A combination of scGOS/lcFOS with Bifidobacterium breve M-16V protects suckling rats from rotavirus gastroenteritis

European Journal of Nutrition

Volumn 56, Issue 4, 2017, Pages 1657-1670

  Rigo Adrover, M ^a,b   Saldana Ruiz S ^a,b   van Limpt, K ^c   Knipping, K ^c,d   Garssen, J ^c,d   Knol, J ^c   Franch, A ^a,b   Castell, M ^a,b   Perez Cano F J ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b Nutrition and Food Safety Research Institute (INSA)   (Spain)

^c DANONE NUTRICIA RESEARCH   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Bifidobacterium breve; FOS; GOS; Prebiotic; Probiotic; Rotavirus; Synbiotic

Indexed keywords

FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M ANTIBODY; LONG CHAIN FRUCTOOLIGOSACCHARIDE; PREBIOTIC AGENT; PROBIOTIC AGENT; SHORT CHAIN FATTY ACID; SHORT CHAIN GALACTOOLIGOSACCHARIDE; UNCLASSIFIED DRUG; IMMUNOGLOBULIN M; SYNBIOTIC AGENT; VIRUS ANTIBODY; VOLATILE FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIFIDOBACTERIUM BREVE; CONTROLLED STUDY; DIARRHEA; DIET SUPPLEMENTATION; DISEASE SEVERITY; FECES ANALYSIS; FEMALE; IMMUNE RESPONSE; NONHUMAN; ROTAVIRUS; ROTAVIRUS INFECTION; VIRAL GASTROENTERITIS; VIRUS SHEDDING; ANIMAL; BLOOD; BODY WEIGHT; DISEASE MODEL; FECES; GASTROENTERITIS; LEWIS RAT; METABOLISM; MICROBIOLOGY; NEWBORN; RAT; SPECIMEN HANDLING; VIROLOGY;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, VIRAL; BIFIDOBACTERIUM BREVE; BODY WEIGHT; DIARRHEA; DISEASE MODELS, ANIMAL; FATTY ACIDS, VOLATILE; FECES; GASTROENTERITIS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; PREBIOTICS; PROBIOTICS; RATS; RATS, INBRED LEW; ROTAVIRUS; ROTAVIRUS INFECTIONS; SPECIMEN HANDLING; SYNBIOTICS;

EID: 84964490740     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-016-1213-1     Document Type: Article

References (87)

