Maternal modifiers of the infant gut microbiota: Metabolic consequences

Journal of Endocrinology

Volumn 235, Issue 1, 2017, Pages R1-R12

  Mulligan, Christopher M ^a   Friedman, Jacob E ^a  

^a University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

Metabolism; NAFLD; Neonatal; Obesity; Pregnancy

Indexed keywords

BODY WEIGHT; BREAST MILK; CHRONIC INFLAMMATION; COMMENSAL; DIETARY INTAKE; FEMALE; GESTATIONAL AGE; HEPATITIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; INTESTINE FLORA; LIPID DIET; MATERNAL OBESITY; MICROBIAL COLONIZATION; NEWBORN PERIOD; PRIORITY JOURNAL; PROGENY; PROTEOBACTERIA; REVIEW; ANIMAL; EMBRYOLOGY; INFANT; METABOLIC DISORDER; METABOLISM; MICROBIOLOGY; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT; METABOLIC DISEASES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 85029667943     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-17-0303     Document Type: Review

References (103)

1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J & Versalovic J 2014 The placenta harbors a unique microbiome. Science Translational Medicine 6 237ra265.
2. Agopian VG, Kaldas FM, Hong JC, Whittaker M, Holt C, Rana A, Zarrinpar A, Petrowsky H, Farmer D, Yersiz H, et al. 2012 Liver transplantation for nonalcoholic steatohepatitis: the new epidemic. Annals of Surgery 256 624-633. (doi:10.1097/SLA.0b013e31826b4b7e)
3. Ajslev TA, Andersen CS, Gamborg M, Sorensen TI & Jess T 2011 Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. International Journal of Obesity 35 522-529. (doi:10.1038/ijo.2011.27)
4. Alderete TL, Autran C, Brekke BE, Knight R, Bode L, Goran MI & Fields DA 2015 Associations between human milk oligosaccharides and infant body composition in the first 6 mo of life. American Journal of Clinical Nutrition 102 1381-1388. (doi:10.3945/ajcn.115.115451)
5. Anderson EL, Howe LD, Jones HE, Higgins JP, Lawlor DA & Fraser A 2015 The prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and meta-analysis. PLoS ONE 10 e0140908. (doi:10.1371/journal.pone.0140908)
6. Andreas NJ, Hyde MJ, Gale C, Parkinson JR, Jeffries S, Holmes E & Modi N 2014 Effect of maternal body mass index on hormones in breast milk: a systematic review. PLoS ONE 9 e115043. (doi:10.1371/journal.pone.0115043)
7. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF & Gordon JI 2004 The gut microbiota as an environmental factor that regulates fat storage. PNAS 101 15718-15723. (doi:10.1073/pnas.0407076101
8. Binns C, Lee M & Low WY 2016 The long-term public health benefits of breastfeeding. Asia-Pacific Journal of Public Health 28 7-14. (doi:10.1177/1010539515624964)
9. Biswas SK, Bist P, Dhillon MK, Kajiji T, Del Fresno C, Yamamoto M, Lopez-Collazo E, Akira S & Tergaonkar V 2007 Role for MyD88-independent, TRIF pathway in lipid A/TLR4-induced endotoxin tolerance. Journal of Immunology 179 4083-4092. (doi:10.4049/jimmunol.179.6.4083)
10. Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, Guy CD, Seed PC, Rawls JF, David LA, et al. 2016 The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 63 764-775. (doi:10.1002/hep.28356)
11. Bradley PH & Pollard KS 2017 Proteobacteria explain significant functional variability in the human gut microbiome. Microbiome 5 36. (doi:10.1186/s40168-017-0244-z)
12. Burgess SL, Buonomo E, Carey M, Cowardin C, Naylor C, Noor Z, Wills-Karp M & Petri WA Jr 2014 Bone marrow dendritic cells from mice with an altered microbiota provide interleukin 17A-dependent protection against Entamoeba histolytica colitis. mBio 5 e01817. (doi:10.1128/mBio.02046-14)
13. Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E & Mira A 2012 The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. American Journal of Clinical Nutrition 96 544-551. (doi:10.3945/ajcn.112.037382)
14. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. 2007 Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56 1761-1772. (doi:10.2337/db06-1491)
15. Chu DM, Antony KM, Ma J, Prince AL, Showalter L, Moller M & Aagaard KM 2016 The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Medicine 8 77. (doi:10.1186/s13073-016-0330-z)
16. Collado MC, Isolauri E, Laitinen K & Salminen S 2008 Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. American Journal of Clinical Nutrition 88 894-899.
