Does microbiota influence the risk of childhood obesity?
DOI:
https://doi.org/10.14306/renhyd.22.2.389Keywords:
Obesity, Gastrointestinal Microbiome, Pediatric Obesity, Breast Feeding, DysbiosisAbstract
Childhood obesity is associated to incremented risk of developing diseases such as diabetes, cardiovascular diseases, or cancer, later in life. Several factors affect infant weight gain such as genetics, maternal lifestyle, and other environmental factors. Perinatal period is considered to be the most important one to when defining metabolic programming of the future adult. Several previous researches have discussed the role that gut microbiota might play on obesity risk and its development between 3-5 years old. Again, perinatal period is crucial to define quantity and diversity of a healthy intestinal microbiota. Maternal diet/BMI, delivery mode, antibiotic exposure and breastfeeding are some of the processes that will determine a favorable gut microbiota. Functions of gut microbiota, mostly by producing short-chain fatty acids as metabolites, include regulation of metabolism and immune system of the host, which may be compromised in case of dysbiosis. This review pretends to evaluate the state of the art concerning infant obesity and the role of gut microbiota. Despite the large amount of scientific publications, there is still much work to do regarding the clarification of mechanisms and the possible therapy for childhood obesity.References
(1) World Health Organization. Obesity and overweight. Fact Sheet [Internet]. World Health Organization. 2016 [citado 1 de septiembre de 2016]. Disponible en: http://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight
(2) Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384(9945):766-81.
(3) Herrera BM, Keildson S, Lindgren CM. Genetics and epigenetics of obesity. Maturitas. 2011;69(1):41-9.
(4) Katzmarzyk PT, Barlow S, Bouchard C, Catalano PM, Hsia DS, Inge TH, et al. An evolving scientific basis for the prevention and treatment of pediatric obesity. Int J Obes. 2014;38(7):887-905.
(5) Woo Baidal JA, Locks LM, Cheng ER, Blake-Lamb TL, Perkins ME, Taveras EM. Risk Factors for Childhood Obesity in the First 1,000 Days: A Systematic Review. Am J Prev Med. 2016;50(6):761-79.
(6) Albuquerque D, Stice E, Rodríguez-López R, Manco L, Nóbrega C. Current review of genetics of human obesity: from molecular mechanisms to an evolutionary perspective. Mol Genet Genomics. 2015;290(4):1191-221.
(7) Goldstone AP, Beales PL. Genetic obesity syndromes. Front Horm Res. 2008;36:37-60.
(8) Chesi A, Grant SFA. The Genetics of Pediatric Obesity. Trends Endocrinol Metab. 2015;26(12):711-21.
(9) Hinney A, Vogel CIG, Hebebrand J. From monogenic to polygenic obesity: recent advances. Eur Child Adolesc Psychiatry. 2010;19(3):297-310.
(10) Young BE, Johnson SL, Krebs NF. Biological determinants linking infant weight gain and child obesity: current knowledge and future directions. Adv Nutr. 2012;3(5):675-86.
(11) Gillman MW. The first months of life: a critical period for development of obesity. Am J Clin Nutr. 2008;87(6):1587-9.
(12) Thompson AL. Developmental origins of obesity: early feeding environments, infant growth, and the intestinal microbiome. Am J Hum Biol. 2012;24(3):350-60.
(13) Kon IY, Shilina NM, Gmoshinskaya MV, Ivanushkina TA. The study of breast milk IGF-1, leptin, ghrelin and adiponectin levels as possible reasons of high weight gain in breast-fed infants. Ann Nutr Metab. 2014;65(4):317-23.
(14) Brunner S, Schmid D, Zang K, Much D, Knoeferl B, Kratzsch J, et al. Breast milk leptin and adiponectin in relation to infant body composition up to 2 years. Pediatr Obes. 2015;10(1):67-73.
(15) Dewey KG. Growth characteristics of breast-fed compared to formula-fed infants. Biol Neonate. 1998;74(2):94-105.
(16) 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(12):1019-26.
