Childhood obesity: A role for gut microbiota?

International Journal of Environmental Research and Public Health

Volumn 12, Issue 1, 2015, Pages 162-175

  Sanchez, Marina ^a   Panahi, Shirin ^a   Tremblay, Angelo ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Body weight; Childhood obesity; Composition; Gut microbiota; Prebiotics; Probiotics

Indexed keywords

CHOLECYSTOKININ; GLUCAGON LIKE PEPTIDE 1; PEPTIDE YY; PREBIOTIC AGENT; PROBIOTIC AGENT; YOGHURT;

CHILD HEALTH; ENVIRONMENTAL FACTOR; HEALTH GEOGRAPHY; HEALTH RISK; HOMEOSTASIS; OBESITY; PROBIOTICS; PUBLIC HEALTH;

BIFIDOBACTERIUM; BODY COMPOSITION; CHILD SAFETY; CHILDHOOD OBESITY; DIET SUPPLEMENTATION; DYSBIOSIS; ENERGY BALANCE; ENVIRONMENTAL FACTOR; FOOD INTAKE; HUMAN; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS AMYLOVORUS; LIPID STORAGE; MICROBIAL COMMUNITY; NONHUMAN; REVIEW; RISK FACTOR; RISK REDUCTION; SATIETY; SYMBIOSIS; THERAPY EFFECT; WEIGHT CONTROL; CALORIC INTAKE; CHILD; GASTROINTESTINAL TRACT; METABOLISM; MICROBIOLOGY; MICROFLORA; OBESITY;

BACTERIA (MICROORGANISMS);

CHILD; ENERGY INTAKE; GASTROINTESTINAL TRACT; HUMANS; MICROBIOTA; OBESITY; PEDIATRIC OBESITY; PREBIOTICS; PROBIOTICS;

EID: 84919795255     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph120100162     Document Type: Review

References (81)

