The infant gut microbiome: Evidence for obesity risk and dietary intervention

Nutrients

Volumn 7, Issue 4, 2015, Pages 2237-2260

  Koleva, Petya T ^a   Bridgman, Sarah L ^a   Kozyrskyj, Anita L ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Atopy; Human milk; Infant; Microbiome; Nutrition; Overweight; Prebiotics; Probiotics

Indexed keywords

C REACTIVE PROTEIN; PROBIOTIC AGENT; PREBIOTIC AGENT;

BODY MASS; BREAST MILK; CHILD; CHILDHOOD OBESITY; CLINICAL ASSESSMENT; DIET RESTRICTION; DIETARY INTAKE; EVIDENCE BASED PRACTICE; GENETIC ANALYSIS; HUMAN; INFANT; INTERVENTION STUDY; INTESTINE FLORA; LIFESTYLE; PUBLIC HEALTH; QUANTITATIVE ASSAY; REVIEW; RISK FACTOR; WEIGHT GAIN; ARTIFICIAL MILK; BACTEROIDES; CHEMISTRY; DIET; GASTROINTESTINAL TRACT; LACTOBACILLUS; MICROBIOLOGY; OVERWEIGHT; PEDIATRIC OBESITY;

ANIMALIA; BACTEROIDES; LACTOBACILLUS;

BACTEROIDES; DIET; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; INFANT; INFANT FORMULA; LACTOBACILLUS; MILK, HUMAN; OVERWEIGHT; PEDIATRIC OBESITY; PREBIOTICS; PROBIOTICS; RISK FACTORS;

EID: 84927939405     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7042237     Document Type: Review

References (110)

