Fetal programming of overweight through the microbiome: Boys are disproportionately affected

Journal of Developmental Origins of Health and Disease

Volumn 7, Issue 1, 2016, Pages 25-34

  Kozyrskyj, A L ^a,b   Kalu, R ^a   Koleva, P T ^a   Bridgman, S L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

gut; infant; microbiota; overweight; pregnancy

Indexed keywords

CHILD DEVELOPMENT; FEMALE; FETUS DEVELOPMENT; HUMAN; INNATE IMMUNITY; INTESTINE FLORA; MALE; MICROBIOLOGY; NEWBORN; OBESITY; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; SEXUAL DEVELOPMENT;

CHILD DEVELOPMENT; FEMALE; FETAL DEVELOPMENT; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNITY, INNATE; INFANT, NEWBORN; MALE; OVERWEIGHT; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS;

EID: 84933567371     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174415001269     Document Type: Review

References (91)

1. Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358-368.
2. Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412-417.
3. Azad MB, Kozyrskyj AL. Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol. 2012; 2012, 932072.
4. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010. JAMA. 2012; 307, 483-490.
5. Shields M. Overweight and obesity among children and youth. Health Rep. 2006; 17, 27-42.
6. Serdula MK, Ivery D, Coates RJ, et al. Do obese children become obese adults? A review of the literature. Prev Med. 1993; 22, 167-177.
7. Weng SF, Redsell SA, Swift JA, Yang M, Glazebrook CP. Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch Dis Child. 2012; 97, 1019-1026.
8. Begum F, Colman I, McCargar LJ, Bell RC. Gestational weight gain and early postpartum weight retention in a prospective cohort of alberta women. J Obstet Gynaecol Can. 2012; 34, 637-647.
9. Yogev Y, Catalano PM. Pregnancy and obesity. Obstet Gynecol Clin North Am. 2009; 36, 285-300.
10. Cassidy-Bushrow AE, Peters RM, Johnson DA, Li J, Rao DS. Vitamin D nutritional status and antenatal depressive symptoms in African American women. J Womens Health (Larchmt). 2012; 21, 1189-1195.
11. Poston L. Gestational weight gain: influences on the long-termhealth of the child. Curr Opin Clin Nutr Metab Care. 2012; 15, 252-257.
12. Heslehurst N, Simpson H, Ells LJ, et al. The impact of maternal BMI status on pregnancy outcomes with immediate short-term obstetric resource implications: a meta-analysis. Obes Rev. 2008; 9, 635-683.
13. 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.
14. Angelakis E, Armougom F, Million M, Raoult D. The relationship between gut microbiota and weight gain in humans. Future Microbiol. 2012; 7, 91-109.
15. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012; 9, 577-589.
16. Brahe LK, Astrup A, Larsen LH. Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes Rev. 2013; 14, 950-959.
17. Le Chatelier E, Nielsen T, Qin J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013; 500, 541-546.
18. Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013; 341, 1241214.
19. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in lactobacillus in obese patients and methanogens in anorexic patients. PLoS One. 2009; 4, 1-8.
20. Koleva PT, Bridgman SL, Kozyrskyj AL. The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients. 2015; 7, 2237-2260.
21. Karlsson CL, Onnerfalt J, Xu J, et al. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity (Silver Spring). 2012; 20, 2257-2261.
22. Bervoets L, Van HK, Kortleven I, et al. Differences in gut microbiota composition between obese and lean children: a crosssectional study. Gut Pathog. 2013; 5, 10.
23. Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Obesity (Silver Spring). 2010; 18, 190-195.
24. Payne AN, Chassard C, Zimmermann M, et al. The metabolic activity of gut microbiota of obese children is increased compared with normal-weight children and exhibits more exhaustive substrate utilization. Nutr Diabetes. 2011; e12, 1-8.
25. Penders J, Thijs C, Vink C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006; 118, 511-521.
26. 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. CMAJ. 2013; 185, 385-394.
27. Kaplan JL, Walker WA. Early gut colonization and subsequent obesity risk. Curr Opin Clin Nutr Metab Care. 2012; 15, 278-284.
28. Luoto R, Kalliomaki M, Laitinen K, et al. Initial dietary and microbiological environments deviate in normal-weight compared to overweight children at 10 years of age. J Pediatr Gastroenterol Nutr. 2011; 52, 90-95.
