Probiotics, prebiotics, and synbiotics for the prevention of necrotizing enterocolitis

Advances in Nutrition

Volumn 7, Issue 5, 2016, Pages 928-937

  Johnson Henry, Kathene C ^a   Abrahamsson, Thomas R ^b   Wu, Richard You ^a,c   Sherman, Philip M ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b LINKÖPING UNIVERSITY   (Sweden)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Breast milk; Functional foods; Human milk oligosaccharides; Inflammation; Necrotizing enterocolitis; Neonatology; Prebiotics; Premature; Probiotics; Synbiotics

Indexed keywords

OLIGOSACCHARIDE; PREBIOTIC AGENT; PROBIOTIC AGENT; SYNBIOTIC AGENT;

BACTERIUM; BREAST MILK; CHEMISTRY; ENTEROCOLITIS, NECROTIZING; HUMAN; MICROBIOLOGY; NEONATOLOGY;

BACTERIA; ENTEROCOLITIS, NECROTIZING; HUMANS; MILK, HUMAN; NEONATOLOGY; OLIGOSACCHARIDES; PREBIOTICS; PROBIOTICS; SYNBIOTICS;

EID: 84992679483     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.116.012237     Document Type: Review

References (101)

1. Huttenhower C, Knight R, Brown CT, Caporaso JG, Clemente JC, Gevers D, Franzosa EA, Kelley ST, Knights D, Ley RE, et al. Advancing the microbiome research community. Cell 2014;159:227-30.
2. Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, Versalovic J, Young V, Finlay BB. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 2012;12:611-22.
3. de Souza HS, Fiocchi C. Immunopathogenesis of IBD: current state of the art. Nat Rev Gastroenterol Hepatol 2016;13:13-27.
4. Abrahamsson TR, Wu RY, Jenmalm MC. Gut microbiota and allergy: the importance of the pregnancy period. Pediatr Res 2015;77:214-9.
5. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014;15:317-28.
6. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013;341:1241214.
7. Brower-Sinning R, Zhong D, Good M, Firek B, Baker R, Sodhi CP, Hackam DJ, Morowitz MJ. Mucosa-associated bacterial diversity in necrotizing enterocolitis. PLoS One 2014;9:e105046.
8. Ford AC, Quigley EM, Lacy BE, Lembo AJ, Saito YA, Schiller LR, Soffer EE, Spiegel BM, Moayyedi P. Efficacy of prebiotics, probiotics, and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: systematic review and meta-analysis. Am J Gastroenterol 2014;109:1547-61; quiz: 6, 62.
9. Chau K, Lau E, Greenberg S, Jacobson S, Yazdani-Brojeni P, Verma N, Koren G. Probiotics for infantile colic: a randomized, double-blind, placebo-controlled trial investigating Lactobacillus reuteri DSM 17938. J Pediatr 2015;166:74-8.
10. Olsen R, Greisen G, Schroder M, Brok J. Prophylactic probiotics for preterm infants: a systematic review and meta-analysis of observational studies. Neonatology 2016;109:105-12.
11. Patel RM, Kandefer S, Walsh MC, Bell EF, Carlo WA, Laptook AR, Sanchez PJ, Shankaran S, Van Meurs KP, Ball MB, et al. Causes and timing of death in extremely premature infants from 2000 through 2011. N Engl J Med 2015;372:331-40.
12. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 2011;364: 255-64.
13. Lu P, Sodhi CP, Jia H, Shaffiey S, Good M, Branca MF, Hackam DJ. Animal models of gastrointestinal and liver diseases. Animal models of necrotizing enterocolitis: pathophysiology, translational relevance, and challenges. Am J Physiol Gastrointest Liver Physiol 2014;306:G917-28.
14. Fallon EM, Nehra D, Potemkin AK, Gura KM, Simpser E, Compher C; American Society for Parenteral and Enteral Nutrition Board of D; Puder M. A.S.P.E.N. clinical guidelines: nutrition support of neonatal patients at risk for necrotizing enterocolitis. JPEN J Parenter Enteral Nutr 2012;36:506-23.
15. Meinzen-Derr J, Poindexter B, Wrage L, Morrow AL, Stoll B, Donovan EF. Role of human milk in extremely low birth weight infants' risk of necrotizing enterocolitis or death. J Perinatol 2009;29:57-62.
