Effects of probiotics on the intrauterine programming of infant microbiota

1. Chow J., Lee S.M., Shen Y., Khosravi A., Mazmanian S.K. Host-bacterial symbiosis in health and disease. Adv. Immunol. 2010; 107: 243-74.
2. Koleva P.T., Kim J.S., Scott J.A., Kozyrskyj A.L. Microbial programming of health and disease starts during fetal life. Birth Defects Res. C Embryo Today. 2015; 105(4): 265-77.
3. Funkhouser L.J., Bordenstein S.R. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 2013; 11(8): e1001631.
4. Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. The placenta harbors a unique microbiome. Sci. Transl. Med. 2014; 6(237): 237ra65.
5. 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. 2016;6: 23129.
6. Larsen B., Hwang J. Mycoplasma, ureaplasma, and adverse pregnancy outcomes: a fresh look. Infect. Dis. Obstet. Gynecol. 2010; 2010: pii: 521921.
7. Capoccia R., Greub G., Baud D. Ureaplasma urealyticum, Mycoplasma hominis and adverse pregnancy outcomes. Curr. Opin. Infect. Dis. 2013; 26(3): 231-40.
8. Nguyen D.P., Gerber S., Hohlfeld P., Sandrine G., Witkin S.S. Mycoplasma hominis in mid-trimester amniotic fluid: relation to pregnancy outcome. J. Perinat. Med. 2004; 32(4): 323-6.
9. Koren O., Goodrich J.K., Cullender T.C., Spor A., Laitinen K., Bäckhed K.H. et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150(3): 470-80.
10. Murdie P.J., Costello E.K., Lyell D.J., Robaczewska A., Sun C.L., Goltsman D.S.A. et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc. Natl. Acad. Sci. USA. 2015; 112(35): 11060-5.
11. Stanislawski M.A., Dabelea D., Wagner B.D., Sontag M.K., Lozupone C.A., Eggesbø M. Pre-pregnancy weight, gestational weight gain, and the gut microbiota of mothers and their infants. Microbiome. 2017; 5(1): 113.
12. Abrahamsson T.R., Wu R.Y., Jenmalm M.C. Gut microbiota and allergy: The importance of the pregnancy period. Pediatr. Res. 2015; 77(1-2): 214-9.
13. Vuillermin P.J., Macia L., Nanan R., Tang M.L., Collier F., Brix S. The maternal microbiome during pregnancy and allergic disease in the offspring. Semin. Immunopathol. 2017; 39(6): 669-75.
14. Rock R., Ben-Amram H., Neuman H., Hanya H., Koren O., Youngster I. The impact of antibiotic use in breastfeeding women on the infant’s gut microbiome – a prospective cohort study. Open Forum Infect. Dis. 2017; 4(Suppl. 1): S232.
15. Ma J., Prince A.L., Bader D., Hu M., Ganu R., Baquero K. et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat. Commun. 2014; 5: 3889.
16. Chu D.M., Antony K.M., Ma J., Prince A.L., Showalter L., Moller M., Aagaard KM. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. 2016; 8: 77.
17. Gomez de Agüero M., Ganal-Vonarburg S.C., Fuhrer T., Rupp S., Uchimura Y., Li H. et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016; 351(6279): 1296-302.
18. Barker D.J.P. The origins of the developmental origins theory. J. Intern. Med. 2007; 261(5): 412-7.
19. Jimønez E., Fernµndez L., Marín M.L., Martín R., Odriozola J.M., Nueno-Palop C. et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 2005; 51(4): 270-4.
20. 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. 2012; 102(3): 178-84.
21. Bearfield C., Davenport E.S., Sivapathasundaram V., Allaker R.P. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG. 2002; 109(5): 527-33.
22. Jones H.E., Harris K.A., Azizia M., Bank L., Carpenter B., Hartley J.C. et al. Differing prevalence and diversity of bacterial species in fetal membranes from very preterm and term labor. PLoS One. 2009; 4(12): e8205. https://doi.org/10.1371/journal.pone.0008205
23. Gosalbes M.J., Llop S., Vallès Y., Moya A., Ballester F., Francino M.P. Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy. 2013; 43(2): 198-211.
24. Gomez-Arango L.F., Barrett H.L., McIntyre H.D., Callaway L.K., Morrison M., Nitert M.D. Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. Sci. Rep. 2017; 7: 2860.
25. DiGiulio D.B. Diversity of microbes in amniotic fluid. Semin. Fetal Neonatal Med. 2012; 17: 2-11.
26. Aagaard K., Riehle K., Ma J., Segata N., Mistretta T.A., Coarfa C. et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012; 7(6): e36466.
27. Romero R., Hassan S.S., Gajer P., Tarca A.L., Fadrosh D.W., Nikita L. et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1): 4.
28. Avershina E., Storro O., Oien T., Johnsen R., Pope P., Rudi K. Major faecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol. Ecol. 2014; 87(1): 280-90.
29. Jost T., Lacroix C., Braegger C., Chassard C. Stability of the maternal gut microbiota during late pregnancy and early lactation. Curr. Microbiol. 2014; 68(4): 419-27.