1. Brien, S.E.; Katzmarzyk, P.T. Physical activity and the metabolic syndrome in Canada. Appl. Physiol. Nutr. Metab. 2006, 31, 40-47.
2. Whitaker, R.C.; Wright, J.A.; Pepe, M.S.; Seidel, K.D.; Dietz, W.H. Predicting obesity in young adulthood from childhood and parental obesity. N. Engl. J. Med. 1997, 337, 869-873.
3. Smith, J.D.; Montano, Z.; Dishion, T.J.; Shaw, D.S.; Wilson, M.N. Preventing weight gain and obesity: Indirect effects of the family check-up in early childhood. Prev. Sci. 2014, doi:10.1007/s11121-014-0505-z.
4. Chaput, J.P.; Despres, J.P.; Bouchard, C.; Tremblay, A. Longer sleep duration associates with lower adiposity gain in adult short sleepers. Int. J. Obes. 2012, 36, 752-756.
5. Zemel, M.B.; Thompson, W.; Milstead, A.; Morris, K.; Campbell, P. Calcium and dairy acceleration of weight and fat loss during energy restriction in obese adults. Obes. Res. 2004, 12, 582-590.
6. Chaput, J.P.; Leblanc, C.; Perusse, L.; Despres, J.P.; Bouchard, C.; Tremblay, A. Risk factors for adult overweight and obesity in the quebec family study: Have we been barking up the wrong tree? Obesity 2009, 17, 1964-1970.
7. Bervoets, L.; Van Hoorenbeeck, K.; Kortleven, I.; Van Noten, C.; Hens, N.; Vael, C.; Goossens, H.; Desager, K.N.; Vankerckhoven, V. Differences in gut microbiota composition between obese and lean children: A cross-sectional study. Gut Pathog. 2013, 5, doi:10.1186/1757-4749-5-10.
8. Bouchard, C.; Tremblay, A.; Despres, J.P.; Nadeau, A.; Lupien, P.J.; Theriault, G.; Dussault, J.; Moorjani, S.; Pinault, S.; Fournier, G. The response to long-term overfeeding in identical twins. N. Engl. J. Med. 1990, 322, 1477-1482.
9. Backhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Nat. Acad. Sci. USA 2004, 101, 15718-15723.
10. Backhed, F.; Manchester, J.K.; Semenkovich, C.F.; Gordon, J.I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Nat. Acad. Sci. USA 2007, 104, 979-984.
11. Turnbaugh, P.J.; Gordon, J.I. The core gut microbiome, energy balance and obesity. J. Physiol. 2009, 587, 4153-4158.
12. Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027-1031.
13. Kadooka, Y.; Sato, M.; Imaizumi, K.; Ogawa, A.; Ikuyama, K.; Akai, Y.; Okano, M.; Kagoshima, M.; Tsuchida, T. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur. J. Clin. Nutr. 2010, 64, 636-643.
14. Chang, B.J.; Park, S.U.; Jang, Y.S.; Ko, S.H.; Joo, N.M.; Kim, S.I.; Kim, C.H.; Chang, D.K. Effect of functional yogurt NY-YP901 in improving the trait of metabolic syndrome. Eur. J. Clin. Nutr. 2011, 65, 1250-1255.
15. Omar, J.M.; Chan, Y.-M.; Jones, M.L.; Prakash, S.; Jones, P.J.H. Lactobacillus fermentum and Lactobacillus amylovorus as probiotics alter body adiposity and gut microflora in healthy persons. J. Funct. Foods 2013, 5, 116-123.
16. Zarrati, M.; Salehi, E.; Nourijelyani, K.; Mofid, V.; Zadeh, M.J.; Najafi, F.; Ghaflati, Z.; Bidad, K.; Chamari, M.; Karimi, M.; et al. Effects of probiotic yogurt on fat distribution and gene expression of proinflammatory factors in peripheral blood mononuclear cells in overweight and obese people with or without weight-loss diet. J. Amer. Coll. Nutr. 2014, 33, 417-425.
17. Kang, J.H.; Yun, S.I.; Park, H.O. Effects of Lactobacillus gasseri BNR17 on body weight and adipose tissue mass in diet-induced overweight rats. J. Microbiol. 2010, 48, 712-714.
18. Piche, T.; des Varannes, S.B.; Sacher-Huvelin, S.; Holst, J.J.; Cuber, J.C.; Galmiche, J.P. Colonic fermentation influences lower esophageal sphincter function in gastroesophageal reflux disease. Gastroenterology 2003, 124, 894-902.
19. Cani, P.D.; Bibiloni, R.; Knauf, C.; Waget, A.; Neyrinck, A.M.; Delzenne, N.M.; Burcelin, R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008, 57, 1470-1481.
