.1502875112
16. DiGiulio, D. B., Gervasi, M., Romero, R., Mazaki-Tovi, S., Vaisbuch, E., Kusanovic, J. P., et al. (2010a). Microbial invasion of the amniotic cavity in preeclampsia as assessed by cultivation and sequence-based methods. J. Perinat. Med. 38, 503-513. doi: 10.1515/jpm.2010.078
17. DiGiulio, D. B., Romero, R., Kusanovic, J. P., Gomez, R., Kim, C. J., Seok, K. S., et al. (2010b). 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, 38-57. doi: 10.1111/j.1600-0897.2010.00830.x
18. Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., et al. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U.S.A. 107, 11971-11975. doi: 10.1073/pnas.1002601107
19. Dominguez-Bello, M. G., De Jesus-Laboy, K. M., Shen, N., Cox, L. M., Amir, A., Gonzalez, A., et al. (2016). Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat. Med. 22, 250-253. doi: 10.1038/nm.4039
20. Dunlop, A. L., Mulle, J. G., Ferranti, E. P., Edwards, S., Dunn, A. B., and Corwin, E. J. (2015). Maternal microbiome and pregnancy outcomes that impact infant health: a review. Adv. Neonatal Care 15, 377-385. doi: 10.1097/ANC.0000000000000218
21. ElAttar, T. M. (1976). Prostaglandin E2 in human gingiva in health and disease and its stimulation by female sex steroids. Prostaglandins 11, 331-341. doi: 10.1016/0090-6980(76)90155-6
22. Emanuela, F., Grazia, M., Marco de, R., Maria Paola, L., Giorgio, F., and Marco, B. (2012). Inflammation as a link between obesity and metabolic syndrome. J. Nutr. Metab. 2012: 476380. doi: 10.1155/2012/476380
23. Farr, A., Kiss, H., Holzer, I., Husslein, P., Hagmann, M., and Petricevic, L. (2015). Effect of asymptomatic vaginal colonization with Candida albicans on pregnancy outcome. Acta Obstet. Gynecol. Scand. 94, 989-996. doi: 10.1111/aogs.12697
24. Fuglsang, J. (2008). Ghrelin in pregnancy and lactation. Vitam. Horm. 77, 259-284. doi: 10.1016/S0083-6729(06)77011-X
25. Fujiwara, N., Tsuruda, K., Iwamoto, Y., Kato, F., Odaki, T., Yamane, N., et al. (2015). Significant increase of oral bacteria in the early pregnancy period in Japanese women. J. Investig. Clin. Dent. doi: 10.1111/jicd.12189. [Epub ahead of print].
26. Gibbs, R. S., Romero, R., Hillier, S. L., Eschenbach, D. A., and Sweet, R. L. (1992). A review of premature birth and subclinical infection. Am. J. Obstet. Gynecol. 166, 1515-1528. doi: 10.1016/0002-9378(92)91628-n
27. Gohir, W., Whelan, F. J., Surette, M. G., Moore, C., Schertzer, J. D., and Sloboda, D. M. (2015). Pregnancy-related changes in the maternal gut microbiota are dependent upon the mother's periconceptional diet. Gut Microbes 6, 310-320. doi: 10.1080/19490976.2015.1086056
28. Goldenberg, R. L., Hauth, J. C., and Andrews, W. W. (2000). Intrauterine infection and preterm delivery. N. Engl. J. Med. 342, 1500-1507. doi: 10.1056/NEJM200005183422007
29. Gomez-Arango, L. F., Barrett, H. L., McIntyre, H. D., Callaway, L. K., Morrison, M., Nitert, M. D., and group, S. T. (2016). Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes. doi: 10.2337/db16-0278. [Epub ahead of print].