1. De Onis, M.; Blossner, M.; Borghi, E. Global prevalence and trends of overweight and obesity among preschool children. Am. J. Clin. Nutr. 2010, 92, 1257-1264.
2. Biro, F.M.; Wien, M. Childhood obesity and adult morbidities. Am. J. Clin. Nutr. 2010, 91, 1499S-1505S.
3. 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. Natl. Acad. Sci. USA 2004, 101, 15718-15723.
4. 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.
5. 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.
6. Azad, M.B.; Konya, T.; Maughan, H.; Guttman, D.S.; Field, C.J.; Chari, R.S.; Sears, M.R.; Becker, A.B.; Scott, J.A.; Kozyrskyj, A.L. Gut microbiota of healthy Canadian infants: Profiles by mode of delivery and infant diet at 4 months. CMAJ 2013, 185, 385-394.
7. 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. Natl. Acad. Sci. USA 2011, 108, 4578-4585.
8. Penders, J.; Thijs, C.; Vink, C.; Stelma, F.F.; Snijders, B.; Kummeling, I.; van den Brandt, P.A.; Stobberingh, E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006, 118, 511-521.
9. Ley, R.E.; Backhed, F.; Turnbaugh, P.; Lozupone, C.A.; Knight, R.D.; Gordon, J.I. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 2005, 102, 11070-11075.
10. 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.
11. Fleissner, C.K.; Huebel, N.; Abd El-Bary, M.M.; Loh, G.; Klaus, S.; Blaut, M. Absence of intestinal microbiota does not protect mice from diet-induced obesity. Br. J. Nutr. 2010, 104, 919-929.
12. Turnbaugh, P.J.; Ridaura, V.K.; Faith, J.J.; Rey, F.E.; Knight, R.; Gordon, J.I. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009, 1, doi:10.1126/scitranslmed.3000322.
13. Waldram, A.; Holmes, E.; Wang, Y.; Rantalainen, M.; Wilson, I.D.; Tuohy, K.M.; McCartney, A.L.; Gibson, G.R.; Nicholson, J.K. Top-down systems biology modeling of host metabotype-microbiome associations in obese rodents. J. Proteome Res. 2009, 8, 2361-2375.
14. Cani, P.D.; Amar, J.; Iglesias, M.A.; Poggi, M.; Knauf, C.; Bastelica, D.; Neyrinck, A.M.; Fava, F.; Tuohy, K.M.; Chabo, C.; et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761-1772.
15. Murphy, E.F.; Cotter, P.D.; Healy, S.; Marques, T.M.; O'Sullivan, O.; Fouhy, F.; Clarke, S.F.; O'Toole, P.W.; Quigley, E.M.; Stanton, C.; et al. Composition and energy harvesting capacity of the gut microbiota: Relationship to diet, obesity and time in mouse models. Gut 2010, 59, 1635-1642.
16. Nguyen, T.L.A.; Vieira-Silva, S.; Liston, A.; Raes, J. How informative is the mouse for human gut microbiota research? Disease Models Mech. 2014, 8, 1-16.
17. Kararli, T. Comparison of the gastrointestinal anatomy, physiology and biochemistry of humans and commonly used laboratory animals. Biopharm. Drug Dispos. 1995, 16, 351-380.
18. Walter, J. Ecological role of lactobacilli in the gastrointestinal tract: Implications for fundamental and biomedical research. Appl. Environ. Microbiol. 2008, 74, 4985-4996.
19. Eckburg, P.B.; Bik, E.M.; Bernstein, C.N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S.R.; Nelson, K.E.; Relman, D.A. Diversity of the human intestinal microbial flora. Science 2005, 308, 1635-1638.
20. Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Microbial ecology: Human gut microbes associated with obesity. Nature 2006, 444, 1022-1023.
21. Angelakis, E.; Armougom, F.; Million, M.; Raoult, D. The relationship between gut microbiota and weight gain in humans. Future Microbiol. 2012, 7, 91-109.
22. 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.
23. Million, M.; Maraninchi, M.; Henry, M.; Armougom, F.; Richet, H.; Carrieri, P.; Valero, R.; Raccah, D.; Vialettes, B.; Raoult, D. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes. 2012, 36, 817-825.
24. Million, M.; Angelakis, E.; Maraninchi, M.; Henry, M.; Giorgi, R.; Valero, R.; Vialettes, B.; Raoult, D. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. (Lond.) 2013, 37, 1460-1466.
