The impact of early life gut colonization on metabolic and obesogenic outcomes: What have animal models shown us?

Journal of Developmental Origins of Health and Disease

Volumn 7, Issue 1, 2016, Pages 15-24

  Wallace, J G ^a,b   Gohir, W ^a,b   Sloboda, D M ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

developmental programming; microbiome; offspring

Indexed keywords

ANIMAL; DISEASE MODEL; FEMALE; INTESTINE FLORA; MICROBIOLOGY; NEWBORN; OBESITY; PREGNANCY; PREGNANCY COMPLICATION;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; FEMALE; GASTROINTESTINAL MICROBIOME; OBESITY; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 84943785702     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174415001518     Document Type: Review

References (130)

1. World Health Organization. BMI Classification. 2015. World Health Organization.
2. Hedley AA, Ogden CL, Johnson CL, et al. Prevalence of overweight and obesity among us children, adolescents, and adults, 1999-2002. JAMA. 2004; 291, 2847-2850.
3. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the united states, 2011-2012. JAMA. 2014; 311, 806-814.
4. Catalano P, deMouzon SH. Maternal obesity and metabolic risk to the offspring: why lifestyle interventions may have not achieved the desired outcomes. Int J Obes. 2015; 39, 642-649.
5. Athukorala C, Rumbold A, Willson K, Crowther C. The risk of adverse pregnancy outcomes in women who are overweight or obese. BMC Pregnancy Childbirth. 2010; 10, 56.
6. Crane JM, Murphy P, Burrage L, Hutchens D. Maternal and perinatal outcomes of extreme obesity in pregnancy. J Obstet Gynaecol Can. 2013; 35, 606-611.
7. Portela DS, Vieira TO, Matos SM, de Oliveira NF, Vieira GO. Maternal obesity, environmental factors, cesarean delivery and breastfeeding as determinants of overweight and obesity in children: results from a cohort. BMC Pregnancy Childbirth. 2015; 15, 94.
8. Gluckman P, Hanson M. The Developmental Origins of Health and Disease. 2006. Springer: New York.
9. Gluckman PD, Hanson MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183-187.
10. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesityassociated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444, 1027-1031.
11. Henao-Mejia J, Elinav E, Jin C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature. 2012; 482, 179-185.
12. Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Trans Med 2014; 6, 237ra65.
13. Madan JC, Salari RC, Saxena D, et al. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed. 2012; 97, F456-F462.
14. Gritz EC, Bhandari V. The human neonatal gut microbiome: a brief review. Front Pediatr. 2015; 3, 17.
15. Azad MB, Konya T, Maughan H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can Med Assoc J. 2013; 185, 385-394.
16. Barker DJ. Childhood causes of adult diseases. Arch Dis Child. 1988; 63, 867-869.
17. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577-580.
18. Barker DJP. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171-174.
19. Howie GJ, Sloboda DM, Kamal T, Vickers MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905-915.
20. Zheng J, Xiao X, Zhang Q, et al. Maternal high-fat diet modulates hepatic glucose, lipid homeostasis and gene expression in the PPAR pathway in the early life of offspring. Int J Mol Sci. 2014; 15, 14967-14983.
21. Shankar K, Harrell A, Liu X, et al. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R528-R538.
22. Page KC, Malik RE, Ripple JA, Anday EK. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. 2009; 297, R1049-R1057.
23. Samuelsson A-M, Matthews PA, Argenton M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51, 383-392.
24. Nivoit P,Morens C, Van Assche FA, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009; 52, 1133-1142.
25. Howie GJ, Sloboda DM, Reynolds CM, Vickers MH. Timing of maternal exposure to a high fat diet and development of obesity and hyperinsulinemia in male rat offspring: same metabolic phenotype, different developmental pathways? J Nutr Metab. 2013; 2013, 517384.
26. Taylor PD, McConnell J, Khan IY, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Integr Comp Physiol. 2005; 288, R134-R139.
27. Borengasser SJ, Lau F, Kang P, et al. Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One. 2011; 6, e24068.
28. Oben JA, Mouralidarane A, Samuelsson A-M, et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol. 2010; 52, 913-920.
29. Bruce KD, Cagampang FR, Argenton M, et al. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology. 2009; 50, 1796-1808.
30. Connor KL, Vickers MH, Beltrand J, Meaney MJ, Sloboda DM. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol. 2012; 590, 2167-2180.
31. Yan X, Huang Y, Zhao J-X, et al.Maternal obesity-impaired insulin signaling in sheep and induced lipid accumulation and fibrosis in skeletal muscle of offspring. Biol Reprod. 2011; 85, 172-178.