29. Vael C, Verhulst SL, Nelen V, Goossens H, Desager KN. Intestinal microflora and body mass index during the first three years of life: an observational study. Gut Pathog. 2011; 3, 8.
30. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008; 87, 534-538.
31. Scheepers LE, Penders J, Mbakwa CA, et al. The intestinal microbiota composition and weight development in children: the KOALA Birth Cohort Study. Int J Obes (Lond). 2015; 39, 16-25.
32. White RA, Bjornholt JV, Baird DD, et al. Novel developmental analyses identify longitudinal patterns of early gut microbiota that affect infant growth. PLoS Comput Biol. 2013; 9, e1003042.
33. Koleva PT, Bridgman SL, Kozyrskyj AL. The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients. 2015; 7, 2237-2260.
34. Eggesbo M, Moen B, Peddada S, et al. Development of gut microbiota in infants not exposed to medical interventions. APMIS. 2011; 119, 17-35.
35. Jakobsson HE, Abrahamsson TR, Jenmalm MC, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014; 63, 559-566.
36. Brandt K, Taddei CR, Takagi EH, et al. Establishment of the bacterial fecal community during the first month of life in Brazilian newborns. Clinics (Sao Paulo). 2012; 67, 113-123.
37. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.
38. Rautava S, Collado MC, 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, 178-184.
39. Jimenez E, Marin ML, Martin R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187-193.
40. Gosalbes MJ, Llop S, Valles Y, et al. 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, 198-211.
41. Kollmann TR, Levy O, Montgomery RR, Goriely S. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly. Immunity. 2012; 37, 771-783.
42. Brandtzaeg P. Homeostatic impact of indigenous microbiota and secretory immunity. Benef Microbes. 2010; 1, 211-227.
43. Mirpuri J, Raetz M, Sturge CR, et al. Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microbes. 2014; 5, 28-39.
44. Kohler H, Donarski S, Stocks B, et al. Antibacterial characteristics in the feces of breast-fed and formula-fed infants during the first year of life. J Pediatr Gastroenterol Nutr. 2002; 34, 188-193.
45. Sjogren YM, Tomicic S, Lundberg A, et al. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy. 2009; 39, 1842-1851.
46. Kukkonen K, Kuitunen M, Haahtela T, et al. High intestinal IgA associates with reduced risk of IgE-associated allergic diseases. Pediatr Allergy Immunol. 2010; 21(1 Pt 1), 67-73.
47. Pallaro A, Barbeito S, Taberner P, et al. Total salivary IgA, serum C3c and IgA in obese school children. J Nutr Biochem. 2002; 13, 539.
48. Chandel DS, Braileanu GT, Chen JH, Chen HH, Panigrahi P. Live colonocytes in newborn stool: surrogates for evaluation of gut physiology and disease pathogenesis. Pediatr Res. 2011; 70, 153-158.
49. Patro B, Liber A, Zalewski B, et al. Maternal and paternal body mass index and offspring obesity: a systematic review. An Nutr Metab. 2013; 63, 32-41.
50. Paliy O, Piyathilake CJ, Kozyrskyj A, et al. Excess body weight during pregnancy and offspring obesity: potential mechanisms. Nutrition. 2014; 30, 245-251.
51. Cox LM, Blaser MJ. Pathways in microbe-induced obesity. Cell Metab. 2013; 17, 883-894.
52. Persaud RR, Azad MB, Chari RS, et al. Perinatal antibiotic exposure of neonates in Canada and associated risk factors: a population-based study. J Matern Fetal Neonatal Med. 2014; 14, 1-6.
53. Hakansson S, Kallen K. High maternal body mass index increases the risk of neonatal early onset group B streptococcal disease. Acta Paediatr. 2008; 97, 1386-1389.
54. Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150, 470-480.
55. 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.
56. 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.
57. Collado MC, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res. 2012; 72, 77-85.
58. Collado MC, 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, 1023-1030.
59. Galley JD, Bailey M, Kamp DC, Schoppe-Sullivan S, Christian LM. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS One. 2014; 9, e113026.
60. Solt I. The human microbiome and the great obstetrical syndromes: a new frontier in maternal-fetal medicine. Best Pract Res Clin Obstet Gynaecol. 2015; 29, 165-175.
61. Vitali B, Cruciani F, Baldassarre ME, et al. Dietary supplementation with probiotics during late pregnancy: outcome on vaginal microbiota and cytokine secretion. BMC Microbiol. 2012; 12, 236.