25. Guarner, F.; Malagelada, J.R. Gut flora in health and disease. Lancet 2003, 361, 512-519.
26. Hakala, P.; Rissanen, A.; Koskenvuo, M.; Kaprio, J.; Ronnemaa, T. Environmental factors in the development of obesity in identical twins. Int. J. Obes. Relat. Metab. Disord. 1999, 23, 746-753.
27. Rissanen, A.; Hakala, P.; Lissner, L.; Mattlar, C.E.; Koskenvuo, M.; Ronnemaa, T. Acquired preference especially for dietary fat and obesity: A study of weight-discordant monozygotic twin pairs. Int. J. Obes. Relat. Metab. Disord. 2002, 26, 973-977.
28. Duncan, S.H.; Lobley, G.E.; Holtrop, G.; Ince, J.; Johnstone, A.M.; Louis, P.; Flint, H.J. Human colonic microbiota associated with diet, obesity and weight loss. Int. J. Obes. (Lond.) 2008, 32, 1720-1724.
29. Schwiertz, A.; Taras, D.; Schafer, K.; Beijer, S.; Bos, N.A.; Donus, C.; Hardt, P.D. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 2010, 18, 190-195.
30. Zhang, H.; DiBaise, J.K.; Zuccolo, A.; Kudrna, D.; Braidotti, M.; Yu, Y.; Parameswaran, P.; Crowell, M.D.; Wing, R.; Rittmann, B.E.; et al. Human gut microbiota in obesity and after gastric bypass. Obesity 2010, 18, 190-195.
31. Santacruz, A.; Collado, M.C.; Garcia-Valdes, L.; Segura, M.T.; Martin-Lagos, J.A.; Anjos, T.; Marti-Romero, M.; Lopez, R.M.; Florido, J.; Campoy, C.; 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.
32. Collado, M.C.; 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.
33. Karlsson, C.L.; Onnerfalt, J.; Xu, J.; Molin, G.; Ahrne, S.; Thorngren-Jerneck, K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 2012, 20, 2257-2261.
34. Bervoets, L.; van, H.K.; Kortleven, I.; van, N.C.; Hens, N.; Vael, C.; Goossens, H.; Desager, K.N.; Vankerckoven, V. Differences in gut microbiota composition between obese and lean children: A cross-sectional study. Gut Pathog. 2013, 5, 1-10.
35. Eggesbo, M.; Moen, B.; Peddada, S.; Baird, D.; Rugtveit, J.; Midtvedt, T.; Bushel, P.R.; Sekelja, M.; Rudi, K. Development of gut microbiota in infants not exposed to medical interventions. APMIS 2011, 119, 17-35.
36. Jakobsson, H.E.; Abrahamsson, T.R.; Jenmalm, M.C.; Harris, K.; Quince, C.; Jernberg, C.; Bjorksten, B.; Engstrand, L.; Andersson, A.F. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 2014, 63, 559-566.
37. Kalliomaki, M.; Collado, M.C.; Salminen, S.; Isolauri, E. Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 2008, 87, 534-538.
38. 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.
39. Kalliomaki, M.; Salminen, S.; Arvilommi, H.; Kero, P.; Koskinen, P.; Isolauri, E. Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. Lancet 2001, 357, 1076-1079.
40. 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, 8, doi:10.1186/1757-4749-3-8.
41. White, R.A.; Bjornholt, J.V.; Baird, D.D.; Midtvedt, T.; Harris, J.R.; Pagano, M.; Hide, W.; Rudi, K.; Moen, B.; Iszatt, N.; et al. Novel developmental analyses identify longitudinal patterns of early gut microbiota that affect infant growth. PLoS Comput. Biol. 2013, 9, e1003042, doi:10.1371/ journal.pcbi.1003042.
42. Scheepers, L.E.; Penders, J.; Mbakwa, C.A.; Thijs, C.; Mommers, M.; Arts, I.C. The intestinal microbiota composition and weight development in children: The KOALA Birth Cohort Study. Int. J. Obes. (Lond.) 2014, 39,16-25.
43. Ajslev, T.A.; Andersen, C.S.; Gamborg, M.; Sorensen, T.I.; 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.
44. Azad, M.B.; Bridgman, S.L.; Becker, A.B.; Kozyrskyj, A.L. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int. J. Obes. (Lond.) 2014, 38, 1290-1298.
45. Bailey, L.C.; Forrest, C.B.; Zhang, P.; Richards, T.M.; Livshits, A.; DeRusso, P.A. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 2014, 168, 1063-1069.
46. Murphy, R.; Stewart, A.W.; Braithwaite, I.; Beasley, R.; Hancox, R.J.; Mitchell, E.A. Antibiotic treatment during infancy and increased body mass index in boys: An international cross-sectional study. Int. J. Obes. (Lond.) 2014, 38, 1115-1119.