32. Zhu MJ, Han B, Tong J, et al. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol. 2008; 586, 2651-2664.
33. Yan X, Zhu MJ, Xu W, et al. Up-regulation of toll-like receptor 4/nuclear factor-κB signaling is associated with enhanced adipogenesis and insulin resistance in fetal skeletal muscle of obese sheep at late gestation. Endocrinology. 2010; 151, 380-387.
34. McCurdy CE, Bishop JM, Williams SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009; 119, 323-335.
35. Conner B, Hetrik B, Chicco A, McCurdy C. Maternal obesity alters offspring muscle mitochondrial function in nonhuman primates. FASEB J. 2015; 29, 1036-1037.
36. Fan L, Lindsley SR, Comstock SM, et al. Maternal high-fat diet impacts endothelial function in nonhuman primate offspring. Int J Obes. 2013; 37, 254-262.
37. GrantWF, Gillingham MB, Batra AK, et al. Maternal high fat diet is associated with decreased plasma n-3 fatty acids and fetal hepatic apoptosis in nonhuman primates. PLoS One. 2011; 6, e17261.
38. Grant WF, Nicol LE, Thorn SR, et al.. Perinatal exposure to a high-fat diet is associated with reduced hepatic sympathetic innervation in one-year old male Japanese macaques. PLoS One. 2012; 7, e48119.
39. Suter MA, Chen A, Burdine MS, et al. A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J. 2012; 26, 5106-5114.
40. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci. 1998; 95, 6578-6583.
41. Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK. Chapter 8-Host-bacterial symbiosis in health and disease. In Advances in Immunology (eds. Sidonia F, Andrea C), 2010; pp. 243-274. Academic Press: Pasadena, CA.
42. Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004; 101, 15718-15723.
43. Nieuwdorp M, Gilijamse PW, Pai N, Kaplan LM. Role of the microbiome in energy regulation and metabolism. Gastroenterology. 2014; 146, 1525-1533.
44. Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol. 2010; 10, 159-169.
45. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009; 9, 799-809.
46. Reyniers JA. The pure-culture concept and gnotobiotics. An N Y Acad Sci. 1959; 78, 3-16.
47. Thompson GR, Trexler PC. Gastrointestinal structure and function in germ-free or gnotobiotic animals. Gut. 1971; 12, 230-235.
48. Duncan SH, Lobley GE, Holtrop G, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes. 2008; 32, 1720-1724.
49. Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010; 26, 5-11.
50. Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005; 102, 11070-11075.
51. Tissier H. Recherches Sur la blore Intestinales des Nourrisons (etat Normal et Pathologiques). 1900. G. Carré et C. Naud: Paris, France.
52. Lamont RF. Infection in the prediction and antibiotics in the prevention of spontaneous preterm labour and preterm birth. BJOG. 2003; 110, 71-75.
53. Schaedler RW, Dubos R, Costello R. The development of the bacterial flora in the gastrointestinal tract of mice. J Exp Med. 1965; 122, 59-66.
54. Methe B. A framework for human microbiome research. Nature. 2012; 486, 215-221.
55. Jiménez E, Marín ML, Martín R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187-193.
56. Moles L, GómezM,Heilig H, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One. 2013; 8, e66986.
57. Jiménez E, Fernández L, Marín M, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005; 51, 270-274.
58. Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008; 88, 894-899.
59. Fak F, Ahrne S, Molin G, Jeppsson B, Westrom B. Microbial manipulation of the rat dam changes bacterial colonization and alters properties of the gut in her offspring. Am J Physiol Gastrointest Liver Physiol. 2008; 294, G148-G154.
60. Mueller NT, Whyatt R, Hoepner L, et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes. 2015; 39, 665-670.
61. Pacha J. Development of intestinal transport function in mammals. Physiol Rev. 2000; 80, 1633-1667.
62. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999; 69, 1035s-1045ss.
63. Perez PF, Doré J, Leclerc M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007; 119, e724-e732.
64. Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001; 204, 572-581.
65. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001; 2, 361-367.
66. Jin L, Hinde K, Tao L. Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta). J Med Primatol. 2011; 40, 52-58.
67. Funkhouser LJ, Bordenstein SR. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 2013; 11, e1001631.
68. Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150, 470-480.
69. Jost T, Lacroix C, Braegger C, Chassard C. Stability of the maternal gut microbiota during late pregnancy and early lactation. Curr Microbiol. 2014; 68, 419-427.