20. Cani, P.D.; Delzenne, N.M. Interplay between obesity and associated metabolic disorders: New insights into the gut microbiota. Curr. Opin. Pharmacol. 2009, 9, 737-743.
21. Cani, P.D.; Delzenne, N.M. The gut microbiome as therapeutic target. Pharmacol. Ther. 2011, 130, 202-212.
22. Hill, J.O.; Peters, J.C. Environmental contributions to the obesity epidemic. Science 1998, 280, 1371-1374.
23. Delzenne, N.M.; Cani, P.D. Interaction between obesity and the gut microbiota: Relevance in nutrition. Annu. Rev. Nutr. 2011, 31, 15-31.
24. Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022-1023.
25. Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P.; et al. A core gut microbiome in obese and lean twins. Nature 2009, 457, 480-484.
26. Jumpertz, R.; Le, D.; Turnbaugh, P.; Trinidad, C.; Bogardus, C.; Gordon, J.; Krakoff, J. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Amer. J. Clin. Nutr. 2011, 94, 58-65.
27. Vael, C.; Verhulst, S.L.; Nelen, V.; Goossens, H.; Desager, K.N. Intestinal microflora and body mass index during the first three years of life: An observational study. Gut Pathog. 2011, 3, doi:10.1186/1757-4749-3-8.
28. Luoto, R.; Kalliomaki, M.; Laitinen, K.; Delzenne, N.M.; Cani, P.D.; Salminen, S.; Isolauri, E. 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. Hildebrandt, M.A.; Hoffmann, C.; Sherrill-Mix, S.A.; Keilbaugh, S.A.; Hamady, M.; Chen, Y.Y.; Knight, R.; Ahima, R.S.; Bushman, F.; Wu, G.D. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 2009, 137, 1716-1724.
30. Mackie, R.I.; Sghir, A.; Gaskins, H.R. Developmental microbial ecology of the neonatal gastrointestinal tract. Amer. J. Clin. Nutr. 1999, 69, S1035-S1045.
31. Palmer, C.; Bik, E.M.; DiGiulio, D.B.; Relman, D.A.; Brown, P.O. Development of the human infant intestinal microbiota. PLoS Biol. 2007, 5, doi:10.1371/journal.pbio.0050177.
32. Koenig, J.E.; Spor, A.; Scalfone, N.; Fricker, A.D.; Stombaugh, J.; Knight, R.; Angenent, L.T.; Ley, R.E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Nat. Acad. Sci. USA 2011, 108, S4578-S4585.
33. Turnbaugh, P.J.; Backhed, F.; Fulton, L.; Gordon, J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell. Host Microbe 2008, 3, 213-223.
34. Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401-1412.
35. Roberfroid, M. Prebiotics: The concept revisited. J. Nutr. 2007, 137, S830-S837.
36. Geier, M.; Butler, R.; Howarth, G. Inflammatory bowel disease: Current insights into pathogenesis and new therapeutic options: Probiotics, prebiotics and synbiotics. Int. J. Food Microbiol. 2007, 115, 1-11.
37. Hedin, C.; Whelan, K.; Lindsay, J. Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: A review of clinical trials. Proc. Nutr. Soc. 2007, 66, 307-315.
38. Lomax, A.R.; Calder, P.C. Prebiotics, immune function, infection and inflammation: A review of the evidence. Brit. J. Nutr. 2009, 101, 633-658.
39. Yeo, S.K.; Ooi, L.G.; Lim, T.J.; Liong, M.T. Antihypertensive properties of plant-based prebiotics. Int. J. Mol. Sci. 2009, 10, 3517-3530.
40. Flamm, G.; Glinsmann, W.; Kirtchevsky, D.; Prosky, L.; Roberfroid, M. Inulin and oligofructose as dietary fiber: A review of the evidence. Crit. Rev. Food Sci. Nutr. 2001, 41, 353-362.
41. FAO/WHO Working Group. Guidelines for the Evaluation of Probiotics in Food; FAO: London, ON, Canada, 2002.
42. Saraf, K.; Shashikanth, M.; Priy, T.; Sultana, N.; Chaitanya, N. Probiotics-Do they have a role in medicine and dentistry? J. Assoc. Physic. India 2010, 58, 488-490, 495-486.
