Prevention of rotavirus diarrhea in suckling rats by a specific fermented milk concentrate with prebiotic mixture

Nutrients

Volumn 11, Issue 1, 2019, Pages

  Rigo Adrover, Maria Del Mar ^a,b   Knipping, Karen ^c,d   Garssen, Johan ^c,d   van Limpt, Kees ^c   Knol, Jan ^c   Franch, Àngels ^a,b   Castell, Margarida ^a,b   Rodríguez Lagunas, Maria J ^a,b   Pérez Cano, Francisco J ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b Institut de Recerca en Nutrició i Seguretat Alimentària de la UB INSA UB   (Spain)

^c DANONE NUTRICIA RESEARCH   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Fermented formula; Postbiotic; Prebiotic; Probiotic; Rotavirus

Indexed keywords

FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; KETAMINE; PREBIOTIC AGENT; XYLAZINE; OLIGOSACCHARIDE; PROBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; BIFIDOBACTERIUM; DIARRHEA; DIARRHEA INDEX; DIET SUPPLEMENTATION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES; FERMENTED DAIRY PRODUCT; GROWTH RATE; HEALTH STATUS INDICATOR; HUMORAL IMMUNITY; IMMUNE RESPONSE; INCIDENCE; INOCULATION; MILK; MORPHOMETRY; NONHUMAN; PH; RAT; ROTAVIRUS; STREPTOCOCCUS THERMOPHILUS; SUCKLING ANIMAL; VIRUS LOAD; VIRUS SHEDDING; ANIMAL; ARTIFICIAL MILK; BACTERIUM; BIFIDOBACTERIUM BREVE; COMPLICATION; FEMALE; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNITY; INFANT; INTESTINE FLORA; LEWIS RAT; MALE; MICROBIOLOGY; NEWBORN; ROTAVIRUS INFECTION; SEVERITY OF ILLNESS INDEX; VIROLOGY;

ANIMALS; ANIMALS, NEWBORN; BACTERIA; BIFIDOBACTERIUM BREVE; CULTURED MILK PRODUCTS; DIARRHEA; FEMALE; FERMENTATION; GASTROINTESTINAL MICROBIOME; HUMANS; IMMUNITY; INFANT; INFANT FORMULA; MALE; MILK; OLIGOSACCHARIDES; PREBIOTICS; PROBIOTICS; RATS, INBRED LEW; ROTAVIRUS; ROTAVIRUS INFECTIONS; SEVERITY OF ILLNESS INDEX; STREPTOCOCCUS THERMOPHILUS;

EID: 85060401553     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu11010189     Document Type: Article

References (43)