(17) Grunewald M, Hellmuth C, Demmelmair H, Koletzko B. Excessive weight gain during full breast-feeding. Ann Nutr Metab. 2014;64(3-4):271-5.
(18) Fenton TR, Premji SS, Al-Wassia H, Sauve RS. Higher versus lower protein intake in formula-fed low birth weight infants. Cochrane Database Syst Rev. 2014;(4):CD003959.
(19) Castillo-Laura H, Santos IS, Quadros LCM, Matijasevich A. Maternal obesity and offspring body composition by indirect methods: a systematic review and meta-analysis. Cad Saude Publica. 2015;31(10):2073-92.
(20) Ahuja S, Boylan M, Hart SL, Román-Shriver C, Spallholz JE, Pence BC, et al. Glucose and Insulin Levels are Increased in Obese and Overweight Mothers’ Breast-Milk. Food Nutr Sci. 2011;2(3):201-6.
(21) Fleddermann M, Demmelmair H, Grote V, Nikolic T, Trisic B, Koletzko B. Infant formula composition affects energetic efficiency for growth: the BeMIM study, a randomized controlled trial. Clin Nutr. 2014;33(4):588-95.
(22) Weber M, Grote V, Closa-Monasterolo R, Escribano J, Langhendries J-P, Dain E, et al. Lower protein content in infant formula reduces BMI and obesity risk at school age: follow-up of a randomized trial. Am J Clin Nutr. 2014;99(5):1041-51.
(23) Inostroza J, Haschke F, Steenhout P, Grathwohl D, Nelson SE, Ziegler EE. Low-protein formula slows weight gain in infants of overweight mothers. J Pediatr Gastroenterol Nutr. 2014;59(1):70-7.
(24) Oddy WH. Infant feeding and obesity risk in the child. Breastfeed Rev. 2012;20(2):7-12.
(25) Klag EA, McNamara K, Geraghty SR, Keim SA. Associations Between Breast Milk Feeding, Introduction of Solid Foods, and Weight Gain in the First 12 Months of Life. Clin Pediatr. 2015;54(11):1059-67.
(26) Sabin MA, Kiess W. Childhood obesity: Current and novel approaches. Best Pract Res Clin Endocrinol Metab. 2015;29(3):327-38.
(27) Brestoff JR, Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol. 2013;14(7):676-84.
(28) Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148(6):1258-70.
(29) Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242-9.
(30) Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients. 2015;7(4):2839-49.
(31) Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11(10):577-91.
(32) Duboc H, Rajca S, Rainteau D, Benarous D, Maubert M-A, Quervain E, et al. Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut. 2013;62(4):531-9.
(33) Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, et al. Colonization-induced host-gut microbial metabolic interaction. MBio. 2011;2(2):e00271-00210.
(34) Matsumoto M, Kibe R, Ooga T, Aiba Y, Kurihara S, Sawaki E, et al. Impact of intestinal microbiota on intestinal luminal metabolome. Sci Rep. 2012;2:233.
(35) Vighi G, Marcucci F, Sensi L, Di Cara G, Frati F. Allergy and the gastrointestinal system. Clin Exp Immunol. 2008;153(Suppl 1):3-6.
(36) Moloney RD, Desbonnet L, Clarke G, Dinan TG, Cryan JF. The microbiome: stress, health and disease. Mamm Genome. 2014;25(1-2):49-74.
(37) Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci. 2014;15(6):367-78.
(38) Robles-Alonso V, Guarner F. Progreso en el conocimiento de la microbiota intestinal humana. Nutr Hosp. 2013;28(3):553-7.
(39) Gotteland M. El papel de la microbiota intestinal en el desarrollo de la obesidad y de la diabetes de tipo-2. Rev Chil Endocrinol Diabetes. 2013;6(4):155-62.
(40) Verdu EF, Galipeau HJ, Jabri B. Novel players in coeliac disease pathogenesis: role of the gut microbiota. Nat Rev Gastroenterol Hepatol. 2015;12(9):497-506.