30. Gonzalez-Perez, G., Hicks, A. L., Tekieli, T. M., Radens, C. M., Williams, B. L., and Lamouse-Smith, E. S. (2016). Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J. Immunol. 196, 3768-3779. doi: 10.4049/jimmunol.1502322
31. Gosalbes, M. J., Llop, S., Valles, Y., Moya, A., Ballester, F., and Francino, M. P. (2013). Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy 43, 198-211. doi: 10.1111/cea.12063
32. Hansen, R., Scott, K. P., Khan, S., Martin, J. C., Berry, S. H., Stevenson, M., et al. (2015). First-pass meconium samples from healthy term vaginally-delivered neonates: an analysis of the microbiota. PLoS ONE 10: e0133320. doi: 10.1371/journal.pone.0133320
33. Harley, I. T., and Karp, C. L. (2012). Obesity and the gut microbiome: striving for causality. Mol. Metab. 1, 21-31. doi: 10.1016/j.molmet.2012.07.002
34. Haro, C., Garcia-Carpintero, S., Alcala-Diaz, J. F., Gomez-Delgado, F., Delgado-Lista, J., Perez-Martinez, P., et al. (2015). The gut microbial community in metabolic syndrome patients is modified by diet. J. Nutr. Biochem. doi: 10.1016/j.jnutbio.2015.08.011
35. Heikkila, M. P., and Saris, P. E. (2003). Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J. Appl. Microbiol. 95, 471-478. doi: 10.1046/j.1365-2672.2003.02002.x
36. Holgerson, P. L., Vestman, N. R., Claesson, R., Ohman, C., Domellof, M., Tanner, A. C., et al. (2013). Oral microbial profile discriminates breast-fed from formula-fed infants. J. Pediatr. Gastroenterol. Nutr. 56, 127-136. doi: 10.1097/MPG.0b013e31826f2bc6
37. Hu, J., Nomura, Y., Bashir, A., Fernandez-Hernandez, H., Itzkowitz, S., Pei, Z., et al. (2013). Diversified microbiota of meconium is affected by maternal diabetes status. PLoS ONE 8: e78257. doi: 10.1371/journal.pone.0078257
38. Hunt, K. M., Foster, J. A., Forney, L. J., Schutte, U. M., Beck, D. L., Abdo, Z., et al. (2011). Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 6: e21313. doi: 10.1371/journal.pone.0021313
39. Hyman, R. W., Fukushima, M., Jiang, H., Fung, E., Rand, L., Johnson, B., et al. (2014). Diversity of the vaginal microbiome correlates with preterm birth. Reprod. Sci. 21, 32-40. doi: 10.1177/1933719113488838
40. Jakobsson, H. E., Abrahamsson, T. R., Jenmalm, M. C., Harris, K., Quince, C., Jernberg, C., et al. (2014). Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63, 559-566. doi: 10.1136/gutjnl-2012-303249
41. Jefferson, K. K. (2012). The bacterial etiology of preterm birth. Adv. Appl. Microbiol. 80, 1-22. doi: 10.1016/B978-0-12-394381-1.00001-5
42. Jeurink, P. V., van Bergenhenegouwen, J., Jimenez, E., Knippels, L. M., Fernandez, L., Garssen, J., et al. (2013). Human milk: a source of more life than we imagine. Benef. Microbes 4, 17-30. doi: 10.3920/BM2012.0040
43. Jimenez, E., Marin, M. L., Martin, R., Odriozola, J. M., Olivares, M., Xaus, J., et al. (2008). Is meconium from healthy newborns actually sterile?. Res. Microbiol. 159, 187-193. doi: 10.1016/j.resmic.2007.12.007
44. Kalliomaki, M., Collado, M. C., Salminen, S., and Isolauri, E. (2008). Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 87, 534-538.