30. Saini R., Saini S., Saini S.R. Periodontitis: A risk for delivery of premature labor and low-birth-weight infants. J. Nat. Sci. Biol. Med. 2010; 1(1): 40-2.
31. Dasanayake A.P., Li Y., Wiener H., Ruby J.D., Lee M.J. Salivary Actinomyces naeslundii genospecies 2 and Lactobacillus casei levels predict pregnancy outcomes. J. Periodontol. 2005; 76(2): 171-7.
32. Haque M.M., Merchant M., Kumar P.N., Dutta A., Mande S.S. First-trimester vaginal microbiome diversity: A potential indicator of preterm delivery risk. Sci. Rep. 2017; 7: 16145.
33. Cao B., Stout M.J., Lee I., Mysorekar I.U. Placental microbiome and its role in preterm birth. Neoreviews. 2014; 15(12): e537-45.
34. Paropkari A.D., Leblebicioglu B., Christian L.M., Kumar P.S. Smoking, pregnancy and the subgingival microbiome. Sci. Rep. 2016; 6: 30388.
35. Santacruz A., Collado M.C., Garcia-Valdes L., Segura M.T., Martín-Lagos J.A., Anjos T. et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br. J. Nutr. 2010; 104(1): 83-92.
36. Collado M.C., Isolauri E., Laitinen K., Salminen S. Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am. J. Clin. Nutr. 2010; 92(5): 1023-30.
37. Hu J., Nomura Y., Bashir A., Fernandez-Hernandez H., Itzkowitz S., Pei Z. et al. Diversified microbiota of meconium is affected by maternal diabetes status. PLoS One. 2013; 8(11): e78257.
38. Sjogren Y.M., Jenmalm M.C., Bottcher M.F., Bjorksten B., Sverremark-Ekstrom E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin. Exp. Allergy. 2009; 39(4): 518-26.
39. Kalliomaki M., Collado M.C., Salminen S., Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 2008; 87(3): 534-8.
40. Isik G., Demirezen S., Donmez H.G., Beksac M.S. Bacterial vaginosis in association with spontaneous abortion and recurrent pregnancy losses. J. Cytol. 2016; 33(3): 135-40.
41. Hogenkamp A., Knippels L.M., Garssen J., van Esch B.C. Supplementation of mice with specific nondigestible oligosaccharides during pregnancy or lactation leads to diminished sensitization and allergy in the female offspring. J. Nutr. 2015; 145(5): 996-1002.
42. Bueno-Vargas P., Manzano M., Diaz-Castro J., Lopez-Aliaga I., Rueda R., Lopez-Pedrosa J.M. Maternal dietary supplementation with oligofructose-enriched inulin in gestating/lactating rats preserves maternal bone and improves bone microarchitecture in their offspring. PLoS One. 2016; 11(4): e0154120.
43. Taghizadeh M., Asemi Z. Effects of synbiotic food consumption on glycemic status and serum hs-CRP in pregnant women: a randomized controlled clinical trial. Hormones (Athens). 2014; 13(3): 398-406.
44. Brantsaeter A.L., Myhre R., Haugen M., Myking S., Sengpiel V., Magnus P. et al. Intake of probiotic food and risk of preeclampsia in primiparous women: the Norwegian Mother and Child Cohort Study. Am. J. Epidemiol. 2011; 174(7): 807-15.
45. Gomez Arango L.F., Barrett H.L., Callaway L.K., Nitert M.D. Probiotics and pregnancy. Curr. Diabet. Rep. 2015; 15: 567.
46. Ilmonen J., Isolauri E., Poussa T., Laitinen K. Impact of dietary counselling and probiotic intervention on maternal anthropometric measurements during and after pregnancy: a randomized placebo-controlled trial. Clin. Nutr. 2011; 30(2): 156-64.
47. Swartwout B., Luo X.M. Implications of probiotics on the maternal-neonatal interface: gut microbiota, immunomodulation, and autoimmunity. Front. Immunol. 2018; 9: 2840. https://doi.org/10.3389/fimmu.2018.02840.
48. Asemi Z., Jazayeri S., Najafi M., Samimi M., Mofid V., Shidfar F. et al. Effects of daily consumption of probiotic yoghurt on inflammatory factors in pregnant women: a randomized controlled trial. Pak. J. Biol. Sci. 2011; 14(8):476-82.
49. Vitali B., Cruciani F., Baldassarre M.E., Capursi T., Spisni E., Valerii M.C. et al. Dietary supplementation with probiotics during late pregnancy: Outcome on vaginal microbiota and cytokine secretion. BMC Microbiol. 2012; 12: 236. https://doi.org/10.1186/1471-2180-12-236.
50. Russell N.J., Seale A.C., O’Sullivan C., Le Doare K., Heath P.T., Lawn J.E. et al. Risk of early-onset neonatal group B streptococcal disease with maternal colonization worldwide: systematic review and meta-analyses. Clin. Infect. Dis. 2017;65(Suppl. 2): S152-9. https://doi.org/10.1093/cid/cix655.
51. Verani J.R., McGee L., Schrag S.J. Prevention of perinatal group B streptococcal disease--revised guidelines from CDC, 2010. MMWR Recomm. Rep. 2010; 59(RR-10): 1-32.