(41) Soderborg TK, Borengasser SJ, Barbour LA, Friedman JE. Microbial transmission from mothers with obesity or diabetes to infants: an innovative opportunity to interrupt a vicious cycle. Diabetologia. 2016;59(5):895-906.
(42) Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449(7164):804-10.
(43) Brinkworth GD, Noakes M, Clifton PM, Bird AR. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. Br J Nutr. 2009;101(10):1493-502.
(44) Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062-72.
(45) Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52-60.
(46) Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101(44):15718-23.
(47) Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341(6150):1241214.
(48) Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027-31.
(49) López-Cepero AA, Palacios C. Association of the Intestinal Microbiota and Obesity. P R Health Sci J. 2015;34(2):60-4.
(50) Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TMS, Comelli EM. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes. 2014;4:e121.
(51) Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480-4.
(52) De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell. 2014;156(1-2):84-96.
(53) Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13(5):517-26.
(54) Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S, et al. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res. 2010;51(5):1101-12.
(55) Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, et al. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun. 2014;5:3611.
(56) Zhou J, Martin RJ, Tulley RT, Raggio AM, McCutcheon KL, Shen L, et al. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab. 2008;295(5):E1160-1166.
(57) Cani PD, Lecourt E, Dewulf EM, Sohet FM, Pachikian BD, Naslain D, et al. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am J Clin Nutr. 2009;90(5):1236-43.
(58) Myers MG, Leibel RL, Seeley RJ, Schwartz MW. Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol Metab. 2010;21(11):643-51.
(59) Chan YK, Estaki M, Gibson DL. Clinical consequences of diet-induced dysbiosis. Ann Nutr Metab. 2013;63(Suppl 2):28-40.
(60) Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011;9(4):279-90.
(61) Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J. 2010;4(2):232-41.
(62) Rodríguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050.
(63) Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra65.
(64) Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529(7585):212-5.
(65) 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(4):894-9.
(66) Jašarević E, Rodgers AB, Bale TL. A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment. Neurobiol Stress. 2015;1:81-8.
(67) Zijlmans MAC, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology. 2015;53:233-45.
(68) 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(1):77-85.
(69) Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63(4):559-66.
(70) Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015;17(5):690-703.
(71) Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250-3.
(72) Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, et al. The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res. 2013;69(1):1-10.
(73) Favier CF, Vaughan EE, De Vos WM, Akkermans ADL. Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol. 2002;68(1):219-26.
(74) Perez PF, Doré J, Leclerc M, Levenez F, Benyacoub J, Serrant P, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007;119(3):e724-732.
(75) Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22(9):1147-62.
(76) Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011;108(Suppl 1):4578-85.
(77) Laursen MF, Andersen LBB, Michaelsen KF, Mølgaard C, Trolle E, Bahl MI, et al. Infant Gut Microbiota Development Is Driven by Transition to Family Foods Independent of Maternal Obesity. mSphere. 2016;1(1):00069-15.
(78) Francino MP. Antibiotics and the Human Gut Microbiome: Dysbioses and Accumulation of Resistances. Front Microbiol. 2015;6:1543.
(79) Kumar H, Rautava S, Collado M, Borzykh N, Loyttyniemi E, Isolauri E, et al. Neonatal Antibiotic Exposure Alters Compositional Gut Microbiota Development During the First 6 Months of Life. FASEB J. 2015;29(Suppl. 1):1.
(80) Ege MJ, Mayer M, Normand A-C, Genuneit J, Cookson WOCM, Braun-Fahrländer C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364(8):701-9.
(81) Zhou D. Impact of sanitary living environment on gut microbiota. Precis Med. 2016;2:e1161.
(82) Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, et al. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol. 2013;9(1):15.
(83) Sanchez M, Panahi S, Tremblay A. Childhood obesity: a role for gut microbiota? Int J Environ Res Public Health. 2015;12(1):162-75.
(84) 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(3):178-84.
(85) Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr. 2010;103(12):1792-9.
(86) Gueimonde M, Sakata S, Kalliomäki M, Isolauri E, Benno Y, Salminen S. Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr. 2006;42(2):166-70.