17. Collado MC, Isolauri E, Laitinen K & Salminen S 2010 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. American Journal of Clinical Nutrition 92 1023-1030. (doi:10.3945/ajcn.2010.29877)
18. Collado MC, Laitinen K, Salminen S & Isolauri E 2012 Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatric Research 72 77-85. (doi:10.1038/pr.2012.42)
19. Collado MC, Rautava S, Aakko J, Isolauri E & Salminen S 2016 Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Scientific Reports 6 23129. (doi:10.1038/srep23129)
20. Coveney AP, Wang W, Kelly J, Liu JH, Blankson S, Wu QD, Redmond HP & Wang JH 2015 Myeloid-related protein 8 induces self-tolerance and cross-tolerance to bacterial infection via TLR4- and TLR2-mediated signal pathways. Scientific Reports 5 13694. (doi:10.1038/srep13694)
21. De Leoz ML, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, Mills DA & Lebrilla CB 2015 Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. Journal of Proteome Research 14 491-502. (doi:10.1021/pr500759e)
22. Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Praticò G, Capuani G, Masotti A, Reddel S, Russo A, et al. 2015 Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PLoS ONE 10 e0137347. (doi:10.1371/journal.pone.0137347)
23. Deputy NP, Sharma AJ, Kim SY & Hinkle SN 2015 Prevalence and characteristics associated with gestational weight gain adequacy. Obstetrics and Gynecology 125 773-781. (doi:10.1097/AOG.0000000000000739)
24. Deriu E, Liu JZ, Pezeshki M, Edwards RA, Ochoa RJ, Contreras H, Libby SJ, Fang FC & Raffatellu M 2013 Probiotic bacteria reduce salmonella typhimurium intestinal colonization by competing for iron. Cell Host and Microbe 14 26-37. (doi:10.1016/j.chom.2013.06.007)
25. Dieterich CM, Felice JP, O'Sullivan E & Rasmussen KM 2013 Breastfeeding and health outcomes for the mother-infant dyad. Pediatric Clinics of North America 60 31-48. (doi:10.1016/j.pcl.2012.09.010)
26. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N & Knight R 2010 Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. PNAS 107 11971-11975. (doi:10.1073/pnas.1002601107)
27. Dosch NC, Guslits EF, Weber MB, Murray SE, Ha B, Coe CL, Auger AP & Kling PJ 2016 Maternal obesity affects inflammatory and iron indices in umbilical cord blood. Journal of Pediatrics 172 20-28. (doi:10.1016/j.jpeds.2016.02.023)
28. Drakesmith H & Prentice AM 2012 Hepcidin and the iron-infection axis. Science 338 768-772. (doi:10.1126/science.1224577)
29. Eggesbø M, Moen B, Peddada S, Baird D, Rugtveit J, Midtvedt T, Bushel PR, Sekelja M & Rudi K 2011 Development of gut microbiota in infants not exposed to medical interventions. APMIS 119 17-35. (doi:10.1111/j.1600-0463.2010.02688.x)
30. Ellermann M & Arthur JC 2017 Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radical Biology and Medicine 105 68-78. (doi:10.1016/j.freeradbiomed.2016.10.489)
31. Erridge C, Attina T, Spickett CM & Webb DJ 2007a A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. American Journal of Clinical Nutrition 86 1286-1292.
32. Erridge C, Spickett CM & Webb DJ 2007b Non-enterobacterial endotoxins stimulate human coronary artery but not venous endothelial cell activation via Toll-like receptor 2. Cardiovascular Research 73 181-189. (doi:10.1016/j.cardiores.2006.11.004)
33. Erroi A, Fantuzzi G, Mengozzi M, Sironi M, Orencole SF, Clark BD, Dinarello CA, Isetta A, Gnocchi P & Giovarelli M 1993 Differential regulation of cytokine production in lipopolysaccharide tolerance in mice. Infection and Immunity 61 4356-4359.