47. Trasande, L.; Blustein, J.; Liu, M.; Corwin, E.; Cox, L.M.; Blaser, M.J. Infant antibiotic exposures and early-life body mass. Int. J. Obes. (Lond.) 2013, 37, 16-23.
48. Backhed, F.; Manchester, J.K.; Semenkovich, C.F.; Gordon, J.I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. USA 2007, 104, 979-984.
49. Ridaura, V.K.; Faith, J.J.; Rey, F.E.; Cheng, J.; Duncan, A.E.; Kau, A.L.; Griffin, N.W.; Lombard, V.; Henrissat, B.; Bain, J.R.; et al. Culture gut microbiota from twins discordant for obesity modulate adiposity and metabolic phenotypes in mice. Science 2013, 341, 1-22.
50. Hirasawa, A.; Hara, T.; Katsuma, S.; Adachi, T.; Tsujimoto, G. Free fatty acid receptors and drug discovery. Biol. Pharm. Bull. 2008, 31, 1847-1851.
51. Karaki, S.; Tazoe, H.; Hayashi, H.; Kashiwabara, H.; Tooyama, K.; Suzuki, Y.; Kuwahara, A. Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J. Mol. Histol. 2008, 39, 135-142.
52. Tazoe, H.; Otomo, Y.; Karaki, S.; Kato, I.; Fukami, Y.; Terasaki, M.; Kuwahara, A. Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed. Res. 2009, 30, 149-156.
53. Jumpertz, R.; Le, D.S.; Turnbaugh, P.J.; Trinidad, C.; Bogardus, C.; Gordon, J.I.; Krakoff, J. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 2011, 94, 58-65.
54. Payne, A.N.; Chassard, C.; Zimmermann, M.; Muler, P.; Stinca, S.; Lacroix, C. 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.
55. Cherbut, C.; Ferrier, L.; Roze, C.; Anini, Y.; Blottiere, H.; Lecannu, G.; Galmiche, J.P. Short-chain fatty acids modify colonic motility through nerves and polypeptide YY release in the rat. Am. J. Physiol. 1998, 275, G1415-G1422.
56. Freeland, K.R.; Wolever, T.M. Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-alpha. Br. J. Nutr. 2010, 103, 460-466.
57. Hong, Y.H.; Nishimura, Y.; Hishikawa, D.; Tsuzuki, H.; Miyahara, H.; Gotoh, C.; Choi, K.C.; Feng, D.D.; Chen, C.; Lee, H.G.; et al. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 2005, 146, 5092-5099.
58. 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.
59. Torrazza, M.R.; Neu, J. The developing intestinal microbiome and its relationship to health and disease in the neonate. J. Perinatol. 2011, 31, S29-S34.
60. West, C.E.; Renz, H.; Jenmalm, M.C.; Kozyrskyj, A.L.; Allen, K.J.; Vuillermin, P.; Prescott, S.L. The gut microbiota and inflammatory noncommunicable diseases: Associations and potentials for gut microbiota therapies. J. Allergy Clin. Immunol. 2015, 135, 3-13.
61. Arenz, S.; Ruckerl, R.; Koletzko, B.; von Kries, R. Breast-feeding and childhood obesity-A systematic review. Int. J. Obes. Relat. Metab. Disord. 2004, 28, 1247-1256.
62. Horta, B.L.; Bahl, R.; Martinés, J.C.; Victoria, C.G. Evidence on the Long-Term Effects of Breastfeeding: Systematic Review and Meta-Analyses; World Health Organization: Geneva, Switzerland, 2007; pp. 1-57.
63. Owen, C.G.; Martin, R.M.; Whincup, P.H.; Davey-Smith, G.; Gillman, M.W.; Cook, D.G. The effect of breastfeeding on mean body mass index throughout life: A quantitative review of published and unpublished observational evidence. Am. J. Clin. Nutr. 2005, 82, 1298-1307.
64. Field, C.J. The immunological components of human milk and their effect on immune development in infants. J. Nutr. 2005, 135, 1-4.
65. Jeurink, P.V.; van, B.J.; Jimenez, E.; Knippels, L.M.; Fernandez, L.; Garssen, J.; Knol, J.; Rodriguez, J.M.; Martin, R. Human milk: A source of more life than we imagine. Benef. Microbes 2013, 4, 17-30.
66. Coppa, G.V.; Gabrielli, O.; Pierani, P.; Catassi, C.; Carlucci, A.; Giorgi, P.L. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 1993, 91, 637-641.
67. Viverge, D.; Grimmonprez, L.; Cassanas, G.; Bardet, L.; Solere, M. Variations in oligosaccharides and lactose in human milk during the first week of lactation. J. Pediatr. Gastroenterol. Nutr. 1990, 11, 361-364.