70. Makino H, Kushiro A, Ishikawa E, et al. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota. PLoS One. 2013; 8, e78331.
71. Biasucci G, Rubini M, Riboni S, et al. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev. 2010; 86(Suppl 1), 13-15.
72. Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast-and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe. 2011; 17, 478-482.
73. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010; 107, 11971-11975.
74. Murono K, Fujita K, Yoshikawa M, et al. Acquisition of nonmaternal enterobacteriaceae by infants delivered in hospitals. J Pediatr. 1993; 122, 120-125.
75. Gronlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr. 1999; 28, 19-25.
76. Salminen S, Gibson GR, McCartney AL, Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut. 2004; 53, 1388-1389.
77. WangM, Radlowski EC,MonacoMH, et al.Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr. 2013; 143, 795-803.
78. Fallani M, Young D, Scott J, et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J Pediatr Gastroenterol Nutr. 2010; 51, 77-84.
79. Gomez-Llorente C, Plaza-Diaz J, Aguilera M, et al. Threemain factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr. 2013; 57, 461-466.
80. Hansen CH, Andersen LS, Krych L, et al. Mode of delivery shapes gut colonization pattern and modulates regulatory immunity in mice. J Immunol. 2014; 193, 1213-1222.
81. Goedert JJ, Hua X, Yu G, Shi J. Diversity and composition of the adult fecal microbiome associated with history of cesarean birth or appendectomy: analysis of the American gut project. EBioMedicine. 2014; 1, 167-172.
82. Le J, Briggs GG, McKeown A, Bustillo G. Urinary tract infections during pregnancy. An Pharmacother. 2004; 38, 1692-1701.
83. Chan BT, Hohmann E, Barshak MB, Pukkila-Worley R. Treatment of listeriosis in first trimester of pregnancy. Emerg Infect Dis. 2013; 19, 839-841.
84. Sheehy O, Santos F, Ferreira E, Berard A. The use of metronidazole during pregnancy: a review of evidence. Curr Drug Saf. 2015; 10, 170-179.
85. Turrentine MA, Greisinger AJ, Brown KS, Wehmanen OA, Mouzoon ME. Duration of intrapartum antibiotics for group B streptococcus on the diagnosis of clinical neonatal sepsis. Infect Dis Obstet Gynecol. 2013; 2013, 525878.
86. Stokholm J, Schjorring S, Eskildsen CE, et al. Antibiotic use during pregnancy alters the commensal vaginal microbiota. Clin Microbiol Infect. 2014; 20, 629-635.
87. Jauréguy F, Carton M, Panel P, et al. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J Clin Microbiol. 2004; 42, 5184-5188.
88. Mangin I, Suau A, Gotteland M, Brunser O, Pochart P. Amoxicillin treatment modifies the composition of Bifidobacterium species in infant intestinal microbiota. Anaerobe. 2010; 16, 433-438.
89. Arnal M-E, Zhang J, Erridge C, Smidt H, Lallès J-P. Maternal antibiotic-induced early changes in microbial colonization selectively modulate colonic permeability and inducible heat shock proteins, and digesta concentrations of alkaline phosphatase and TLR-Stimulants in swine offspring. PLoS One. 2015; 10, e0118092.
90. Scarpellini E, Lupo M, Iegri C, et al. Intestinal permeability in non-alcoholic fatty liver disease: the gut-liver axis. Rev Recent Clin Trials. 2014; 9, 141-147.
91. Tormo-Badia N, Hakansson A, Vasudevan K, et al. Antibiotic treatment of pregnant non-obese diabetic mice leads to altered gut microbiota and intestinal immunological changes in the offspring. Scand J Immunol. 2014; 80, 250-260.
92. Turnbaugh PJ, Ridaura VK, Faith JJ, et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 1, 6ra14.
93. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008; 3, 213-223.
94. Santacruz A, Collado MC, Garcia-Valdes L, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010; 104, 83-92.
95. Yan X, Huang Y, Wang H, et al. Maternal obesity induces sustained inflammation in both fetal and offspring large intestine of sheep. Inflamm Bowel Dis. 2011; 17, 1513-1522.
96. Stenman LK, Holma R, Korpela R. High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids. World J Gastroenterol. 2012; 18, 923-929.
97. Huang S, Rutkowsky JM, Snodgrass RG, et al. Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J Lipid Res. 2012; 53, 2002-2013.
98. Myles IA, Fontecilla NM, Janelsins BM, et al. Parental dietary fat intake alters offspring microbiome and immunity. J Immunol (Baltimore, Md: 1950). 2013; 191. 10.4049/jimmunol.1301057.
99. Myles IA, Pincus NB, Fontecilla NM, Datta SK. Effects of parental omega-3 fatty acid intake on offspring microbiome and immunity. PLoS One. 2014; 9, e87181.
100. Kostic AD, Howitt MR, Garrett WS. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 2013; 27, 701-718.
101. Nguyen TLA, Vieira-Silva S, Liston A, Raes J. How informative is the mouse for human gut microbiota research? Dis Model Mech. 2015; 8, 1-16.