62. Konstantinov SR, van der Woude CJ, Peppelenbosch MP. Do pregnancy-related changes in the microbiome stimulate innate immunity? Trends Mol Med. 2013; 19, 454-459.
63. Gohir W, Ratcliffe EM, Sloboda DM. Of the bugs that shape us: maternal obesity, the gut microbiome, and long-term disease risk. Pediatr Res. 2015; 77, 196-204.
64. Cho CE, Norman M. Cesarean section and development of the immune system in the offspring. Am J Obstet Gynecol. 2013; 208, 249-254.
65. Priyadarshini M, Thomas A, Reisetter AC, et al. Maternal shortchain fatty acids are associated with metabolic parameters in mothers and newborns. Transl Res. 2014; 164, 153-157.
66. Mischke M, Plosch T. More than just a gut instinct - the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am J Physiol Regul Integr Comp Physiol. 2013; 304, R1065-R1069.
67. Vidal AC, Murphy SK, Murtha AP, et al. Associations between antibiotic exposure during pregnancy, birth weight and aberrant methylation at imprinted genes among offspring. Int J Obes (Lond). 2013; 37, 907-913.
68. Xu P, Li M, Zhang J, Zhang T. Correlation of intestinal microbiota with overweight and obesity in Kazakh school children. BMC Microbiol. 2012; 12, 283.
69. Ip S, Chung M, Raman G, Trikalinos TA, Lau J. A summary of the Agency for Healthcare Research and Quality's evidence report on breastfeeding in developed countries. Breastfeed Med. 2009; 4 (Suppl. 1), S17-S30.
70. Holscher HD, Faust KL, Czerkies LA, et al. Effects of prebioticcontaining infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. J Parenter Enteral Nutr. 2012; 36(Suppl.), 95S-105S.
71. Aagaard K, Riehle K, Ma J, et al. A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One. 2012; 7, e36466.
72. Robinson EL, Thompson WL. Effect of weight gain of the addition of Lactobacillus acidophilus to the formula of newborn infants. J Pediatr. 1952; 41, 395-398.
73. Neuman H, Debelius JW, Knight R, Koren O. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS Microbiol Rev. 2015; February 19 [Epub], pii: fuu010.
74. Dominianni C, Sinha R, Goedert JJ, et al. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 2015; 10, e0124599.
75. Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond). 2011; 35, 522-529.
76. Azad MB, Bridgman SL, Becker AB, Kozyrskyj AL. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int J Obes (Lond). 2014; 38, 1290-1298.
77. Bailey LC, Forrest CB, Zhang P, et al. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 2014; 168, 1063-1069.
78. Murphy R, Stewart AW, Braithwaite I, et al. Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes (Lond). 2014; 38, 1115-1119.
79. Trasande L, Blustein J, Liu M, et al. Infant antibiotic exposures and early-life body mass. Int J Obes (Lond). 2013; 37, 16-23.
80. Cutting TM, Fisher JO, Grimm-Thomas K, Birch LL. Like mother, like daughter: familial patterns of overweight are mediated by mothers' dietary disinhibition. Am J Clin Nutr. 1999; 69, 608-613.
81. Faith MS, Heo M, Kral TV, Sherry B. Compliant eating of maternally prompted food predicts increased body mass index z-score gain in girls: results from a population-based sample. Child Obes. 2013; 9, 427-436.
82. Suzuki K, Kondo N, Sato M, et al. Gender differences in the association between maternal smoking during pregnancy and childhood growth trajectories: multilevel analysis. Int J Obes (Lond). 2011; 35, 53-59.
83. Zheng JS, Liu H, Li J, et al. Exclusive breastfeeding is inversely associated with risk of childhood overweight in a large Chinese cohort. J Nutr. 2014; 144, 1454-1459.
84. Kalu R. Maternal overweight prior to pregnancy and its impact on the infant gut microbiome and subsequent child overweight risk. University of Alberta. 2014.
85. Hesla HM, Stenius F, Jaderlund L, et al. Impact of lifestyle on the gut microbiota of healthy infants and their mothers - the ALADDIN birth cohort. FEMS Microbiol Ecol. 2014; 90, 791-801.
86. Koleva PT, Kim JS, Guttman DS, et al. Bacterial composition of the infant gut is shaped by maternal prenatal weight. International Human Microbiome Congress, Luxembourg, 2015.
87. 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.
88. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486, 207-214.
89. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486, 222-227.
90. Lozupone CA, Stombaugh J, Gonzalez A, et al. Meta-analyses of studies of the human microbiota. Genome Res. 2013; 23, 1704-1714.
91. Lin A, Bik EM, Costello EK, et al. Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS One. 2013; 8, e53838.