52. Olsen P., Williamson M., Traynor V., Georgiou C. The impact of oral probiotics on vaginal Group B Streptococcal colonisation rates in pregnant women: A pilot randomised control study. Women Birth. 2018; 31: 31-7. https://doi.org/10.1016/j.wombi.2017.06.012
53. Ho M., Chang Y.Y., Chang W.C., Lin H.C., Wang M.H., Lin W.C., Chiu T.H. Oral Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 to reduce Group B Streptococcus colonization in pregnant women: A randomized controlled trial. Taiwan. J. Obstet. Gynecol. 2016; 55(4): 515-8. https://doi.org/10.1016/j.tjog.2016.06.003.
54. Nelson D.B., Hanlon A., Nachamkin I., Haggerty C., Mastrogiannis D.S., Liu C., Fredricks D.N. Early pregnancy changes in bacterial vaginosis-associated bacteria and preterm delivery. Paediatr. Perinat. Epidemiol. 2014; 28: 88-96. https://doi.org/10.1111/ppe.12106.
55. Myhre R., Brantsæter A.L., Myking S., Gjessing H.K., Sengpiel V., Meltzer H.M. et al. Intake of probiotic food and risk of spontaneous preterm delivery. Am. J. Clin. Nutr. 2011; 93(1): 151-7. https://doi.org/10.3945/ajcn.110.004085.
56. Krauss-Silva L., Moreira M.E.L., Alves M.B., Braga A., Camacho K.G., Batista M.R.R. et al. A randomised controlled trial of probiotics for the prevention of spontaneous preterm delivery associated with bacterial vaginosis: Preliminary results. Trials. 2011; 12: 239. https://doi.org/10.1186/1745-6215-12-239.
57. Dotterud C.K., Storrø O., Johnsen R., Oien T. Probiotics in pregnant women to prevent allergic disease: A randomized, double-blind trial. Br. J. Dermatol. 2010; 163(3): 616-23. https://doi.org/10.1111/j.1365-2133.2010.09889.x.
58. Enomoto T., Sowa M., Nishimori K., Shimazu S., Yoshida A., Yamada K. et al. Effects of bifidobacterial supplementation to pregnant women and infants in the prevention of allergy development in infants and on fecal microbiota. Allergol. Int. 2014; 63(4): 575-85. https://doi.org/10.2332/allergolint.13-OA-0683.
59. Rautava S., Kainonen E., Salminen S., Isolauri E. Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J. Allergy Clin. Immunol. 2012; 130(6): 1355-60. https://doi.org/10.1016/j.jaci.2012.09.003.
60. Kim J.Y., Kwon J.H., Ahn S.H., Lee S.I., Han Y.S., Choi Y.O. et al. Effect of probiotic mix (Bifidobacterium bifidum, Bifidobacterium lactis, Lactobacillus acidophilus) in the primary prevention of eczema: A double-blind, randomized, placebo-controlled trial. Pediatr. Allergy Immunol. 2010; 21(2, Pt2): e386-93. https://doi.org/10.1111/j.1399-3038.2009.00958.x.
61. Niers L., Martín R., Rijkers G., Sengers F., Timmerman H., van Uden N. et al. The effects of selected probiotic strains on the development of eczema (the PandA study). Allergy. 2009; 64(9): 1349-58. https://doi.org/10.1111/j.1398-9995.2009.02021.x.
62. Fiocchi A., Pawankar R., Cuello-Garcia C., Ahn K., Al-Hammadi S., Agarwal A. et al. World Allergy Organization-McMaster University Guidelines for allergic disease prevention (GLAD-P): probiotics. World Allergy Organ. J. 2015; 8(1): 4. https://doi.org/10.1186/s40413-015-0055-2.
63. Baldassarre M.E., Di Mauro A., Mastromarino P., Fanelli M., Martinelli D., Urbano F. et al. Administration of a multi-strain probiotic product to women in the perinatal period differentially affects the breast milk cytokine profile and may have beneficial effects on neonatal gastrointestinal function symptoms. A randomized clinical trial. Nutrients. 2016; 8: 677. https://doi.org/10.3390/nu8110677.
64. Asgharian H., Homayouni-Rad A., Mirghafourvand M. et al. Effect of probiotic yoghurt on plasma glucose in overweight and obese pregnant women: a randomized controlled clinical trial. Eur. J. Nutr. 2019 May 8. https ://doi.org/10.1007/s0039 4-019-01900 -1.
65. Allen S.J., Jordan S., Storey M., Thornton C.A., Gravenor M., Garaiova I. et al. Dietary supplementation with lactobacilli and bifidobacteria is well tolerated and not associated with adverse events during late pregnancy and early infancy. J. Nutr. 2010; 140(3): 483-8. https://doi.org/10.3945/jn.109.117093.
66. Luoto R., Laitinen K., Nermes M., Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: A double-blind, placebo-controlled study. Br. J. Nutr. 2010; 103(12): 1792-9. https://doi.org/10.1017/S0007114509993898.

Received 11.07.2019

Accepted 23.08.2019