34. Everts B, Amiel E, Huang SC, Smith AM, Chang CH, Lam WY, Redmann V, Freitas TC, Blagih J, van der Windt GJ, et al. 2014 TLR-driven early glycolytic reprogramming via the kinases TBK1-IKK? supports the anabolic demands of dendritic cell activation. Nature Immunology 15 323-332. (doi:10.1038/ni.2833)
35. Fensterheim BA, Guo Y, Sherwood ER & Bohannon JK 2017 The cytokine response to lipopolysaccharide does not predict the host response to infection. Journal of Immunology 198 3264-3273. (doi:10.4049/jimmunol.1602106)
36. Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S & Christian LM 2014 Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS ONE 9 e113026. (doi:10.1371/journal.pone.0113026)
37. Ghanim H, Abuaysheh S, Sia CL, Korzeniewski K, Chaudhuri A, Fernandez-Real JM & Dandona P 2009 Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care 32 2281-2287. (doi:10.2337/dc09-0979)
38. Ghanim H, Sia CL, Upadhyay M, Korzeniewski K, Viswanathan P, Abuaysheh S, Mohanty P & Dandona P 2010 Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression. American Journal of Clinical Nutrition 91 940-949. (doi:10.3945/ajcn.2009.28584)
39. Giusti L, Gabriele M, Penno G, Garofolo M, Longo V, Del Prato S, Lucchesi D & Pucci L 2017 A fermented whole grain prevents lipopolysaccharides-induced dysfunction in human endothelial progenitor cells. Oxidative Medicine and Cellular Longevity 2017 1026268.
40. Gomez de Agüero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, et al. 2016 The maternal microbiota drives early postnatal innate immune development. Science 351 1296-1302. (doi:10.1126/science.aad2571)
41. Granowitz EV, Porat R, Mier JW, Orencole SF, Kaplanski G, Lynch EA, Ye K, Vannier E, Wolff SM & Dinarello CA 1993 Intravenous endotoxin suppresses the cytokine response of peripheral blood mononuclear cells of healthy humans. Journal of Immunology 151 1637-1645.
42. Grönlund MM, Arvilommi H, Kero P, Lehtonen OP & Isolauri E 2000 Importance of intestinal colonisation in the maturation of humoral immunity in early infancy: a prospective follow up study of healthy infants aged 0-6 months. Archives of Disease in Childhood 83 F186-F192. (doi:10.1136/fn.83.3.f186)
43. Heikkilä MP & Saris PE 2003 Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. Journal of Applied Microbiology 95 471-478. (doi:10.1046/j.1365-2672.2003.02002.x)
44. Hill CJ, Lynch DB, Murphy K, Ulaszewska M, Jeffery IB, O'Shea CA, Watkins C, Dempsey E, Mattivi F, Touhy K, et al. 2017 Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome 5 4. (doi:10.1186/s40168-016-0213-y)
45. Hooper LV, Xu J, Falk PG, Midtvedt T & Gordon JI 1999 A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. PNAS 96 9833-9838. (doi:10.1073/pnas.96.17.9833)
46. Ip S, Chung M, Raman G, Trikalinos TA & Lau J 2009 A summary of the Agency for Healthcare Research and Quality's evidence report on breastfeeding in developed countries. Breastfeeding Medicine 4 1 S17-S30. (doi:10.1089/bfm.2009.0050)
47. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, Björkstén B, Engstrand L & Andersson AF 2014 Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63 559-566. (doi:10.1136/gutjnl-2012-303249)
48. Jantscher-Krenn E, Lauwaet T, Bliss LA, Reed SL, Gillin FD & Bode L 2012 Human milk oligosaccharides reduce Entamoeba histolytica attachment and cytotoxicity in vitro. British Journal of Nutrition 108 1839-1846. (doi:10.1017/S0007114511007392)
49. Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J, Fernandez L & Rodriguez JM 2008 Is meconium from healthy newborns actually sterile? Research in Microbiology 159 187-193. (doi:10.1016/j.resmic.2007.12.007)
50. Jones AD, Zhao G, Jiang YP, Zhou M, Xu G, Kaciroti N, Zhang Z & Lozoff B 2016 Maternal obesity during pregnancy is negatively associated with maternal and neonatal iron status. European Journal of Clinical Nutrition 70 918-924. (doi:10.1038/ejcn.2015.229)
51. Kamada N, Chen GY, Inohara N & Núñez G 2013 Control of pathogens and pathobionts by the gut microbiota. Nature Immunology 14 685-690. (doi:10.1038/ni.2608)
52. Kelly B & O'Neill LA 2015 Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Research 25 771-784. (doi:10.1038/cr.2015.68)
53. Koch MA, Reiner GL, Lugo KA, Kreuk LS, Stanbery AG, Ansaldo E, Seher TD, Ludington WB & Barton GM 2016 Maternal IgG and IgA antibodies dampen mucosal T helper cell responses in early life. Cell 165 827-841. (doi:10.1016/j.cell.2016.04.055)
54. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, et al. 2012 Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150 470-480. (doi:10.1016/j.cell.2012.07.008)