1. Parashar UD, Hummelman EG, Bresee JS et al (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9:565–572. doi:10.3201/eid0905.020562
2. Greenberg HB, Estes MK (2009) Rotaviruses: from pathogenesis to vaccination. Gastroenterology 136:1939–1951. doi:10.1053/j.gastro.2009.02.076
3. Clarke E, Desselberger U (2015) Correlates of protection against human rotavirus disease and the factors influencing protection in low-income settings. Mucosal Immunol 8:1–17. doi:10.1038/mi.2014.114
4. Riechmann ER, Cilleruelo ML, Rivero MJ (2006) Infección por rotavirus en España. In: Riechmann ER (ed) Infección por rotavirus. Undergraf S.L, Madrid, pp 67–75
5. Tate JE, Burton AH, Boschi-Pinto C et al (2012) 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis 12:136–141. doi:10.1016/S1473-3099(11)70253-5
6. Bines JE, Kirkwood CD (2015) Conquering rotavirus: from discovery to global vaccine implementation. J Paediatr Child Health 51:34–39. doi:10.1111/jpc.12815
7. Rigo-Adrover M, Franch À, Castell M et al (2014) Whey protein is beneficial for rotavirus-induced diarrhoea in preclinical studies. In: Preedy VR, Watson RR, Zibadi S (eds) Handbook of dietary and nutritional aspects of bottle feeding. Wageningen Academic Publishers, Wageningen, pp 491–506
8. Monedero V, Rodríguez-Díaz J, Viana R et al (2004) Selection of single-chain antibodies against the VP8* subunit of rotavirus VP4 outer capsid protein and their expression in Lactobacillus casei. Appl Environ Microbiol 70:6936–6939. doi:10.1128/AEM.70.11.6936-6939.2004
9. Maragkoudakis PA, Chingwaru W, Gradisnik L et al (2010) Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int J Food Microbiol 141:91–97. doi:10.1016/j.ijfoodmicro.2009.12.024
10. Varyukhina S, Freitas M, Bardin S et al (2012) Glycan-modifying bacteria-derived soluble factors from Bacteroides thetaiotaomicron and Lactobacillus casei inhibit rotavirus infection in human intestinal cells. Microbes Infect 14:273–278. doi:10.1016/j.micinf.2011.10.007
11. Lee DK, Park JE, Kim MJ et al (2015) Probiotic bacteria, B. longum and L. acidophilus inhibit infection by rotavirus in vitro and decrease the duration of diarrhea in pediatric patients. Clin Res Hepatol Gastroenterol 39:237–244. doi:10.1016/j.clinre.2014.09.006
12. Liu F, Li G, Wen K et al (2010) Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics. Viral Immunol 23:135–149. doi:10.1089/vim.2009.0088
13. Muñoz JAM, Chenoll E, Casinos B et al (2011) Novel probiotic Bifidobacterium longum subsp. infantis CECT 7210 strain active against rotavirus infections. Appl Environ Microbiol 77:8775–8783. doi:10.1128/AEM.05548-11
14. Seo BJ, Mun MR, Kumar RVJ et al (2010) Bile tolerant Lactobacillus reuteri isolated from pig feces inhibits enteric bacterial pathogens and porcine rotavirus. Vet Res Commun 34:323–333. doi:10.1007/s11259-010-9357-6
15. MacPherson C, Audy J, Mathieu O, Tompkins TA (2014) Multistrain probiotic modulation of intestinal epithelial cells’ immune response to a double-stranded RNA ligand, Poly(I C). Appl Environ Microbiol 80:1692–1700. doi:10.1128/AEM.03411-13
16. Buccigrossi V, Laudiero G, Russo C et al (2014) Chloride secretion induced by rotavirus is oxidative stress-dependent and inhibited by Saccharomyces boulardii in human enterocytes. PLoS ONE 9:1–12. doi:10.1371/journal.pone.0099830
17. Chattha KS, Vlasova AN, Kandasamy S et al (2013) Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J Immunol 191:2446–2456. doi:10.4049/jimmunol.1300678
18. Zhang W, Azevedo MSP, Gonzalez AM et al (2008) Influence of probiotic Lactobacilli colonization on neonatal B cell responses in a gnotobiotic pig model of human rotavirus infection and disease. Vet Immunol Immunopathol 122:175–181. doi:10.1016/j.vetimm.2007.10.003
19. Zhang W, Azevedo MSP, Wen K et al (2008) Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 26:3655–3661. doi:10.1016/j.vaccine.2008.04.070
20. Wen K, Li G, Zhang W et al (2011) Development of γδ T cell subset responses in gnotobiotic pigs infected with human rotaviruses and colonized with probiotic lactobacilli. Vet Immunol Immunopathol 141:267–275. doi:10.1016/j.vetimm.2011.03.016
21. Liu F, Li G, Wen K et al (2013) Lactobacillus rhamnosus GG on rotavirus-induced injury of ileal epithelium in gnotobiotic pigs. J Pediatr Gastroenterol Nutr 57:750–758. doi:10.1097/MPG.0b013e3182a356e1