68. Bode, L. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology 2012, 22, 1147-1162.
69. Zivkovic, A.M.; German, J.B.; Lebrilla, C.B.; Mills, D.A. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. USA 2011, 108, 4653-4658.
70. Duncan, S.H.; Louis, P.; Thomson, J.M.; Flint, H.J. The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol. 2009, 11, 2112-2122.
71. Den Besten, G.; van Eunen, K.; Groen, A.K.; Venema, K.; Reijngoud, D.J.; Bakker, B.M. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013, 54, 2325-2340.
72. Collado, M.C.; Delgado, S.; Maldonado, A.; Rodriguez, J.M. Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR. Lett. Appl. Microbiol. 2009, 48, 523-528.
73. Hunt, K.M.; Foster, J.A.; Forney, L.J.; Schutte, U.M.; Beck, D.L.; Abdo, Z.; Fox, L.K.; Williams, J.E.; McGuire, M.K.; McGuire, M.A. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One 2011, 6, e21313, doi:10.1371/journal. pone.0021313.
74. Martin, R.; Jimenez, E.; Heilig, H.; Fernandez, L.; Marin, M.L.; Zoetendal, E.G.; Rodriguez, J.M. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl. Environ. Microbiol. 2009, 75, 965-969.
75. McGuire, M.K.; McGuire, M.A. Human milk: Mother nature's prototypical probiotic food? Adv. Nutr. 2015, 6, 112-123.
76. Arroyo, R.; Martin, V.; Maldonado, A.; Jimenez, E.; Fernandez, L.; Rodriguez, J.M. Treatment of infectious mastitis during lactation: Antibiotics versus oral administration of Lactobacilli isolated from breast milk. Clin. Infect. Dis. 2010, 50, 1551-1558.
77. Jimenez, E.; Fernandez, L.; Maldonado, A.; Martin, R.; Olivares, M.; Xaus, J.; Rodriguez, J.M. Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Appl. Environ. Microbiol. 2008, 74, 4650-4655.
78. Fernandez, L.; Langa, S.; Martin, V.; Maldonado, A.; Jimenez, E.; Martin, R.; Rodriguez, J.M. The human milk microbiota: Origin and potential roles in health and disease. Pharmacol. Res. 2013, 69, 1-10.
79. Ballard, O.; Morrow, A.L. Human milk composition: Nutrients and bioactive factors. Pediatr. Clin. North Am. 2013, 60, 49-74.
80. Cabrera-Rubio, R.; Collado, M.C.; Laitinen, K.; Salminen, S.; Isolauri, E.; Mira, A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 2012, 96, 544-551.
81. Gronlund, M.M.; Gueimonde, M.; Laitinen, K.; Kociubinski, G.; Gronroos, T.; Salminen, S.; Isolauri, E. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin. Exp. Allergy 2007, 37, 1764-1772.
82. Khodayar-Pardo, P.; Mira-Pascual, L.; Collado, M.C.; Martinez-Costa, C. Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J. Perinatol. 2014, 34, 599-605.
83. Forno, E.; Young, O.M.; Kumar, R.; Simhan, H.; Celedon, J.C. Maternal obesity in pregnancy, gestational weight gain, and risk of childhood asthma. Pediatrics 2014, 134, e535-e546.
84. FAO/WHO (Food and Agriculture Organization/World Health Organization). Guidelines for the evaluation of probiotics in food: Report of a Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food; Food and Agriculture Organization/World Health Organization:London, ON, Canada, 2002.
85. Fuller, R. Probiotics in human medicine. Gut 1991, 32, 439-442.
86. Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506-514.
87. Watson, R. Probiotics to treat visceral obesity and related liver disease. In Nutrition in the Prevention and Treatment of Abdominal Obesity; Elsevier: London, UK, 2014; pp. 363-380.
88. Braegger, C.; Chmielewska, A.; Decsi, T.; Kolacek, S.; Mihatsch, W.; Moreno, L.; Piescik, M.; Puntis, J.; Shamir, R.; Szajewska, H.; et al. Supplementation of infant formula with probiotics and/or prebiotics: A systematic review and comment by the ESPGHAN committee on nutrition. J. Pediatr. Gastroenterol. Nutr. 2011, 52, 238-250.
89. Nopchinda, S.; Varavithya, W.; Phuapradit, P.; Sangchai, R.; Suthutvoravut, U.; Chantraruksa, V.; Haschke, F. Effect of bifidobacterium Bb12 with or without Streptococcus thermophilus supplemented formula on nutritional status. J. Med. Assoc. Thai. 2002, 85, S1225-S1231.