45. Kelly, D., Campbell, J. I., King, T. P., Grant, G., Jansson, E. A., Coutts, A. G., et al. (2004). Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat. Immunol. 5, 104-112. doi: 10.1038/ni1018
46. Kero, J., Gissler, M., Gronlund, M. M., Kero, P., Koskinen, P., Hemminki, E., et al. (2002). Mode of delivery and asthma - is there a connection?. Pediatr. Res. 52, 6-11. doi: 10.1203/00006450-200207000-00004
47. Khan, I., Azhar, E. I., Abbas, A. T., Kumosani, T., Barbour, E. K., Raoult, D., et al. (2016). Metagenomic analysis of antibiotic-induced changes in gut microbiota in a pregnant rat model. Front. Pharmacol. 7: 104. doi: 10.3389/fphar.2016.00104
48. Kim, J., and Amar, S. (2006). Periodontal disease and systemic conditions: a bidirectional relationship. Odontology 94, 10-21. doi: 10.1007/s10266-006-0060-6
49. Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., et al. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl. 1), 4578-4585. doi: 10.1073/pnas.1000081107
50. Koleva, P. T., Kim, J. S., Scott, J. A., and Kozyrskyj, A. L. (2015). Microbial programming of health and disease starts during fetal life. Birth Defects Res. C Embryo Today 105, 265-277. doi: 10.1002/bdrc.21117
51. Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Backhed, H. K., et al. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150, 470-480. doi: 10.1016/j.cell.2012.07.008
52. Kovalovszki, L., Villanyi, Z., Pataki, I., Veszelowvsky, I., and Nagy, Z. B. (1982). Isolation of aerobic bacteria from the placenta. Acta Paediatr. Acad. Sci. Hung. 23, 357-360.
53. Kuitunen, M., Kukkonen, K., Juntunen-Backman, K., Korpela, R., Poussa, T., Tuure, T., et al. (2009). Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J. Allergy Clin. Immunol. 123, 335-341. doi: 10.1016/j.jaci.2008.11.019
54. Kujovich, J. L. (2004). Thrombophilia and pregnancy complications. Am. J. Obstet. Gynecol. 191, 412-424. doi: 10.1016/j.ajog.2004.03.001
55. Kumar, P. S. (2013). Sex and the subgingival microbiome: do female sex steroids affect periodontal bacteria?. Periodontol. 2000 61, 103-124. doi: 10.1111/j.1600-0757.2011.00398.x
56. Kumar, P., and Magon, N. (2012). Hormones in pregnancy. Niger. Med. J. 53, 179-183. doi: 10.4103/0300-1652.107549
57. Kunz, C., Rudloff, S., Baier, W., Klein, N., and Strobel, S. (2000). Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu. Rev. Nutr. 20, 699-722. doi: 10.1146/annurev.nutr.20.1.699
58. Lajos, G. J., Passini Junior, R., Nomura, M. L., Amaral, E., Pereira, B. G., Milanez, H., et al. (2008). [Cervical bacterial colonization in women with preterm labor or premature rupture of membranes]. Rev. Bras. Ginecol. Obstet. 30, 393-399. doi: 10.1590/S0100-72032008000800004
59. Li, Y., Caufield, P. W., Dasanayake, A. P., Wiener, H. W., and Vermund, S. H. (2005). Mode of delivery and other maternal factors influence the acquisition of Streptococcus mutans in infants. J. Dent. Res. 84, 806-811. doi: 10.1177/154405910508400905
60. Lif Holgerson, P., Harnevik, L., Hernell, O., Tanner, A. C., and Johansson, I. (2011). Mode of birth delivery affects oral microbiota in infants. J. Dent. Res. 90, 1183-1188. doi: 10.1177/0022034511418973
61. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., and Knight, R. (2012). Diversity, stability and resilience of the human gut microbiota. Nature 489, 220-230. doi: 10.1038/nature11550
62. MacIntyre, D. A., Chandiramani, M., Lee, Y. S., Kindinger, L., Smith, A., Angelopoulos, N., et al. (2015). The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci. Rep. 5: 8988. doi: 10.1038/srep08988
63. Mackie, R. I., Sghir, A., and Gaskins, H. R. (1999). Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69, 1035S-1045S.