16. Quigley M, McGuire W. Formula versus donor breast milk for feeding preterm or low birth weight infants. Cochrane Database Syst Rev 2014;4:CD002971.
17. Boyd CA, Quigley MA, Brocklehurst P. Donor breast milk versus infant formula for preterm infants: systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed 2007;92:F169-75.
18. Nandhini LP, Biswal N, Adhisivam B, Mandal J, Bhat BV, Mathai B. Synbiotics for decreasing incidence of necrotizing enterocolitis among preterm neonates-a randomized controlled trial. J Matern Fetal Neonatal Med 2016;29:821-5.
19. Bell MJ, Ternberg JL, Feigin RD, Keating JP, Marshall R, Barton L, Brotherton T. Neonatal necrotizing enterocolitis: therapeutic decisions based upon clinical staging. Ann Surg 1978;187:1-7.
20. Guillet R, Stoll BJ, Cotten CM, Gantz M, McDonald S, Poole WK, Phelps DL; National Institute of Child Health and Human Development Neonatal Research Network. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006;117:e137-42.
21. Lin PW, Stoll BJ. Necrotising enterocolitis. Lancet 2006;368:1271-83.
22. Nanthakumar N, Meng D, Goldstein AM, Zhu W, Lu L, Uauy R, Llanos A, Claud EC, Walker WA. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response. PLoS One 2011;6:e17776.
23. Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S, Conway S. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 2004;5:104-12.
24. Collier-Hyams LS, Neish AS. Innate immune relationship between commensal flora and the mammalian intestinal epithelium. Cell Mol Life Sci 2005;62:1339-48.
25. Alexander VN, Northrup V, Bizzarro MJ. Antibiotic exposure in the newborn intensive care unit and the risk of necrotizing enterocolitis. J Pediatr 2011;159:392-7.
26. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, Antonopoulos DA, Chang EB, Claud EC. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 2009;3:944-54.
27. Normann E, Fahlen A, Engstrand L, Lilja HE. Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis. Acta Paediatr 2013;102:129-36.
28. Robinson J. Cochrane in context: probiotics for prevention of necrotizing enterocolitis in preterm infants. Evid Based Child Health 2014; 9:672-4.
29. Vongbhavit K, Underwood MA. Prevention of necrotizing enterocolitis through manipulation of the intestinal microbiota of the premature infant. Clin Ther 2016;38:716-32.
30. Sreenivasa B, Kumar PS, Suresh Babu MT, Ragavendra K. Role of synbiotics in the prevention of necrotizing enterocolitis in preterm neonates: a randomized controlled trial. Int J Contemp Pediatr. 2015;2: 127-30.
31. Soto A, Martin V, Jimenez E, Mader I, Rodriguez JM, Fernandez L. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr 2014;59:78-88.
32. Gregory KE, Walker WA. Immunologic factors in human milk and disease prevention in the preterm infant. Curr Pediatr Rep 2013;1: 1-19.
33. Levy O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 2007;7:379-90.
34. Nussbaum C, Sperandio M. Innate immune cell recruitment in the fetus and neonate. J Reprod Immunol 2011;90:74-81.
35. Castellote C, Casillas R, Ramirez-Santana C, Perez-Cano FJ, Castell M, Moretones MG, Lopez-Sabater MC, Franch A. Premature delivery influences the immunological composition of colostrum and transitional and mature human milk. J Nutr 2011;141:1181-7.
36. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 2006;177: 3273-82.
37. Leaphart CL, Cavallo J, Gribar SC, Cetin S, Li J, Branca MF, Dubowski TD, Sodhi CP, Hackam DJ. A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J Immunol 2007;179:4808-20.
38. Gribar SC, Sodhi CP, Richardson WM, Anand RJ, Gittes GK, Branca MF, Jakub A, Shi XH, Shah S, Ozolek JA, et al. Reciprocal expression and signaling of TLR4 and TLR9 in the pathogenesis and treatment of necrotizing enterocolitis. J Immunol 2009;182:636-46.