90. Karlsson, V.F.; Ohlund, I.; Stenlund, H.; Hernell, O.; West, C.E. Probiotics during weaning: A follow-up study on effects on body composition and metabolic markers at school age. Eur. J. Nutr. 2014, 54, 355-363.
91. Luoto, R.; Kalliomaki, 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. (Lond.) 2010, 34, 1531-1537.
92. Roberfroid, M.; Gibson, G.R.; Hoyles, L.; McCartney, A.L.; Rastall, R.; Rowland, I.; Wolvers, D.; Watzl, B.; Szajewska, H.; Stahl, B.; et al. Prebiotic effects: Metabolic and health benefits. Br. J. Nutr. 2010, 104, S1-S63.
93. Cani, P.D.; Neyrinck, A.M.; Maton, N.; Delzenne, N.M. Oligofructose promotes satiety in rats fed a high-fat diet: Involvement of glucagon-like peptide-1. Obes. Res. 2005, 13, 1000-1007.
94. Lyon, M.; Wood, S.; Pelletier, X.; Donazzolo, Y.; Gahler, R.; Bellisle, F. Effects of a 3-month supplementation with a novel soluble highly viscous polysaccharide on anthropometry and blood lipids in nondieting overweight or obese adults. J. Hum. Nutr. Diet 2011, 24, 351-359.
95. 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. Am. J. Clin. Nutr. 2009, 89, 1751-1759.
96. Yang, H.Y.; Yang, S.C.; Chao, J.C.; Chen, J.R. Beneficial effects of catechin-rich green tea and inulin on the body composition of overweight adults. Br. J. Nutr. 2012, 107, 749-754.
97. 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.
98. EC Scientific Committee on Food. Additional statement on the use of resistant short chain carbohydrates (oligofurctosyl-saccharose and oligogalactosyl-lactose) in infant formula and in follow-on formula; EC Scientific Committee on Food: Brussels, Belgium, 2001.
99. Rao, S.; Srinivasjois, R.; Patole, S. Prebiotic supplementation in full-term neonates: A systematic review of randomized controlled trials. Arch. Pediatr. Adolesc. Med. 2009, 163, 755-764.
100. Holscher, H.D.; Faust, K.L.; Czerkies, L.A.; Litov, R.; Ziegler, E.E.; Lessin, H.; Hatch, T.; Sun, S.; Tappenden, K.A. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. J. Parenter. Enter. Nutr. 2012, 36, 95S-105S.
101. Sanders, M.E.; Guarner, F.; Guerrant, R.; Holt, P.R.; Quigley, E.M.; Sartor, R.B.; Sherman, P.M.; Mayer, E.A. An update on the use and investigation of probiotics in health and disease. Gut 2013, 62, 787-796.
102. Million, M.; Angelakis, E.; Paul, M.; Armougom, F.; Leibovici; L.; Rauolt, D. Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb. Pathog. 2012, 53, 100-108.
103. Million, M.; Raoult, D. Species and strain specificity of Lactobacillus probiotics effect on weight regulation. Microb. Pathog. 2013, 55, 52-54.
104. Anadon, A.; Martinez-Larranaga, M.R.; Aranzazu, M.M. Probiotics for animal nutrition in the European Union. Regulation and safety assessment. Regul. Toxicol. Pharmacol. 2006, 45, 91-95.
105. Robinson, E.L.; Thompson, W.L. Effect of weight gain of the addition of Lactobacillus acidophilus to the formula of newborn infants. J. Pediatr. 1952, 41, 395-398.
106. Abrahamsson, T.R.; Sinkiewicz, G.; Jakobsson, T.; Fredrikson, M.; Bjorksten, B. Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J. Pediatr. Gastroenterol. Nutr. 2009, 49, 349-354.
107. Oozeer, R.; van Limpt, K.; Ludwig, T.; Ben, A.K.; Martin, R.; Wind, R.D.; Boehm, G.; Knol, J. Intestinal microbiology in early life: Specific prebiotics can have similar functionalities as human-milk oligosaccharides. Am. J. Clin. Nutr. 2013, 98, 561S-571S.
108. Rautava, S.; Collado, M.C.; 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.
109. Gosalbes, M.J.; Llop, S.; Valles, Y.; Moya, A.; Ballester, F.; Francino, M.P. 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.
110. Jimenez, E.; Marin, M.L.; Martin, R.; Odriozola, J.M.; Olivares, M.; Xaus, J.; Fernandez, L.; Rodriguez, J.M. Is meconium from healthy newborns actually sterile? Res. Microbiol. 2008, 159, 187-193.