22. Vlasova AN, Chattha KS, Kandasamy S et al (2013) Lactobacilli and bifidobacteria promote immune homeostasis by modulating innate immune responses to human rotavirus in neonatal gnotobiotic pigs. PLoS ONE 8:1–15. doi:10.1371/journal.pone.0076962
23. Wu S, Yuan L, Zhang Y et al (2013) Probiotic Lactobacillus rhamnosus GG mono-association suppresses human rotavirus-induced autophagy in the gnotobiotic piglet intestine. Gut Pathog 5:22. doi:10.1186/1757-4749-5-22
24. Zhang H, Wang H, Shepherd M et al (2014) Probiotics and virulent human rotavirus modulate the transplanted human gut microbiota in gnotobiotic pigs. Gut Pathog 6:39. doi:10.1186/s13099-014-0039-8
25. Liu F, Wen K, Li G et al (2014) Dual functions of lactobacillus acidophilus NCFM as protection against rotavirus diarrhea. J Pediatr Gastroenterol Nutr 58:169–176. doi:10.1097/MPG.0000000000000197
26. Wen K, Liu F, Li G et al (2015) Lactobacillus rhamnosus GG dosage affects the adjuvanticity and protection against rotavirus diarrhea in gnotobiotic pigs. J Pediatr Gastroenterol Nutr 60:834–843. doi:10.1097/MPG.0000000000000694
27. Kandasamy S, Chattha KS, Vlasova AN et al (2014) Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes 5:639–651. doi:10.4161/19490976.2014.969972
28. Duffy LC, Zielezny MA, Riepenhoff-Talty M et al (1994) Effectiveness of Bifidobacterium bifidum in mediating the clinical course of murine rotavirus diarrhea. Pediatr Res 35:690–695. doi:10.1203/00006450-199406000-00014
29. Pant N, Marcotte H, Brüssow H et al (2007) Effective prophylaxis against rotavirus diarrhea using a combination of Lactobacillus rhamnosus GG and antibodies. BMC Microbiol 7:86. doi:10.1186/1471-2180-7-86
30. Preidis GA, Saulnier DM, Blutt SE et al (2012) Host response to probiotics determined by nutritional status of rotavirus-infected neonatal mice. J Pediatr Gastroenterol Nutr 55:1. doi:10.1097/MPG.0b013e31824d2548
31. Zhang Z, Xiang Y, Li N et al (2013) Protective effects of Lactobacillus rhamnosus GG against human rotavirus-induced diarrhoea in a neonatal mouse model. Pathog Dis 67:184–191. doi:10.1111/2049-632X.12030
32. Guérin-Danan C, Meslin JC, Chambard A et al (2001) Food supplementation with milk fermented by Lactobacillus casei DN-114 001 protects suckling rats from rotavirus-associated diarrhea. J Nutr 131:111–117
33. Ventola H, Lehtoranta L, Madetoja M et al (2012) Effects of the viability of Lactobacillus rhamnosus GG on rotavirus infection in neonatal rats. World J Gastroenterol 18:5925–5931. doi:10.3748/wjg.v18.i41.5925
34. Teran CG, Teran-Escalera CN, Villarroel P (2009) Nitazoxanide vs. probiotics for the treatment of acute rotavirus diarrhea in children: a randomized, single-blind, controlled trial in Bolivian children. Int J Infect Dis 13:518–523. doi:10.1016/j.ijid.2008.09.014
35. Grandy G, Medina M, Soria R et al (2010) Probiotics in the treatment of acute rotavirus diarrhoea. A randomized, double-blind, controlled trial using two different probiotic preparations in Bolivian children. BMC Infect Dis 10:253. doi:10.1186/1471-2334-10-253
36. Szymański H, Pejcz J, Jawień M et al (2006) Treatment of acute infectious diarrhoea in infants and children with a mixture of three Lactobacillus rhamnosus strains—a randomized, double-blind, placebo-controlled trial. Aliment Pharmacol Ther 23:247–253. doi:10.1111/j.1365-2036.2006.02740.x
37. Sindhu KNC, Sowmyanarayanan TV, Paul A et al (2014) Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis 58:1107–1115. doi:10.1093/cid/ciu065
38. Mao M, Yu T, Xiong Y et al (2008) Effect of a lactose-free milk formula supplemented with bifidobacteria and streptococci on the recovery from acute diarrhoea. Asia Pac J Clin Nutr 17:30–34
39. Sarker SA, Sultana S, Fuchs GJ et al (2005) Lactobacillus paracasei strain ST11 has no effect on rotavirus but ameliorates the outcome of nonrotavirus diarrhea in children from Bangladesh. Pediatrics 116:e221–e228. doi:10.1542/peds.2004-2334
40. Dutta P, Mitra U, Dutta S et al (2011) Randomised controlled clinical trial of Lactobacillus sporogenes (Bacillus coagulans), used as probiotic in clinical practice, on acute watery diarrhoea in children. Trop Med Int Heal 16:555–561. doi:10.1111/j.1365-3156.2011.02745.x
41. Erdoǧan Ö, Tanyeri B, Torun E et al (2012) The comparition of the efficacy of two different probiotics in rotavirus gastroenteritis in children. J Trop Med. doi:10.1155/2012/787240