1. Tate, J.E.; Burton, A.H.; Boschi-Pinto, C.; Parashar, U.D. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000–2013. Clin. Infect. Dis. 2016, 62, S96–S105.
2. Estes, M.; Greenberg, H. Rotaviruses. In Fields Virology; Knipe, D.M., Howley, P.M., Eds.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2013.
3. Greenberg, H.B.; Estes, M.K. Rotaviruses: From pathogenesis to vaccination. Gastroenterology 2009, 136, 1939–1951. [CrossRef]
4. Madhi, S.A.; Cunliffe, N.A.; Steele, D.; Witte, D.; Kirsten, M.; Louw, C.; Ngwira, B.; Victor, J.C.; Gillard, P.H.; Cheuvart, B.B.; et al. Effect of human rotavirus vaccine on severe diarrhea in African infants. N. Engl. J. Med. 2010, 362, 289–298. [CrossRef]
5. 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. [CrossRef]
6. Rigo-Adrover, M.D.M.; van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Costabile, A.; Franch, À.; Castell, M.; Pérez-Cano, F.J. Preventive Effect of a Synbiotic Combination of Galacto-and Fructooligosaccharides Mixture with Bifidobacterium breve M-16V in a Model of Multiple Rotavirus Infections. Front. Immunol. 2018, 9, 1318. [CrossRef]
7. Gonzalez-Ochoa, G.; Flores-Mendoza, L.K.; Icedo-Garcia, R.; Gomez-Flores, R.; Tamez-Guerra, P. Modulation of rotavirus severe gastroenteritis by the combination of probiotics and prebiotics. Arch. Microbiol. 2017, 199, 953–961. [CrossRef]
8. Aguilar-Toalá, J.E.; Garcia-Varela, R.; Garcia, H.S.; Mata-Harod, V.; González-Córdova, A.F.; Vallejo-Cordoba, B.; Hernández-Mendoza, A. Postbiotics: An evolving term within the functional foods field. Trends Food Sci. Technol. 2018, 75, 105–114. [CrossRef]
9. Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 1995, 125, 1401–1412. [CrossRef]
10. Gibson, G.R.; Hutkins, R.; Sanders, M.E.; Prescott, S.L.; Reimer, R.A.; Salminen, S.J.; Scott, K.; Stanton, C.; Swanson, K.S.; Verbeke, K.; et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 2017, 14, 491–502. [CrossRef]
11. Rigo-Adrover, M.; Saldaña-Ruíz, S.; van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Franch, A.; Castell, M.; Pérez-Cano, F.J. A combination of scGOS/lcFOS with Bifidobacterium breve M-16V protects suckling rats from rotavirus gastroenteritis. Eur. J. Nutr. 2017, 56, 1657–1670. [CrossRef]
12. Cicenia, A.; Scirocco, A.; Carabotti, M.; Pallotta, L.; Marignani, M.; Severi, C. Postbiotic activities of lactobacilli-derived factors. J. Clin. Gastroenterol. 2014, 48, S18–S22. [CrossRef]
13. Patel, R.M.; Denning, P.W. Therapeutic use of prebiotics, probiotics, and postbiotics to prevent necrotizing enterocolitis: What is the current evidence? Clin. Perinatol. 2013, 40, 11–25. [CrossRef] [PubMed]
14. Tsilingiri, K.; Rescigno, M. Postbiotics: What else? Benef. Microbes 2013, 4, 101–107. [CrossRef] [PubMed]
15. Pérez-Cano, F.J.; Castell, M.; Castellote, C.; Franch, À. Characterization of clinical and immune response in a rotavirus diarrhea model in suckling Lewis rats. Pediatr. Res. 2007, 62, 658–663. [CrossRef]
16. Pérez-Cano, F.J.; Marín-Gallén, S.; Castell, M.; Rodríguez-Palmero, M.; Rivero, M.; Castellote, C.; Franch, À. Supplementing suckling rats with whey protein concentrate modulates the immune response and ameliorates rat rotavirus induced diarrhea. J. Nutr. 2008, 138, 2392–2398. [CrossRef]