64. Manthey, C. F., Autran, C. A., Eckmann, L., and Bode, L. (2014). Human milk oligosaccharides protect against enteropathogenic Escherichia coli attachment in vitro and EPEC colonization in suckling mice. J. Pediatr. Gastroenterol. Nutr. 58, 165-168. doi: 10.1097/MPG.0000000000000172
65. Marild, K., Stephansson, O., Montgomery, S., Murray, J. A., and Ludvigsson, J. F. (2012). Pregnancy outcome and risk of celiac disease in offspring: a nationwide case-control study. Gastroenterology 142, 39.e3-45.e3. doi: 10.1053/j.gastro.2011.09.047
66. Martin, H. L., Richardson, B. A., Nyange, P. M., Lavreys, L., Hillier, S. L., Chohan, B., et al. (1999). Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J. Infect. Dis. 180, 1863-1868. doi: 10.1086/315127
67. Martin, R., Heilig, H. G., Zoetendal, E. G., Jimenez, E., Fernandez, L., Smidt, H., et al. (2007). Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res. Microbiol. 158, 31-37. doi: 10.1016/j.resmic.2006.11.004
68. Martin, R., Jimenez, E., Heilig, H., Fernandez, L., Marin, M. L., Zoetendal, E. G., et al. (2009). Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl. Environ. Microbiol. 75, 965-969. doi: 10.1128/AEM.02063-08
69. McLean, N. W., and Rosenstein, I. J. (2000). Characterisation and selection of a Lactobacillus species to re-colonise the vagina of women with recurrent bacterial vaginosis. J. Med. Microbiol. 49, 543-552. doi: 10.1099/0022-1317-49-6-543
70. Mor, G., and Cardenas, I. (2010). The immune system in pregnancy: a unique complexity. Am. J. Reprod. Immunol. 63, 425-433. doi: 10.1111/j.1600-0897.2010.00836.x
71. Mueller, N. T., Shin, H., Pizoni, A., Werlang, I. C., Matte, U., Goldani, M. Z., et al. (2016). Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci. Rep. 6: 23133. doi: 10.1038/srep23133
72. Mysorekar, I. U., and Cao, B. (2014). Microbiome in parturition and preterm birth. Semin. Reprod. Med. 32, 50-55. doi: 10.1055/s-0033-1361830
73. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., et al. (2012). Compartmentalized control of skin immunity by resident commensals. Science 337, 1115-1119. doi: 10.1126/science.1225152
74. Neuman, H., Debelius, J. W., Knight, R., and Koren, O. (2015). Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol. Rev. 39, 509-521. doi: 10.1093/femsre/fuu010
75. Newbern, D., and Freemark, M. (2011). Placental hormones and the control of maternal metabolism and fetal growth. Curr. Opin. Endocrinol. Diabetes Obes. 18, 409-416. doi: 10.1097/MED.0b013e32834c800d
76. Offenbacher, S., Boggess, K. A., Murtha, A. P., Jared, H. L., Lieff, S., McKaig, R. G., et al. (2006). Progressive periodontal disease and risk of very preterm delivery. Obstet. Gynecol. 107, 29-36. doi: 10.1097/01.AOG.0000190212.87012.96
77. Park, J. S., Park, C. W., Lockwood, C. J., and Norwitz, E. R. (2005). Role of cytokines in preterm labor and birth. Minerva Ginecol. 57, 349-366.
78. Paul, H. A., Bomhof, M. R., Vogel, H. J., and Reimer, R. A. (2016). Diet-induced changes in maternal gut microbiota and metabolomic profiles influence programming of offspring obesity risk in rats. Sci. Rep. 6: 20683. doi: 10.1038/srep20683
79. Prince, A. L., Antony, K. M., Chu, D. M., and Aagaard, K. M. (2014b). The microbiome, parturition, and timing of birth: more questions than answers. J. Reprod. Immunol. 104-105, 12-19. doi: 10.1016/j.jri.2014.03.006
80. Prince, A. L., Antony, K. M., Ma, J., and Aagaard, K. M. (2014a). The microbiome and development: a mother's perspective. Semin. Reprod. Med. 32, 14-22. doi: 10.1055/s-0033-1361818
81. Rajilic-Stojanovic, M., Heilig, H. G., Molenaar, D., Kajander, K., Surakka, A., Smidt, H., et al. (2009). Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environ. Microbiol. 11, 1736-1751. doi: 10.1111/j.1462-2920.2009.01900.x
82. Rautava, S., Collado, M. C., Salminen, S., and Isolauri, E. (2012a). Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102, 178-184. doi: 10.1159/000339182
83. Rautava, S., Kainonen, E., Salminen, S., and Isolauri, E. (2012b). Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J. Allergy Clin. Immunol. 130, 1355-1360. doi: 10.1016/j.jaci.2012.09.003
84. Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S., McCulle, S. L., et al. (2011). Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl. 1), 4680-4687. doi: 10.1073/pnas.1002611107
85. Rizzo, G., and Arduini, D. (2009). Intrauterine growth restriction: diagnosis and management. a review. Minerva Ginecol. 61, 411-420.