55. Kramer CD & Genco CA 2017 Microbiota, immune subversion, and chronic inflammation. Frontiers in Immunology 8 255.
56. Lassenius MI, Pietiläinen KH, Kaartinen K, Pussinen PJ, Syrjanen J, Forsblom C, Pörsti I, Rissanen A, Kaprio J, Mustonen J, et al. 2011 Bacterial endotoxin activity in human serum is associated with dyslipidemia, insulin resistance, obesity, and chronic inflammation. Diabetes Care 34 1809-1815. (doi:10.2337/dc10-2197)
57. Latuga MS, Stuebe A & Seed PC 2014 A review of the source and function of microbiota in breast milk. Seminars in Reproductive Medicine 32 68-73. (doi:10.1055/s-0033-1361824)
58. Laugerette F, Vors C, Géloën A, Chauvin MA, Soulage C, Lambert-Porcheron S, Peretti N, Alligier M, Burcelin R, Laville M, et al. 2011 Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation. Journal of Nutritional Biochemistry 22 53-59. (doi:10.1016/j.jnutbio.2009.11.011)
59. Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, et al. 2013 Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62 1787-1794. (doi:10.1136/gutjnl-2012-303816)
60. Leatham-Jensen MP, Frimodt-Møller J, Adediran J, Mokszycki ME, Banner ME, Caughron JE, Krogfelt KA, Conway T & Cohen PS 2012 The streptomycin-treated mouse intestine selects Escherichia coli envZ missense mutants that interact with dense and diverse intestinal microbiota. Infection and Immunity 80 1716-1727. (doi:10.1128/IAI.06193-11)
61. Lemas DJ, Young BE, Baker PR II, Tomczik AC, Soderborg TK, Hernandez TL, de la Houssaye BA, Robertson CE, Rudolph MC, Ir D, et al. 2016 Alterations in human milk leptin and insulin are associated with early changes in the infant intestinal microbiome. American Journal of Clinical Nutrition 103 1291-1300. (doi:10.3945/ajcn.115.126375)
62. Luo Y, Chen GL, Hannemann N, Ipseiz N, Krönke G, Bäuerle T, Munos L, Wirtz S, Schett G & Bozec A 2015 Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metabolism 22 886-894. (doi:10.1016/j.cmet.2015.08.020)
63. Ma J, Prince AL, Bader D, Hu M, Ganu R, Baquero K, Blundell P, Harris RA, Frias AE, Grove KL, et al. 2014 High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nature Communications 5 3889.
64. Martín R, Heilig HG, Zoetendal EG, Jimenez E, Fernandez L, Smidt H & Rodriguez JM 2007 Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Research in Microbiology 158 31-37. (doi:10.1016/j.resmic.2006.11.004)
65. McCurdy CE, Bishop JM, Williams SM, Grayson BE, Smith MS, Friedman JE & Grove KL 2009 Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. Journal of Clinical Investigation 119 323-335.