17. Rigo-Adrover, M.; Pérez-Berezo, T.; Ramos-Romero, S.; van Limpt, K.; Knipping, K.; Garssen, J.; Knol, J.; Franch, À.; Castell, M.; Pérez-Cano, F.J. A fermented milk concentrate and a combination of short-chain galacto-oligosaccharides/long-chain fructo-oligosaccharides/pectin-derived acidic oligosaccharides protect suckling rats from rotavirus gastroenteritis. Br. J. Nutr. 2017, 117, 209–217. [CrossRef]
18. Veereman-Wauters, G.; Staelens, S.; Van de Broek, H.; Plaskie, K.; Wesling, F.; Roger, L.C.; McCartney, A.L.; Assam, P. Physiological and bifidogenic effects of prebiotic supplements in infant formulae. J. Pediatr. Gastroenterol. Nutr. 2011, 52, 763–771. [CrossRef] [PubMed]
19. Pan, X.; Chen, F.; Wu, T.; Tang, H.G.; Zhao, Z.Y. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J. Zhejiang Univ. Sci. B 2009, 10, 258–263. [CrossRef]
20. Scholtens, P.A.M.J.; Alliet, P.; Raes, M.; Alles, M.S.; Kroes, H.; Boehm, G.; Knippels, L.M.; Knol, J.; Vandenplas, Y. 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. 2008, 138, 1141–1147. [CrossRef]
21. Arslanoglu, S.; Moro, G.E.; Boehm, G. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J. Nutr. 2007, 137, 2420–2424. [CrossRef]
22. Bruzzese, E.; Volpicelli, M.; Squeglia, V.; Bruzzese, D.; Salvini, F.; Bisceglia, M.; Lionetti, P.; Cinquetti, M.; Iacono, G.; Amarri, S.; et al. A formula containing galacto-and fructo-oligosaccharides prevents intestinal and extra-intestinal infections: An observational study. Clin. Nutr. 2009, 28, 156–161. [CrossRef] [PubMed]
23. Van Hoffen, E.; Ruiter, B.; Faber, J.; M’Rabet, L.; Knol, E.F.; Stahl, B.; Arslanoglu, S.; Moro, G.; Boehm, G.; Garssen, J. 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 2009, 64, 484–487. [CrossRef] [PubMed]
24. Romond, M.B.; Ais, A.; Yazourh, A.; Romond, C. Cell-free wheys from bifidobacteria fermented milks exert a regulatory effect on the intestinal microflora of mice and humans. Anaerobe 1997, 3, 137–143. [CrossRef] [PubMed]
25. Romond, M.B.; Ais, A.; Guillemot, F.; Bounouader, R.; Cortot, A.; Romond, C. Cell-free whey from milk fermented with Bifidobacterium breve C50 used to modify the colonic microflora of healthy subjects. J. Dairy Sci. 1998, 81, 1229–1235. [CrossRef]
26. Thibault, H.; Aubert-Jacquin, C.; Goulet, O. Effects of long-term consumption of a fermented infant formula (with Bifidobacterium breve c50 and Streptococcus thermophilus 065) on acute diarrhea in healthy infants. J. Pediatr. Gastroenterol. Nutr. 2004, 39, 147–152. [CrossRef]
27. Macfarlane, H.S.S. Mechanisms of prebiotic impact on health. In Prebiotics and Probiotics Science and Technology; Charalampopoulos, D., Rastall, R.A., Eds.; Springer: New York, NY, USA, 2009; pp. 135–161.
28. Rasmussen, S.O.; Martin, L.; Østergaard, M.V.; Rudloff, S.; Roggenbuck, M.; Nguyen, D.N.; Sangild, P.T.; Bering, S.B. Human milk oligosaccharide effects on intestinal function and inflammation after preterm birth in pigs. J. Nutr. Biochem. 2017, 40, 141–154. [CrossRef] [PubMed]
29. Kareem, K.Y.; Loh, T.C.; Foo, H.L.; Akit, H.; Samsudin, A.A. Effects of dietary postbiotic and inulin on growth performance, IGF1 and GHR mRNA expression, faecal microbiota and volatile fatty acids in broilers. BMC Vet. Res. 2016, 12, 163. [CrossRef]
30. Indrio, F.; Ladisa, G.; Mautone, A.; Montagna, O. Effect of a fermented formula on thymus size and stool pH in healthy term infants. Pediatr. Res. 2007, 62, 98–100. [CrossRef]