(87) Abdulkadir B, Nelson A, Skeath T, Marrs ECL, Perry JD, Cummings SP, et al. Routine Use of Probiotics in Preterm Infants: Longitudinal Impact on the Microbiome and Metabolome. Neonatology. 2016;109(4):239-47.
(88) Mika A, Fleshner M. Early-life exercise may promote lasting brain and metabolic health through gut bacterial metabolites. Immunol Cell Biol. 2016;94(2):151-7.
(89) Suzuki TA, Worobey M. Geographical variation of human gut microbial composition. Biol Lett. 2014;10(2):20131037.
(90) Karlsson CLJ, Onnerfält J, Xu J, Molin G, Ahrné S, Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity. 2012;20(11):2257-61.
(91) Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, Vael C, et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog. 2013;5(1):10.
(92) Ignacio A, Fernandes MR, Rodrigues V a. A, Groppo FC, Cardoso AL, Avila-Campos MJ, et al. Correlation between body mass index and faecal microbiota from children. Clin Microbiol Infect. 2016;22(3):258.e1-8.
(93) Payne AN, Chassard C, Zimmermann M, Müller P, Stinca S, Lacroix C. The metabolic activity of gut microbiota in obese children is increased compared with normal-weight children and exhibits more exhaustive substrate utilization. Nutr Diabetes. 2011;1:e12.
(94) Luoto R, Kalliomäki M, Laitinen K, Delzenne NM, Cani PD, Salminen S, 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(1):90-5.
(95) 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(1):8.
(96) Scheepers LEJM, Penders J, Mbakwa CA, Thijs C, Mommers M, Arts ICW. The intestinal microbiota composition and weight development in children: the KOALA Birth Cohort Study. Int J Obes. 2015;39(1):16-25.
(97) White RA, Bjørnholt JV, Baird DD, Midtvedt T, Harris JR, Pagano M, et al. Novel developmental analyses identify longitudinal patterns of early gut microbiota that affect infant growth. PLoS Comput Biol. 2013;9(5):e1003042.
(98) Luoto R, Kalliomäki M, Laitinen K, Isolauri E. The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes. 2010;34(10):1531-7.
(99) Kelishadi R, Farajian S, Safavi M, Mirlohi M, Hashemipour M. A randomized triple-masked controlled trial on the effects of synbiotics on inflammation markers in overweight children. J Pediatr. 2014;90(2):161-8.
(100) Nicolucci AC, Hume MP, Martínez I, Mayengbam S, Walter J, Reimer RA. Prebiotics Reduce Body Fat and Alter Intestinal Microbiota in Children Who Are Overweight or With Obesity. Gastroenterology. 2017;153(3):711-22.
(101) Zhang C, Yin A, Li H, Wang R, Wu G, Shen J, et al. Dietary Modulation of Gut Microbiota Contributes to Alleviation of Both Genetic and Simple Obesity in Children. EBioMedicine. 2015;2(8):968-84.
(102) Nadal I, Santacruz A, Marcos A, Warnberg J, Garagorri JM, Garagorri M, et al. Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int J Obes. 2009;33(7):758-67.
(103) Santacruz A, Marcos A, Wärnberg J, Martí A, Martin-Matillas M, Campoy C, et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity. 2009;17(10):1906-15.
(104) Seganfredo FB, Blume CA, Moehlecke M, Giongo A, Casagrande DS, Spolidoro JVN, et al. Weight-loss interventions and gut microbiota changes in overweight and obese patients: a systematic review. Obes Rev. 2017;18(8):832-51.
(105) Dahiya DK, Renuka null, Puniya M, Shandilya UK, Dhewa T, Kumar N, et al. Gut Microbiota Modulation and Its Relationship with Obesity Using Prebiotic Fibers and Probiotics: A Review. Front Microbiol. 2017;8:563.
(106) Li J, Riaz Rajoka MS, Shao D, Jiang C, Jin M, Huang Q, et al. Strategies to increase the efficacy of using gut microbiota for the modulation of obesity. Obes Rev. 2017;18(11):1260-71.
This journal 