39. Dvorak B, Halpern MD, Holubec H, Williams CS, McWilliam DL, Dominguez JA, Stepankova R, Payne CM, McCuskey RS. Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am J Physiol Gastrointest Liver Physiol 2002;282:G156-64.
40. Good M, Siggers RH, Sodhi CP, Afrazi A, Alkhudari F, Egan CE, Neal MD, Yazji I, Jia H, Lin J, et al. Amniotic fluid inhibits Toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proc Natl Acad Sci USA 2012;109:11330-5.
41. Good M, Sodhi CP, Egan CE, Afrazi A, Jia H, Yamaguchi Y, Lu P, Branca MF, Ma CI. Breast milk protects against the development of necrotizing enterocolitis through inhibition of Toll-like receptor 4 in the intestinal epithelium via activation of the epidermal growth factor receptor. Mucosal Immunol 2015;8:1166-79.
42. Jain N, Walker WA. Diet and host-microbial crosstalk in postnatal intestinal immune homeostasis. Nat Rev Gastroenterol Hepatol 2015;12:14-25.
43. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012;129:434-40.
44. Smilowitz JT, O'Sullivan A, Barile D, German JB, Lonnerdal B, Slupsky CM. The human milk metabolome reveals diverse oligosaccharide profiles. J Nutr 2013;143:1709-18.
45. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 2012;22:1147-62.
46. Sela DA, Mills DA. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol 2010;18:298-307.
47. Garrido D, Ruiz-Moyano S, Lemay DG, Sela DA, German JB, Mills DA. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci Rep 2015;5:13517.
48. Gregory KE, WalkerWA. Immunologic factors in human milk and disease prevention in the preterm infant. Curr Pediatr Rep 2013;1(Suppl 4):1-11.
49. Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 2009;139:1619-25.
50. Newburg DS, Ruiz-Palacios GM, Morrow AL. Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 2005;25: 37-58.
51. Herrmann K, Carroll K. An exclusively human milk diet reduces necrotizing enterocolitis. Breastfeed Med 2014;9:184-90.
52. Kim J, Unger S. Human milk banking. Paediatr Child Health 2010;15: 595-602.
53. Underwood MA. Human milk for the premature infant. Pediatr Clin North Am 2013;60:189-207.
54. Ewaschuk JB, Unger S, Harvey S, O'Connor DL, Field CJ. Effect of pasteurization on immune components of milk: implications for feeding preterm infants. Appl Physiol Nutr Metab 2011;36:175-82.
55. Stock K, Griesmaier E, Brunner B, Neubauer V, Kiechl-Kohlendorfer U, Trawoger R. Pasteurization of breastmilk decreases the rate of postnatally acquired cytomegalovirus infections, but shows a nonsignificant trend to an increased rate of necrotizing enterocolitis in very preterm infants-a preliminary study. Breastfeed Med 2015;10:113-7.
56. Panczuk J, Unger S, O'Connor D, Lee SK. Human donor milk for the vulnerable infant: a Canadian perspective. Int Breastfeed J 2014;9:4.
57. Rochow N, Landau-Crangle E, Fusch C. Challenges in breast milk fortification for preterm infants. Curr Opin Clin Nutr Metab Care 2015; 18:276-84.
58. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, 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;11:506-14.
59. Sherman PM, Ossa JC, Johnson-Henry K. Unraveling mechanisms of action of probiotics. Nutr Clin Pract 2009;24:10-4.
60. Indrio F, Riezzo G, Raimondi F, Bisceglia M, Cavallo L, Francavilla R. The effects of probiotics on feeding tolerance, bowel habits, and gastrointestinal motility in preterm newborns. J Pediatr 2008;152:801-6.
61. Sütas Y, Soppi E, Korhonen H, Syvaoja EL, Saxelin M, Rokka T, Isolauri E. Suppression of lymphocyte proliferation in vitro by bovine caseins hydrolyzed with Lactobacillus casei GG-derived enzymes. J Allergy Clin Immunol 1996;98:216-24.
62. KunzeWA, Mao YK, Wang B, Huizinga JD, Ma X, Forsythe P, Bienenstock J. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med 2009;13:2261-70.