31. Westerbeek, E.; Hensgens, R.; Mihatsch, W.; Boehm, G.; Lafeber, H.N.; van Elburg, R.M. The effect of neutral and acidic oligosaccharides on stool viscosity, stool frequency and stool pH in preterm infants. Acta Paediatr. 2011, 100, 1426–1431. [CrossRef]
32. Heuvelin, E.; Lebreton, C.; Bichara, M.; Cerf-Bensussan, N.; Heyman, M. A Bifidobacterium probiotic strain and its soluble factors alleviate chloride secretion by human intestinal epithelial cells. J. Nutr. 2010, 140, 7–11. [CrossRef]
33. Shoaf-Sweeney, K.D.; Hutkins, R.W. Chapter 2: Adherence, anti-adherence, and oligosaccharides. Preventing pathogens from sticking to the host. In Advances in Food and Nutrition Research; Taylor, S., Ed.; Elsevier: Lincoln, NE, USA, 2008; Volume 55, pp. 101–161.
34. Wang, Y.; Liu, Y.; Kirpich, I.; Ma, Z.; Wang, C.; Zhang, M.; Suttles, J.; McClain, C.; Feng, W. Lactobacillus rhamnosus GG reduces hepatic TNFα production and inflammation in chronic alcohol-induced liver injury. J. Nutr. Biochem. 2013, 24, 1609–1615. [CrossRef] [PubMed]
35. Yan, F.; Polk, D.B. Characterization of a probiotic-derived soluble protein which reveals a mechanism of preventive and treatment effects of probiotics on intestinal inflammatory diseases. Gut Microbes 2012, 3, 25–28. [CrossRef] [PubMed]
36. Yan, F.; Polk, D.B. Lactobacillus rhamnosus GG: An Updated Strategy to Use Microbial Products to Promote Health. Funct. Food Rev. 2012, 4, 77–84. [PubMed]
37. Verdú, E.F.; Bercík, P.; Bergonzelli, G.E.; Huang, X.X.; Blennerhasset, P.; Rochat, F.; Fiaux, M.; Mansourian, R.; Corthésy-Theulaz, I.; Collins, S.M. Lactobacillus paracasei normalizes muscle hypercontractility in a murine model of postinfective gut dysfunction. Gastroenterology 2004, 127, 826–837. [CrossRef] [PubMed]
38. Macho Fernandez, E.; Valenti, V.; Rockel, C.; Hermann, C.; Pot, B.; Boneca, I.G.; Grangette, C. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 2011, 60, 1050–1059. [CrossRef]
39. Compare, D.; Rocco, A.; Coccoli, P.; Angrisani, D.; Sgamato, C.; Iovine, B.; Salvatore, U.; Nardone, G. Lactobacillus casei DG and its postbiotic reduce the inflammatory mucosal response: An ex-vivo organ culture model of post-infectious irritable bowel syndrome. BMC Gastroenterol. 2017, 17, 53. [CrossRef] [PubMed]
40. Lee, M.J.; Zang, Z.L.; Choi, E.Y.; Shin, H.K.; Ji, G.E. Cytoskeleton Reorganization and Cytokine Production of Macrophages by Bifidobacterial Cells and Cell—Free Extracts. J. Microbiol. Biotechnol. 2002, 12, 398–405.
41. Ménard, S.; Candalh, C.; Ben Ahmed, M.; Rakotobe, S.; Gaboriau-Routhiau, V.; Cerf-Bensussan, N.; Heyman, M. Stimulation of immunity without alteration of oral tolerance in mice fed with heat-treated fermented infant formula. J. Pediatr. Gastroenterol. Nutr. 2006, 43, 451–458. [CrossRef]
42. Campeotto, F.; Suau, A.; Kapel, N.; Magne, F.; Viallon, V.; Ferraris, L.; Waligora-Dupriet, A.J.; Soulaines, P.; Leroux, B.; Kalach, N.; et al. A fermented formula in pre-term infants: Clinical tolerance, gut microbiota, down-regulation of faecal calprotectin and up-regulation of faecal secretory IgA. Br. J. Nutr. 2011, 105, 1843–1851. [CrossRef]
43. Morisset, M.; Aubert-Jacquin, C.; Soulaines, P.; Moneret-Vautrin, D.A.; Dupont, C. A non-hydrolyzed, fermented milk formula reduces digestive and respiratory events in infants at high risk of allergy. Eur. J. Clin. Nutr. 2011, 65, 175–183. [CrossRef]