102. Hofmann RR. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia. 1989; 78, 443-457.
103. Ma J, Prince AL, Bader D, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun. 2014; 5, 3889.
104. Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S, Christian LM. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS One. 2014; 9, e113026.
105. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005; 135, 1382-1386.
106. Waterland RA, TravisanoM, Tahiliani KG, RachedMT,Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes. 2008; 32, 1373-1379.
107. Stoffers DA, Desai BM, DeLeon DD, Simmons RA. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes. 2003; 52, 734-740.
108. Fisher RE, Or'Rashid M, Quinton M, et al. Maternal supplementation with fishmeal protects against late gestation endotoxin-induced fetal programming of the ovine hypothalamic-pituitary-adrenal axis. J Dev Orig Health Dis. 2014; 5, 206-213.
109. Gray C, Vickers MH, Segovia SA, Zhang XD, Reynolds CM. A maternal high fat diet programmes endothelial function and cardiovascular status in adult male offspring independent of body weight, which is reversed by maternal Conjugated Linoleic Acid (CLA) supplementation. PLoS One. 2015; 10, e0115994.
110. BenaissaN,MerzoukH,Merzouk SA,NarceM. Effects ofmaternal linseed oil supplementation on metabolic parameters in cafeteria dietinduced obese rats. Biomed Environ Sci. 2015; 28, 298-302.
111. Carlin J, George R, Reyes TM. Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS One. 2013; 8, e63549.
112. Cordero P, Milagro FI, Campion J, Martinez JA. Supplementation with methyl donors during lactation to highfat-sucrose-fed dams protects offspring against liver fat accumulation when consuming an obesogenic diet. J Dev Orig Health Dis. 2014; 5, 385-395.
113. Schaible TD, Harris RA, Dowd SE, Smith CW, Kellermayer R. Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes. Hum Mol Genet. 2011; 20, 1687-1696.
114. Willing BP, Dicksved J, Halfvarson J, et al. A Pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology. 2010; 139, 1844-54.e1.
115. Hansen CHF, Krych Ł, Buschard K, et al. A maternal glutenfree diet reduces inflammation and diabetes incidence in the offspring of NOD mice. Diabetes. 2014; 63, 2821-2832.
116. 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, 1355-1360.
117. Rautava S, Kalliomäki M, Isolauri E. Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol. 2002; 109, 119-121.
118. Boyle RJ, Ismail IH, Kivivuori S, et al. Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial. Allergy. 2011; 66, 509-516.
119. Field CJ. The immunological components of humanmilk and their effect on immune development in infants. J Nutr. 2005; 135, 1-4.
120. Gueimonde M, Laitinen K, Salminen S, Isolauri E. Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology. 2007; 92, 64-66.
121. Abrahamsson TR, Sinkiewicz G, Jakobsson T, Fredrikson M, Björkstén B. Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr. 2009; 49, 349-354.
122. Starke IC, Pieper R, Neumann K, Zentek J, Vahjen W. Individual responses of mother sows to a probiotic Enterococcus faecium strain lead to different microbiota composition in their offspring. Benef Microbes. 2013; 4, 345-356.
123. Taras D, Vahjen W, Macha M, Simon O. Response of performance characteristics and fecal consistency to long-lasting dietary supplementation with the probiotic strain Bacillus cereus var. toyoi to sows and piglets. Arch Anim Nutr. 2005; 59, 405-417.
124. Jadamus A, Vahjen W, Schäfer K, Simon O. Influence of the probiotic strain Bacillus cereus var. toyoi on the development of enterobacterial growth and on selected parameters of bacterial metabolism in digesta samples of piglets. J Anim Physiol Anim Nutr (Berl). 2002; 86, 42-54.
125. Karlsson CL, Molin G, Fak F, et al. Effects on weight gain and gut microbiota in rats given bacterial supplements and a highenergy-dense diet from fetal life through to 6 months of age. Br J Nutr. 2011; 106, 887-895.
126. Hallam MC, Barile D, Meyrand M, German JB, Reimer RA. Maternal high-protein or high-prebiotic-fiber diets affect maternal milk composition and gut microbiota in rat dams and their offspring. Obesity. 2014; 22, 2344-2351.
127. Sela DA, Li Y, Lerno L, et al. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem. 2011; 286, 11909-11918.
128. Oozeer R, van Limpt K, Ludwig T, et al. Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides. Am J Clin Nutr. 2013; 98, 561S-571SS.
129. Ibrahim Y, Kearney SM, Levkovich T, et al. Maternal gut microbes control offspring sex and survival. J Probiotics Health. 2015; 2, 120.
130. Abecia L, Fondevila M, Balcells J, McEwan NR. The effect of lactating rabbit does on the development of the caecal microbial community in the pups they nurture. J Appl Microbiol. 2007; 103, 557-564.