42. Dalgic N, Sancar M, Bayraktar B et al (2011) Probiotic, zinc and lactose-free formula in children with rotavirus diarrhea: are they effective? Pediatr Int 53:677–682. doi:10.1111/j.1442-200X.2011.03325.x
43. Corrêa NBO, Penna FJ, Lima FMLS et al (2011) Treatment of acute diarrhea with Saccharomyces Boulardii in infants. J Pediatr Gastroenterol Nutr 53:1. doi:10.1097/MPG.0b013e31822b7ab0
44. Isolauri E, Juntunen M, Rautanen T et al (1991) A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88:90–97
45. Suárez JE (2015) Autochthonous microbiota, probiotics and prebiotics. Nutr Hosp 31:3–9. doi:10.3305/nh.2015.31.sup1.8701
46. Corzo N, Alonso JL, Azpiroz F et al (2015) Prebiotics: concept, properties and beneficial effects. Nutr Hosp 31:99–118. doi:10.3305/nh.2015.31.sup1.8715
47. Hester SN, Chen X, Li M et al (2013) Human milk oligosaccharides inhibit rotavirus infectivity in vitro and in acutely infected piglets. Br J Nutr. doi:10.1017/S0007114513000391
48. Li M, Wang M, Comstock SS et al (2014) Human milk oligosaccharides shorten rotavirus-induced diarrhea and modulate piglet mucosal immunity and colonic microbiota. ISME J 8:1609–1620. doi:10.1038/ismej.2014.10
49. Noguera T, Wotring R, Melville CR et al (2014) Resolution of acute gastroenteritis symptoms in children and adults treated with a novel polyphenol-based prebiotic. World J Gastroenterol 20:12301–12307. doi:10.3748/wjg.v20.i34.12301
50. Binns CW, Lee AH, Harding H et al (2007) The CUPDAY Study: prebiotic-probiotic milk product in 1–3-year-old children attending childcare centres. Acta Paediatr Int J Paediatr. doi:10.1111/j.1651-2227.2007.00508.x
51. Veereman-Wauters G, Staelens S, Van de Broek H et al (2011) Physiological and bifidogenic effects of prebiotic supplements in infant formulae. J Pediatr Gastroenterol Nutr 52:763–771. doi:10.1097/MPG.0b013e3182139f39
52. Pan X, Chen F, Wu T et al (2009) Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J Zhejiang Univ Sci B 10:258–263. doi:10.1631/jzus.B0820261
53. Djouzi Z, Andrieux C (1997) Compared effects of three oligosaccharides on metabolism of intestinal microflora in rats inoculated with a human faecal flora. Br J Nutr 78:313–324. doi:10.1079/BJN19970149
54. Bruzzese E, Volpicelli M, Squeglia V et al (2009) A formula containing galacto- and fructo-oligosaccharides prevents intestinal and extra-intestinal infections: an observational study. Clin Nutr 28:156–161. doi:10.1016/j.clnu.2009.01.008
55. Arslanoglu S, Moro GE, Boehm G (2007) Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J Nutr 137:2420–2424
56. Osborn DA, Sinn JKH (2013) Prebiotics in infants for prevention of allergy. Cochrane Db Syst Rev 3:CD006474
57. Van Hoffen E, Ruiter B, Faber J et al (2009) A specific mixture of short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy Eur J Allergy Clin Immunol 64:484–487. doi:10.1111/j.1398-9995.2008.01765.x
58. Scholtens PAMJ, Alliet P, Raes M et al (2008) Fecal secretory immunoglobulin A is increased in healthy infants who receive a formula with short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides. J Nutr 138:1141–1147
59. Bakker-Zierikzee AM, Van Tol EAF, Kroes H et al (2006) Faecal SIgA secretion in infants fed on pre- or probiotic infant formula. Pediatr Allergy Immunol 17:134–140. doi:10.1111/j.1399-3038.2005.00370.x
60. Salvatore S, Vandenplas Y (2010) Bioact Foods Promot Health. doi: 10.1016/B978-0-12-374938-3.00013-X
61. ®) prebiotic mixture and interaction with calcium intake on mineral absorption and bone parameters in growing rats. Eur J Nutr 54:913–923. doi:10.1007/s00394-014-0768-y
62. Bryk G, Hernandez E, Chaves MG et al (2015) Utilidad de una mezcla prebiótica para aumentar la absorción y retención de calcio durante el crecimiento normal y durante la recuperación de una malnutrición proteica: modelo experimental en ratas. Actual Osteol 11:19–37
63. Schmidt K, Cowen PJ, Harmer CJ et al (2015) Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232:1793–1801. doi:10.1007/s00213-014-3810-0
64. Savignac HM, Corona G, Mills H et al (2013) Prebiotic feeding elevates central brain derived neurotrophic factor, N-methyl-d-aspartate receptor subunits and d-serine. Neurochem Int 63:756–764. doi:10.1016/j.neuint.2013.10.006
65. Vos AP, Haarman M, Buco A et al (2006) A specific prebiotic oligosaccharide mixture stimulates delayed-type hypersensitivity in a murine influenza vaccination model. Int Immunopharmacol 6:1277–1286. doi:10.1016/j.intimp.2006.03.010
