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

Published online by Cambridge University Press:  24 September 2015

J. G. Wallace ,
W. Gohir  and
D. M. Sloboda
J. G. Wallace
Affiliation:
Department of Medical Sciences, McMaster University, Hamilton, Ontario, Canada Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, Ontario, Canada
W. Gohir
Affiliation:
Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, Ontario, Canada
D. M. Sloboda*
Affiliation:
Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada Farncombe Family Digestive Health Research Institute, McMaster University, Hamilton, Ontario, Canada Departments of Obstetrics and Gynecology and Pediatrics, McMaster University, Hamilton, Ontario, Canada
*
*Address for correspondence: D. M. Sloboda, Department of Biochemistry and Biomedical Sciences, McMaster University, HSC4H30A, 1280 Main St W, Hamilton, ON L8N 3Z5, Canada. (Email [email protected])
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Abstract

The rise in the occurrence of obesity to epidemic proportions has made it a global concern. Great difficulty has been experienced in efforts to control this growing problem with lifestyle interventions. Thus, attention has been directed to understanding the events of one of the most critical periods of development, perinatal life. Early life adversity driven by maternal obesity has been associated with an increased risk of metabolic disease and obesity in the offspring later in life. Although a mechanistic link explaining the relationship between maternal and offspring obesity is still under investigation, the gut microbiota has come forth as a new factor that may play a role modulating metabolic function of both the mother and the offspring. Emerging evidence suggests that the gut microbiota plays a much larger role in mediating the risk of developing non-communicable disease, including obesity and metabolic dysfunction in adulthood. With the observation that the early life colonization of the neonatal and postnatal gut is mediated by the perinatal environment, the number of studies investigating early life gut microbial establishment continues to grow. This paper will review early life gut colonization in experimental animal models, concentrating on the role of the early life environment in offspring gut colonization and the ability of the gut microbiota to dictate risk of disease later in life.