86. Romero, R., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., et al. (2014a). The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome 2: 4. doi: 10.1186/2049-2618-2-4
87. Romero, R., Miranda, J., Chaiworapongsa, T., Chaemsaithong, P., Gotsch, F., Dong, Z., et al. (2014b). Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J. Matern. Fetal Neonatal Med. 28, 1-17. doi: 10.3109/14767058.2014.954243
88. Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., et al. (2011). An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J. Biol. Chem. 286, 11909-11918. doi: 10.1074/jbc.M110.193359
89. Seong, H. S., Lee, S. E., Kang, J. H., Romero, R., and Yoon, B. H. (2008). The frequency of microbial invasion of the amniotic cavity and histologic chorioamnionitis in women at term with intact membranes in the presence or absence of labor. Am. J. Obstet. Gynecol. 199, 375.e1-375.e5. doi: 10.1016/j.ajog.2008.06.040
90. Smith, M. I., Yatsunenko, T., Manary, M. J., Trehan, I., Mkakosya, R., Cheng, J., et al. (2013). Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339, 548-554. doi: 10.1126/science.1229000
91. Spor, A., Koren, O., and Ley, R. (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279-290. doi: 10.1038/nrmicro2540
92. Spurbeck, R. R., and Arvidson, C. G. (2010). Lactobacillus jensenii surface-associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect. Immun. 78, 3103-3111. doi: 10.1128/iai.01200-09
93. Stout, M. J., Conlon, B., Landeau, M., Lee, I., Bower, C., Zhao, Q., et al. (2013). Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am. J. Obstet. Gynecol. 208, 226.e1-226.e7. doi: 10.1016/j.ajog.2013.01.018
94. Tissier, H. (1900). Recherches Sur La Flore Intestinale Des Nourrissons (État Normal Et Pathologique). Thesis. Paris: G. Carre and C. Naud.
95. Tochitani, S., Ikeno, T., Ito, T., Sakurai, A., Yamauchi, T., and Matsuzaki, H. (2016). Administration of non-absorbable antibiotics to pregnant mice to perturb the maternal gut microbiota is associated with alterations in offspring behavior. PLoS ONE 11: e0138293. doi: 10.1371/journal.pone.0138293
96. Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., and Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031. doi: 10.1038/nature05414
97. Turovskiy, Y., Sutyak Noll, K., and Chikindas, M. L. (2011). The aetiology of bacterial vaginosis. J. Appl. Microbiol. 110, 1105-1128. doi: 10.1111/j.1365-2672.2011.04977.x
98. Ursell, L. K., Clemente, J. C., Rideout, J. R., Gevers, D., Caporaso, J. G., and Knight, R. (2012). The interpersonal and intrapersonal diversity of human-associated microbiota in key body sites. J. Allergy Clin. Immunol. 129, 1204-1208. doi: 10.1016/j.jaci.2012.03.010
99. Valles, Y., Artacho, A., Pascual-Garcia, A., Ferrus, M. L., Gosalbes, M. J., Abellan, J. J., et al. (2014). Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet. 10: e1004406. doi: 10.1371/journal.pgen.1004406
100. Vestman, N. R., Timby, N., Holgerson, P. L., Kressirer, C. A., Claesson, R., Domellof, M., et al. (2013). Characterization and in vitro properties of oral lactobacilli in breastfed infants. BMC Microbiol. 13: 193. doi: 10.1186/1471-2180-13-193
101. Zhang, D., Huang, Y., and Ye, D. (2015). Intestinal dysbiosis: an emerging cause of pregnancy complications?. Med. Hypotheses 84, 223-226. doi: 10.1016/j.mehy.2014.12.029
102. Zi, M. Y., Longo, P. L., Bueno-Silva, B., and Mayer, M. P. (2014). Mechanisms involved in the association between periodontitis and complications in pregnancy. Front. Public Health 2: 290. doi: 10.3389/fpubh.2014.00290