Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-28T13:56:08.057Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  29 June 2015

A. L. Kozyrskyj*
Affiliation:
Department of Pediatrics, University of Alberta, Edmonton, AB, Canada School of Public Health, University of Alberta, Edmonton, AB, Canada Department of Community Health Sciences, University of Manitoba, Winnipeg, MB, Canada
R. Kalu
Affiliation:
Department of Pediatrics, University of Alberta, Edmonton, AB, Canada
P. T. Koleva
Affiliation:
Department of Pediatrics, University of Alberta, Edmonton, AB, Canada
S. L. Bridgman
Affiliation:
Department of Pediatrics, University of Alberta, Edmonton, AB, Canada
*
*Address for correspondence: Dr A. Kozyrskyj, Department of Pediatrics, University of Alberta, 3-527 Edmonton Clinic Health Academy, 11405 – 87th Avenue, Edmonton, AB, Canada T6G IC9. (Email kozyrsky@ualberta.ca)

Abstract

Maternal and childhood obesity in pregnancy are worrisome public health issues facing our world today. New gene sequencing methods have advanced our knowledge of the disruptive effect of birth interventions and postnatal exposures on the maturation of gut microbiota and immunity during infancy. Yet, little is known about the impact of maternal pregnancy overweight on gut microbes and related processes, and how this may affect overweight risk in offspring. To address this gap in knowledge, we surveyed human studies for evidence in children, infants and pregnant women to piece together the limited literature and generate hypotheses for future investigation. From this literature, we learned that higher Lactobacillus yet lower Bacteroides spp. colonization of gut microbiota within 3 months of birth predicted risk for infant and child overweight. The abundance of bifidobacteria and staphylococci also appeared to play a role in the association with overweight, as did infant fecal immunoglobulin A levels, glycoproteins of the gut immune system that are acquired from breast milk and produced by the infant. We proposed that pregnancy overweight influences the compositional structure of gut microbiota in infants through vertical transfer of microbiota and/or their metabolites during pregnancy, delivery and breastfeeding. Finally, we brought forward emerging evidence on sex dimorphism, as well as ethnic and geographic variation, in reported associations between maternal overweight-induced gut microbiota dysbiosis and overweight risk.