43. Vanderpool, C.; Yan, F.; Polk, D.B. Mechanisms of probiotic action: Implications for therapeutic applications in inflammatory bowel diseases. Inflamm. Bowel Dis. 2008, 14, 1585-1596.
44. De Vrese, M.; Marteau, P.R. Probiotics and prebiotics: Effects on diarrhea. J. Nutr. 2007, 137, S803-S811.
45. Minocha, A. Probiotics for preventive health. Nutr. Clin. Pract. 2009, 24, 227-241.
46. Azcarate-Peril, M.A.; Sikes, M.; Bruno-Barcena, J.M. The intestinal microbiota, gastrointestinal environment and colorectal cancer: A putative role for probiotics in prevention of colorectal cancer? Amer. J. Physiol. Gastrointest. Liver Physiol. 2011, 301, 401-424.
47. Singh, M.; Ranjan Das, R. Probiotics for allergic respiratory diseases-Putting it into perspective. Pediatr. Allergy Immunol. 2010, 21, 1399-3038.
48. Tang, M.L.; Lahtinen, S.J.; Boyle, R.J. Probiotics and prebiotics: Clinical effects in allergic disease. Curr. Opin. Pediatr. 2010, 22, 626-634.
49. Borchers, A.T.; Selmi, C.; Meyers, F.J.; Keen, C.L.; Gershwin, M.E. Probiotics and immunity. J. Gastroenterol. 2009, 44, 26-46.
50. Desbonnet, L.; Garrett, L.; Clarke, G.; Kiely, B.; Cryan, J.F.; Dinan, T.G. Effects of the probiotic bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010, 170, 1179-1188.
51. Bravo, J.A.; Forsythe, P.; Chew, M.V.; Escaravage, E.; Savignac, H.M.; Dinan, T.G.; Bienenstock, J.; Cryan, J.F. Ingestion of Lactobacillus strain regulates emotional behavior and central gaba receptor expression in a mouse via the vagus nerve. Proc. Nat. Acad. Sci. USA 2011, 108, 16050-16055.
52. Lye, H.S.; Rusul, G.; Liong, M.T. Removal of cholesterol by Lactobacilli via incorporation and conversion to coprostanol. J. Dairy Sci. 2010, 93, 1383-1392.
53. Saxelin, M.; Lassig, A.; Karjalainen, H.; Tynkkynen, S.; Surakka, A.; Vapaatalo, H.; Järvenpää, S.; Korpela, R.; Mutanen, M.; Hatakka, K. Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. Int. J. Food Microbiol. 2010, 144, 293-300.
54. Samuel, B.S.; Shaito, A.; Motoike, T.; Rey, F.E.; Backhed, F.; Manchester, J.K.; Hammer, R.E.; Williams, S.C.; Crowley, J.; Yanagisawa, M.; et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, GPR41. Proc. Nat. Acad. Sci. USA 2008, 105, 16767-16772.
55. Bjursell, M.; Admyre, T.; Göransson, M.; Marley, A.E.; Smith, D.M.; Oscarsson, J.; Bohlooly-Y, M. Improved glucose control and reduced body fat mass in free fatty acid receptor 2-deficient mice fed a high-fat diet. Amer. J. Physiol. Endocrinol. Metab. 2011, 300, 211-220.
56. Parnell, J.A.; Reimer, R.A. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Amer. J. Clin. Nutr. 2009, 89, 1751-1759.
57. Cani, P.D.; Lecourt, E.; Dewulf, E.M.; Sohet, F.M.; Pachikian, B.D.; Naslain, D.; De Backer, F.; Neyrinck, A.M.; Delzenne, N.M. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Amer. J. Clin. Nutr. 2009, 90, 1236-1243.
58. Cani, P.D.; Dewever, C.; Delzenne, N.M. Inulin-type fructans modulate gastrointestinal peptides involved in appetite regulation (glucagon-like peptide-1 and ghrelin) in rats. Brit. J. Nutr. 2004, 92, 521-526.
59. Wettergren, A.; Schjoldager, B.; Mortensen, P.E.; Myhre, J.; Christiansen, J.; Holst, J.J. Truncated GLP-1 (proglucagon 78-107-amide) inhibits gastric and pancreatic functions in man. Dig. Dis. Sci. 1993, 38, 665-673.
60. Delzenne, N.M.; Cani, P.D. Gut microflora is a key player in host energy homeostasis. Med. Sci. 2008, 24, 505-510.
61. Brun, P.; Castagliuolo, I.; Di Leo, V.; Buda, A.; Pinzani, M.; Palu, G.; Martines, D. Increased intestinal permeability in obese mice: New evidence in the pathogenesis of nonalcoholic steatohepatitis. Amer. J. Physiol.-Gastrointest. L. 2007, 292, 518-525.