66. Medzhitov R 2001 Toll-like receptors and innate immunity. Nature Reviews Immunology 1 135-145. (doi:10.1038/35100529)
67. Mirpuri J, Raetz M, Sturge CR, Wilhelm CL, Benson A, Savani RC, Hooper LV & Yarovinsky F 2014 Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microbes 5 28-39. (doi:10.4161/gmic.26489)
68. Miskinyte M & Gordo I 2013 Increased survival of antibiotic-resistant Escherichia coli inside macrophages. Antimicrobial Agents and Chemotherapy 57 189-195. (doi:10.1128/AAC.01632-12)
69. Moya A & Ferrer M 2016 Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends in Microbiology 24 402-413. (doi:10.1016/j.tim.2016.02.002)
70. Mueller NT, Shin H, Pizoni A, Werlang IC, Matte U, Goldani MZ, Goldani HA & Dominguez-Bello MG 2016 Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Scientific Reports 6 23133. (doi:10.1038/srep23133)
71. Myles IA, Fontecilla NM, Janelsins BM, Vithayathil PJ, Segre JA & Datta SK 2013 Parental dietary fat intake alters offspring microbiome and immunity. Journal of Immunology 191 3200-3209. (doi:10.4049/jimmunol.1301057)
72. Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK & Ganz T 2004a IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. Journal of Clinical Investigation 113 1271-1276. (doi:10.1172/JCI200420945)
73. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T & Kaplan J 2004b Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306 2090-2093. (doi:10.1126/science.1104742)
74. Neu J 2015 Preterm infant nutrition, gut bacteria, and necrotizing enterocolitis. Current Opinion in Clinical Nutrition and Metabolic Care 18 285-288. (doi:10.1097/MCO.0000000000000169)
75. Neu J 2016 Intestinal microbiota studies in preterm infants. Journal of Pediatric Gastroenterology and Nutrition 62 193-194. (doi:10.1097/MPG.0000000000001068)
76. Newton KP, Feldman HS, Chambers CD, Wilson L, Behling C, Clark JM, Molleston JP, Chalasani N, Sanyal AJ, Fishbein MH, et al. 2017 Low and high birth weights are risk factors for nonalcoholic fatty liver disease in children. Journal of Pediatrics (doi:10.1016/j.jpeds.2017.1003.1007)
77. Ng RL, Scott NM, Strickland DH, Gorman S, Grimbaldeston MA, Norval M, Waithman J & Hart PH 2013 Altered immunity and dendritic cell activity in the periphery of mice after long-term engraftment with bone marrow from ultraviolet-irradiated mice. Journal of Immunology 190 5471-5484. (doi:10.4049/jimmunol.1202786)
78. Nicklas JM & Barbour LA 2015 Optimizing weight for maternal and infant health - tenable, or too late? Expert Review of Endocrinology and Metabolism 10 227-242. (doi:10.1586/17446651.2014.991102)
79. Ninonuevo MR, Park Y, Yin H, Zhang J, Ward RE, Clowers BH, German JB, Freeman SL, Killeen K, Grimm R, et al. 2006 A strategy for annotating the human milk glycome. Journal of Agricultural and Food Chemistry 54 7471-7480. (doi:10.1021/jf0615810)
80. Ogden CL, Carroll MD, Kit BK & Flegal KM 2012 Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010. JAMA 307 483-490. (doi:10.1001/jama.2012.40)
81. Ogra PL & Welliver RC Sr 2008 Effects of early environment on mucosal immunologic homeostasis, subsequent immune responses and disease outcome. Nestlé Nutrition Workshop Series Paediatric Programme 61 145-181. (doi:10.1159/000113492)
82. Palmer C, Bik EM, DiGiulio DB, Relman DA & Brown PO 2007 Development of the human infant intestinal microbiota. PLoS Biology 5 e177. (doi:10.1371/journal.pbio.0050177)
83. Paul HA, Bomhof MR, Vogel HJ & Reimer RA 2016 Diet-induced changes in maternal gut microbiota and metabolomic profiles influence programming of offspring obesity risk in rats. Scientific Reports 6 20683. (doi:10.1038/srep20683)
84. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA & Stobberingh EE 2006 Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118 511-521. (doi:10.1542/peds.2005-2824)
85. Perez-Muñoz ME, Arrieta MC, Ramer-Tait AE & Walter J 2017 A critical assessment of the 'sterile womb' and 'in utero colonization' hypotheses: implications for research on the pioneer infant microbiome. Microbiome 5 48.
86. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. 2013 Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341 1241214. (doi:10.1126/science.1241214)
87. Rodríguez JM 2014 The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation? Advances in Nutrition 5 779-784. (doi:10.3945/an.114.007229)
88. Ruiz AG, Casafont F, Crespo J, Cayón A, Mayorga M, Estebanez A, Fernadez-Escalante JC & Pons-Romero F 2007 Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients: evidence for the potential role of endotoxin in the pathogenesis of non-alcoholic steatohepatitis. Obesity Surgery 17 1374-1380. (doi:10.1007/s11695-007-9243-7)
89. Santacruz A, Collado MC, García-Valdés L, Segura MT, Martín-Lagos JA, Anjos T, Martí-Romero M, Lopez RM, Florido J, Campoy C, et al. 2010 Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. British Journal of Nutrition 104 83-92. (doi:10.1017/S0007114510000176)
90. Singer K, DelProposto J, Morris DL, Zamarron B, Mergian T, Maley N, Cho KW, Geletka L, Subbaiah P, Muir L, et al. 2014 Diet-induced obesity promotes myelopoiesis in hematopoietic stem cells. Molecular Metabolism 3 664-675. (doi:10.1016/j.molmet.2014.06.005)
91. Slocum C, Coats SR, Hua N, Kramer C, Papadopoulos G, Weinberg EO, Gudino CV, Hamilton JA, Darveau RP & Genco CA 2014 Distinct lipid a moieties contribute to pathogen-induced site-specific vascular inflammation. PLoS Pathogens 10 e1004215. (doi:10.1371/journal.ppat.1004215)
92. Spencer MD, Hamp TJ, Reid RW, Fischer LM, Zeisel SH & Fodor AA 2011 Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology 140 976-986. (doi:10.1053/j.gastro.2010.11.049)
93. Sze MA & Schloss PD 2016 Looking for a signal in the noise: revisiting obesity and the microbiome. mBio 7 e01018-16. (doi:10.1128/mbio.01018-16)
94. Tang M, Frank DN, Sherlock L, Ir D, Robertson CE & Krebs NF 2016 Effect of vitamin E with therapeutic iron supplementation on iron repletion and gut microbiome in US iron deficient infants and toddlers. Journal of Pediatric Gastroenterology and Nutrition 63 379-385. (doi:10.1097/MPG.0000000000001154)
95. Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP, Loukov D, Schenck LP, Jury J, Foley KP, et al. 2017 Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host and Microbe 21 455-466.e454. (doi:10.1016/j.chom.2017.03.002)
96. Thorn SR, Baquero KC, Newsom SA, El Kasmi KC, Bergman BC, Shulman GI, Grove KL & Friedman JE 2014 Early life exposure to maternal insulin resistance has persistent effects on hepatic NAFLD in juvenile nonhuman primates. Diabetes 63 2702-2713. (doi:10.2337/db14-0276)
97. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER & Gordon JI 2006 An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 1027-1031. (doi:10.1038/nature05414)
98. Vatanen T, Kostic AD, d'Hennezel E, Siljand er H, Franzosa EA, Yassour M, Kolde R, Vlamakis H, Arthur TD, Hämäläinen AM, et al. 2016 Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165 842-853. (doi:10.1016/j.cell.2016.04.007)
99. Voreades N, Kozil A & Weir TL 2014 Diet and the development of the human intestinal microbiome. Frontiers in Microbiology 5 1-9.
100. Weng M & Walker WA 2013 The role of gut microbiota in programming the immune phenotype. Journal of Developmental Origins of Health and Disease 4 203-214. (doi:10.1017/S2040174412000712)
101. Wesolowski SR, El Kasmi KC, Jonscher KR & Friedman JE 2017 Developmental origins of NAFLD: a womb with a clue. Nature Reviews: Gastroenterology and Hepatology 14 81-96. (doi:10.1038/nrgastro.2016.160)
102. Whitfield C & Trent MS 2014 Biosynthesis and export of bacterial lipopolysaccharides. Annual Review of Biochemistry 83 99-128. (doi:10.1146/annurev-biochem-060713-035600)
103. Zeng MY, Cisalpino D, Varadarajan S, Hellman J, Warren HS, Cascalho M, Inohara N & Núñez G 2016 Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44 647-658. (doi:10.1016/j.immuni.2016.02.006)