Keywords

developmental programmingmicrobiomeoffspring
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 1: Themed Issue: The Gut Microbiome and Immunity: How it is Shaped by Early Life , February 2016 , pp. 15 - 24
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© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. World Health Organization. BMI Classification. 2015. World Health Organization.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
8. Gluckman, P, Hanson, M. The Developmental Origins of Health and Disease. 2006. Springer: New York.CrossRefGoogle Scholar
9. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183–187.CrossRefGoogle ScholarPubMed
10. Turnbaugh, PJ, Ley, RE, Mahowald, MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444, 1027–1031.Google Scholar
11. Henao-Mejia, J, Elinav, E, Jin, C, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature. 2012; 482, 179–185.CrossRefGoogle ScholarPubMed
12. Aagaard, K, Ma, J, Antony, KM, et al. The placenta harbors a unique microbiome. Sci Trans Med 2014; 6, 237ra65.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
14. Gritz, EC, Bhandari, V. The human neonatal gut microbiome: a brief review. Front Pediatr. 2015; 3, 17.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
16. Barker, DJ. Childhood causes of adult diseases. Arch Dis Child. 1988; 63, 867–869.Google Scholar
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.CrossRefGoogle ScholarPubMed
18. Barker, DJP. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171–174.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
37. Grant, WF, 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
40. Whitman, WB, Coleman, DC, Wiebe, WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci. 1998; 95, 6578–6583.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
43. Nieuwdorp, M, Gilijamse, PW, Pai, N, Kaplan, LM. Role of the microbiome in energy regulation and metabolism. Gastroenterology. 2014; 146, 1525–1533.Google Scholar
44. Hooper, LV, Macpherson, AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol. 2010; 10, 159–169.Google Scholar
45. Turner, JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009; 9, 799–809.CrossRefGoogle ScholarPubMed
46. Reyniers, JA. The pure-culture concept and gnotobiotics. Ann N Y Acad Sci. 1959; 78, 3–16.CrossRefGoogle Scholar
47. Thompson, GR, Trexler, PC. Gastrointestinal structure and function in germ-free or gnotobiotic animals. Gut. 1971; 12, 230–235.Google Scholar
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.CrossRefGoogle ScholarPubMed
49. Ley, RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010; 26, 5–11.CrossRefGoogle ScholarPubMed
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.Google Scholar
51. Tissier, H. Recherches Sur la blore Intestinales des Nourrisons (etat Normal et Pathologiques). 1900. G. Carré et C. Naud: Paris, France.Google Scholar
52. Lamont, RF. Infection in the prediction and antibiotics in the prevention of spontaneous preterm labour and preterm birth. BJOG. 2003; 110, 71–75.Google Scholar
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.Google Scholar
54. Methe, B. A framework for human microbiome research. Nature. 2012; 486, 215–221.Google Scholar
55. Jiménez, E, Marín, ML, Martín, R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187–193.Google Scholar
56. Moles, L, Gómez, M, 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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
61. Pacha, J. Development of intestinal transport function in mammals. Physiol Rev. 2000; 80, 1633–1667.Google Scholar
62. Mackie, RI, Sghir, A, Gaskins, HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr. 1999; 69, 1035s–1045ss.Google Scholar
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.Google Scholar
64. Rescigno, M, Rotta, G, Valzasina, B, Ricciardi-Castagnoli, P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001; 204, 572–581.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
67. Funkhouser, LJ, Bordenstein, SR. Mom knows best: the universality of maternal microbial transmission. PLoS Biol. 2013; 11, e1001631.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
74. Murono, K, Fujita, K, Yoshikawa, M, et al. Acquisition of nonmaternal enterobacteriaceae by infants delivered in hospitals. J Pediatr. 1993; 122, 120–125.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
77. Wang, M, Radlowski, EC, Monaco, MH, et al. Mode of delivery and early nutrition modulate microbial colonization and fermentation products in neonatal piglets. J Nutr. 2013; 143, 795–803.Google Scholar
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.Google Scholar
79. Gomez-Llorente, C, Plaza-Diaz, J, Aguilera, M, et al. Three main factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr. 2013; 57, 461–466.Google Scholar
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.Google Scholar
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.Google Scholar
82. Le, J, Briggs, GG, McKeown, A, Bustillo, G. Urinary tract infections during pregnancy. Ann Pharmacother. 2004; 38, 1692–1701.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
100. Kostic, AD, Howitt, MR, Garrett, WS. Exploring host–microbiota interactions in animal models and humans. Genes Dev. 2013; 27, 701–718.Google Scholar
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.Google Scholar
102. Hofmann, RR. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia. 1989; 78, 443–457.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
106. Waterland, RA, Travisano, M, Tahiliani, KG, Rached, MT, Mirza, S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes. 2008; 32, 1373–1379.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
110. Benaissa, N, Merzouk, H, Merzouk, SA, Narce, M. Effects of maternal linseed oil supplementation on metabolic parameters in cafeteria diet-induced obese rats. Biomed Environ Sci. 2015; 28, 298–302.Google Scholar
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.Google Scholar
112. Cordero, P, Milagro, FI, Campion, J, Martinez, JA. Supplementation with methyl donors during lactation to high-fat-sucrose-fed dams protects offspring against liver fat accumulation when consuming an obesogenic diet. J Dev Orig Health Dis. 2014; 5, 385–395.Google Scholar
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.Google Scholar
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.Google Scholar
115. Hansen, CHF, Krych, Ł, Buschard, K, et al. A maternal gluten-free diet reduces inflammation and diabetes incidence in the offspring of NOD mice. Diabetes. 2014; 63, 2821–2832.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
119. Field, CJ. The immunological components of human milk and their effect on immune development in infants. J Nutr. 2005; 135, 1–4.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
125. Karlsson, CL, Molin, G, Fak, F, et al. Effects on weight gain and gut microbiota in rats given bacterial supplements and a high-energy-dense diet from fetal life through to 6 months of age. Br J Nutr. 2011; 106, 887–895.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
129. Ibrahim, Y, Kearney, SM, Levkovich, T, et al. Maternal gut microbes control offspring sex and survival. J Probiotics Health. 2015; 2, 120.Google Scholar
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.Google Scholar