62. De La Serre, C.B.; Ellis, C.L.; Lee, J.; Hartman, A.L.; Rutledge, J.C.; Raybould, H.E. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Amer. J. Physiol. Gastrointest.-L. 2010, 299, 440-448.
63. Muccioli, G.G.; Naslain, D.; Backhed, F.; Reigstad, C.S.; Lambert, D.M.; Delzenne, N.M.; Cani, P.D. The endocannabinoid system links gut microbiota to adipogenesis. Mol. Syst. Biol. 2010, 6, doi:10.1038/msb.2010.46.
64. Amar, J.; Burcelin, R.; Ruidavets, J.B.; Cani, P.D.; Fauvel, J.; Alessi, M.C.; Chamontin, B.; Ferrieres, J. Energy intake is associated with endotoxemia in apparently healthy men. Amer. J. Clin. Nutr. 2008, 87, 1219-1223.
65. Fried, S.K.; Bunkin, D.A.; Greenberg, A.S. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: Depot difference and regulation by glucocorticoid. J. Clin. Endocrinol. Metab. 1998, 83, 847-850.
66. Caesar, R.; Reigstad, C.S.; Backhed, H.K.; Reinhardt, C.; Ketonen, M.; Lunden, G.O.; Cani, P.D.; Backhed, F. Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 2012, 61, 1701-1707.
67. Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860-867.
68. Shoelson, S.E.; Lee, J.; Goldfine, A.B. Inflammation and insulin resistance. J. Clin. Invest. 2006, 116, 1793-1801.
69. Puigserver, P.; Spiegelman, B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24, 78-90.
70. Ranganath, L.R.; Beety, J.M.; Morgan, L.M.; Wright, J.W.; Howland, R.; Marks, V. Attenuated GLP-1 secretion in obesity: Cause or consequence? Gut 1996, 38, 916-919.
71. Neary, M.T.; Batterham, R.L. Gut hormones: Implications for the treatment of obesity. Pharmacol. Ther. 2009, 124, 44-56.
72. Musso, G.; Gambino, R.; Cassader, M. Gut microbiota as a regulator of energy homeostasis and ectopic fat deposition: Mechanisms and implications for metabolic disorders. Curr. Opin. Lipidol. 2010, 21, 76-83.
73. Cani, P.D.; Possemiers, S.; Van de Wiele, T.; Guiot, Y.; Everard, A.; Rottier, O.; Geurts, L.; Naslain, D.; Neyrinck, A.; Lambert, D.M.; et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 2009, 58, 1091-1103.
74. Delzenne, N.M.; Cani, P.D.; Daubioul, C.; Neyrinck, A.M. Impact of inulin and oligofructose on gastrointestinal peptides. Brit. J. Nutr. 2005, 93, S157-S161.
75. Forssten, S.D.; Korczynska, M.Z.; Zwijsen, R.M.; Noordman, W.H.; Madetoja, M.; Ouwehand, A.C. Changes in satiety hormone concentrations and feed intake in rats in response to lactic acid bacteria. Appetite 2013, 71, 16-21.
76. Ruijschop, R.; Boelrijk, A.; te Giffel, M. Satiety effects of a dairy beverage fermented with propionic acid bacteria. Int. Dairy J. 2008, 8, 945-950.
77. Alisi, A.; Bedogni, G.; Baviera, G.; Giorgio, V.; Porro, E.; Paris, C.; Giammaria, P.; Reali, L.; Anania, F.; Nobili, V. Randomised clinical trial: The beneficial effects of VSL#3 in obese children with non-alcoholic steatohepatitis. Aliment. Pharmacol. Ther. 2014, 39, 1276-1285.
78. Sanchez, M.; Darimont, C.; Drapeau, V.; Emady-Azar, S.; Lepage, M.; Rezzonico, E.; Ngom-Bru, C.; Berger, B.; Philippe, L.; Ammon-Zuffrey, C.; et al. Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Brit. J. Nutr. 2014, 111, 1507-1519.
79. Safavi, M.; Farajian, S.; Kelishadi, R.; Mirlohi, M.; Hashemipour, M. The effects of synbiotic supplementation on some cardio-metabolic risk factors in overweight and obese children: A randomized triple-masked controlled trial. Int. J. Food Sci. Nutr. 2013, 64, 687-693.
80. Kalliomaki, M.; Collado, M.C.; Salminen, S.; Isolauri, E. Early differences in fecal microbiota composition in children may predict overweight. Amer. J. Clin. Nutr. 2008, 87, 534-538.
81. Payne, A.N.; Chassard, C.; Zimmermann, M.; Muller, 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, doi:10.1038/nutd.2011.8.