66. Vos AP, Haarman M, VanGinkel JWH et al (2007) Dietary supplementation of neutral and acidic oligosaccharides enhances Th1-dependent vaccination responses in mice. Pediatr Allergy Immunol 18:304–312. doi:10.1111/j.1399-3038.2007.00515.x
67. Verheijden KAT, Willemsen LEM, Braber S et al (2015) The development of allergic inflammation in a murine house dust mite asthma model is suppressed by synbiotic mixtures of non-digestible oligosaccharides and Bifidobacterium breve M-16V. Eur J Nutr. doi:10.1007/s00394-015-0928-8
68. Hougee S, Vriesema AJM, Wijering SC et al (2010) Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int Arch Allergy Immunol 151:107–117. doi:10.1159/000236000
69. De Kivit S, Saeland E, Kraneveld AD et al (2012) Galectin-9 induced by dietary synbiotics is involved in suppression of allergic symptoms in mice and humans. Allergy Eur J Allergy Clin Immunol 67:343–352. doi:10.1111/j.1398-9995.2011.02771.x
70. De Kivit S, Kraneveld AD, Knippels LMJ et al (2013) Intestinal epithelium-derived galectin-9 is involved in the immunomodulating effects of nondigestible oligosaccharides. J Innate Immun 5:625–638. doi:10.1159/000350515
71. Van De Pol MA, Lutter R, Smids BS et al (2011) Synbiotics reduce allergen-induced T-helper 2 response and improve peak expiratory flow in allergic asthmatics. Allergy Eur J Allergy Clin Immunol 66:39–47. doi:10.1111/j.1398-9995.2010.02454.x
72. Schouten B, van Esch BCAM, Hofman GA et al (2009) Cow milk allergy symptoms are reduced in mice fed dietary synbiotics during oral sensitization with whey. J Nutr 139:1398–1403. doi:10.3945/jn.109.108514
73. Pérez-Cano FJ, Marín-Gallén S, Castell M et al (2007) Bovine whey protein concentrate supplementation modulates maturation of immune system in suckling rats. Br J Nutr 98:S80–S84. doi:10.1017/S0007114507838074
74. Pérez-Cano FJ, Marín-Gallén S, Castell M et al (2008) Supplementing suckling rats with Whey protein concentrate modulates the immune response and ameliorates rat. J Nutr. doi:10.3945/jn.108.093856
75. Pérez-Cano FJ, Castell M, Castellote C, Franch À (2007) Characterization of clinical and immune response in a rotavirus diarrhea model in suckling Lewis rats. Pediatr Res 62:658–663. doi:10.1203/PDR.0b013e318159a273
76. Costabile A, Kolida S, Klinder A et al (2010) A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104:1007–1017. doi:10.1017/S0007114510001571
77. Gomez E, Tuohy KM, Gibson GR et al (2010) In vitro evaluation of the fermentation properties and potential prebiotic activity of Agave fructans. J Appl Microbiol 108:2114–2121. doi:10.1111/j.1365-2672.2009.04617.x
78. Pérez-Cano FJ, Franch À, Castellote C, Castell M (2012) The suckling rat as a model for immunonutrition studies in early life. Clin Dev Immunol 2012:537310. doi:10.1155/2012/537310
79. Patole S, Keil AD, Chang A et al (2014) Effect of Bifidobacterium breve M-16V supplementation on fecal bifidobacteria in preterm neonates—a randomised double blind placebo controlled trial. PLoS ONE 9:1–8. doi:10.1371/journal.pone.0089511
80. Yamashiro Y, Nagata S (2010) Beneficial microbes for premature infants, and children with malignancy undergoing chemotherapy. Benef Microbes 1:357–365. doi:10.3920/BM2010.0035
81. Guérin-Danan C, Meslin JC, Lambre F et al (1998) Development of a heterologous model in germfree suckling rats for studies of rotavirus diarrhea. J Virol 72:9298–9302
82. Etzold S, Bode L (2014) Glycan-dependent viral infection in infants and the role of human milk oligosaccharides. Curr Opin Virol 7:101–107. doi:10.1016/j.coviro.2014.06.005
83. Ciarlet M, Conner ME, Finegold MJ, Estes MK (2002) Group a rotavirus infection and age-dependent diarrheal disease in rats: a new animal model to study the pathophysiology of rotavirus infection. J Virol 76:41–57. doi:10.1128/JVI.76.1.41
84. Knipping K, McNeal MM, Crienen A et al (2011) A gastrointestinal rotavirus infection mouse model for immune modulation studies. Virol J 8:109. doi:10.1186/1743-422X-8-109
85. Inoue Y, Iwabuchi N, Xiao JZ et al (2009) Suppressive effects of bifidobacterium breve strain M-16V on T-helper type 2 immune responses in a murine model. Biol Pharm Bull 32:760–763. doi:10.1248/bpb.32.760
86. Desselberger U, Huppertz H-I (2011) Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203:188–195. doi:10.1093/infdis/jiq031
87. Macfarlane GT, Macfarlane S (2011) Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol 45:S120–S127. doi:10.1097/MCG.0b013e31822fecfe