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 358368.CrossRefGoogle ScholarPubMed
2. Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412417.CrossRefGoogle ScholarPubMed
3. Azad, MB, Kozyrskyj, AL. Perinatal programming of asthma: the role of gut microbiota. Clin Dev Immunol. 2012; 2012, 932072.CrossRefGoogle ScholarPubMed
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, 483490.CrossRefGoogle ScholarPubMed
5. Shields, M. Overweight and obesity among children and youth. Health Rep. 2006; 17, 2742.Google ScholarPubMed
6. Serdula, MK, Ivery, D, Coates, RJ, et al. Do obese children become obese adults? A review of the literature. Prev Med. 1993; 22, 167177.CrossRefGoogle ScholarPubMed
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, 10191026.CrossRefGoogle ScholarPubMed
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, 637647.Google Scholar
9. Yogev, Y, Catalano, PM. Pregnancy and obesity. Obstet Gynecol Clin North Am. 2009; 36, 285300.CrossRefGoogle ScholarPubMed
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, 11891195.Google Scholar
11. Poston, L. Gestational weight gain: influences on the long-term health of the child. Curr Opin Clin Nutr Metab Care. 2012; 15, 252257.CrossRefGoogle ScholarPubMed
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, 635683.CrossRefGoogle ScholarPubMed
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, 1571815723.Google Scholar
14. Angelakis, E, Armougom, F, Million, M, Raoult, D. The relationship between gut microbiota and weight gain in humans. Future Microbiol. 2012; 7, 91109.CrossRefGoogle ScholarPubMed
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, 577589.CrossRefGoogle ScholarPubMed
16. Brahe, LK, Astrup, A, Larsen, LH. Is butyrate the link between diet, intestinal microbiota and obesity-related metabolic diseases? Obes Rev. 2013; 14, 950959.Google Scholar
17. Le Chatelier, E, Nielsen, T, Qin, J, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013; 500, 541546.CrossRefGoogle ScholarPubMed
18. Ridaura, VK, Faith, JJ, Rey, FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013; 341, 1241214.Google Scholar
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, 18.CrossRefGoogle ScholarPubMed
20. Koleva, PT, Bridgman, SL, Kozyrskyj, AL. The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients. 2015; 7, 22372260.CrossRefGoogle ScholarPubMed
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, 22572261.Google Scholar
22. Bervoets, L, Van, HK, Kortleven, I, et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog. 2013; 5, 10.Google Scholar
23. Zhang, H, DiBaise, JK, Zuccolo, A, et al. Human gut microbiota in obesity and after gastric bypass. Obesity (Silver Spring). 2010; 18, 190195.Google Scholar
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, 18.Google Scholar
25. Penders, J, Thijs, C, Vink, C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006; 118, 511521.CrossRefGoogle ScholarPubMed
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, 385394.CrossRefGoogle ScholarPubMed
27. Kaplan, JL, Walker, WA. Early gut colonization and subsequent obesity risk. Curr Opin Clin Nutr Metab Care. 2012; 15, 278284.CrossRefGoogle ScholarPubMed
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, 9095.Google Scholar
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.Google Scholar
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, 534538.CrossRefGoogle ScholarPubMed
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, 1625.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
33. Koleva, PT, Bridgman, SL, Kozyrskyj, AL. The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients. 2015; 7, 22372260.CrossRefGoogle ScholarPubMed
34. Eggesbo, M, Moen, B, Peddada, S, et al. Development of gut microbiota in infants not exposed to medical interventions. APMIS. 2011; 119, 1735.Google Scholar
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, 559566.Google Scholar
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, 113123.Google Scholar
37. Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.CrossRefGoogle ScholarPubMed
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, 178184.Google Scholar
39. Jimenez, E, Marin, ML, Martin, R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008; 159, 187193.Google Scholar
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, 198211.CrossRefGoogle ScholarPubMed
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, 771783.CrossRefGoogle ScholarPubMed
42. Brandtzaeg, P. Homeostatic impact of indigenous microbiota and secretory immunity. Benef Microbes. 2010; 1, 211227.CrossRefGoogle ScholarPubMed
43. Mirpuri, J, Raetz, M, Sturge, CR, et al. Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microbes. 2014; 5, 2839.CrossRefGoogle ScholarPubMed
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, 188193.Google Scholar
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, 18421851.Google Scholar
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), 6773.Google Scholar
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.Google Scholar
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, 153158.Google Scholar
49. Patro, B, Liber, A, Zalewski, B, et al. Maternal and paternal body mass index and offspring obesity: a systematic review. Ann Nutr Metab. 2013; 63, 3241.Google Scholar
50. Paliy, O, Piyathilake, CJ, Kozyrskyj, A, et al. Excess body weight during pregnancy and offspring obesity: potential mechanisms. Nutrition. 2014; 30, 245251.Google Scholar
51. Cox, LM, Blaser, MJ. Pathways in microbe-induced obesity. Cell Metab. 2013; 17, 883894.Google Scholar
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, 16.Google Scholar
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, 13861389.Google Scholar
54. Koren, O, Goodrich, JK, Cullender, TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012; 150, 470480.Google Scholar
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, 894899.Google Scholar
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, 8392.Google Scholar
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, 7785.CrossRefGoogle ScholarPubMed
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, 10231030.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 165175.Google Scholar
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.CrossRefGoogle ScholarPubMed
62. Konstantinov, SR, van der Woude, CJ, Peppelenbosch, MP. Do pregnancy-related changes in the microbiome stimulate innate immunity? Trends Mol Med. 2013; 19, 454459.Google Scholar
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, 196204.Google Scholar
64. Cho, CE, Norman, M. Cesarean section and development of the immune system in the offspring. Am J Obstet Gynecol. 2013; 208, 249254.Google Scholar
65. Priyadarshini, M, Thomas, A, Reisetter, AC, et al. Maternal short-chain fatty acids are associated with metabolic parameters in mothers and newborns. Transl Res. 2014; 164, 153157.Google Scholar
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, R1065R1069.Google Scholar
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, 907913.Google Scholar
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.Google Scholar
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), S17S30.Google Scholar
70. Holscher, HD, Faust, KL, Czerkies, LA, et al. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. J Parenter Enteral Nutr. 2012; 36(Suppl.), 95S105S.Google Scholar
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.Google Scholar
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, 395398.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 522529.Google Scholar
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, 12901298.Google Scholar
77. Bailey, LC, Forrest, CB, Zhang, P, et al. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 2014; 168, 10631069.CrossRefGoogle ScholarPubMed
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, 11151119.Google Scholar
79. Trasande, L, Blustein, J, Liu, M, et al. Infant antibiotic exposures and early-life body mass. Int J Obes (Lond). 2013; 37, 1623.Google Scholar
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, 608613.Google Scholar
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, 427436.CrossRefGoogle ScholarPubMed
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, 5359.Google Scholar
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, 14541459.Google Scholar
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.Google Scholar
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, 791801.Google Scholar
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.Google Scholar
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, 7784.Google Scholar
88. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486, 207214.Google Scholar
89. Yatsunenko, T, Rey, FE, Manary, MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486, 222227.Google Scholar
90. Lozupone, CA, Stombaugh, J, Gonzalez, A, et al. Meta-analyses of studies of the human microbiota. Genome Res. 2013; 23, 17041714.Google Scholar
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.Google Scholar