63. Verdú EF, Bercik P, Collins SM. Effect of probiotics on gastrointestinal function: evidence from animal models. Therap Adv Gastroenterol 2009;2:31-5.
64. Hunter C, Dimaguila MA, Gal P, Wimmer JE Jr., Ransom JL, Carlos RQ, Smith M, Davanzo CC. Effect of routine probiotic, Lactobacillus reuteri DSM 17938, use on rates of necrotizing enterocolitis in neonates with birthweight < 1000 grams: a sequential analysis. BMC Pediatr 2012;12:142.
65. Deshpande G, Rao S, Patole S, Bulsara M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 2010;125:921-30.
66. Wang Q, Dong J, Zhu Y. Probiotic supplement reduces risk of necrotizing enterocolitis and mortality in preterm very low-birth-weight infants: an updated meta-analysis of 20 randomized, controlled trials. J Pediatr Surg 2012;47:241-8.
67. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Evid Based Child Health 2014;9:584-671.
68. Baucells BJ, Mercadal Hally M, Alvarez Sanchez AT, Figueras Aloy J. [Probiotic associations in the prevention of necrotising enterocolitis and the reduction of late-onset sepsis and neonatal mortality in preterm infants under 1, 500g: a systematic review.] An Pediatr (Barc) 2015 (in English).
69. Ofek Shlomai N, Deshpande G, Rao S, Patole S. Probiotics for preterm neonates: what will it take to change clinical practice? Neonatology 2014;105:64-70.
70. Mihatsch WA, Braegger CP, Decsi T, Kolacek S, Lanzinger H, Mayer B, Moreno LA, Pohlandt F, Puntis J, Shamir R, et al. Critical systematic review of the level of evidence for routine use of probiotics for reduction of mortality and prevention of necrotizing enterocolitis and sepsis in preterm infants. Clin Nutr 2012;31:6-15.
71. Costeloe K, Hardy P, Juszczak E, Wilks M, Millar MR. Bifidobacterium breve BBG-001 in very preterm infants: a randomised controlled phase 3 trial. Lancet 2016;387:649-60.
72. Jacobs SE, Tobin JM, Opie GF, Donath S, Tabrizi SN, Pirotta M, Morley CJ, Garland SM. Probiotic effects on late-onset sepsis in very preterm infants: a randomized controlled trial. Pediatrics 2013;132:1055-62.
73. Bin-Nun A, Bromiker R, Wilschanski M, Kaplan M, Rudensky B, Caplan M, Hammerman C. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 2005;147:192-6.
74. Food and Drug Administration. Solgar Inc issues voluntary class I recall of ABC Dophilus Powder [cited 2016 Apr 20]. Available from: http://www.fda.gov/Safety/Recalls/ucm423219.htm.
75. Abrahamsson TR, Rautava S, Moore AM, Neu J, Sherman PM. The time for a confirmative necrotizing enterocolitis probiotics prevention trial in the extremely low birth weight infant in North America is now! J Pediatr 2014;165:389-94.
76. Zhu A, Sunagawa S, Mende DR, Bork P. Inter-individual differences in the gene content of human gut bacterial species. Genome Biol 2015; 16:82.
77. Gueimonde M, Collado MC. Metagenomics and probiotics. Clin Microbiol Infect 2012;18(Suppl 4):32-4.
78. Vandenplas Y, Zakharova I, Dmitrieva Y. Oligosaccharides in infant formula: more evidence to validate the role of prebiotics. Br J Nutr 2015;113:1339-44.
79. Johnson-Henry KC, Pinnell LJ, Waskow AM, Irrazabal T, Martin A, Hausner M, Sherman PM. Short-chain fructo-oligosaccharide and inulin modulate inflammatory responses and microbial communities in Caco2-bbe cells and in a mouse model of intestinal injury. J Nutr 2014;144:1725-33.
80. González R, Klaassens ES, Malinen E, de Vos WM, Vaughan EE. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl Environ Microbiol 2008;74:4686-94.
81. Veereman-Wauters G, Staelens S, Van de Broek H, Plaskie K, Wesling F, Roger LC, McCartney AL, Assam P. Physiological and bifidogenic effects of prebiotic supplements in infant formulae. J Pediatr Gastroenterol Nutr 2011;52:763-71.
82. Boehm G, Moro G. Structural and functional aspects of prebiotics used in infant nutrition. J Nutr 2008;138:1818S-28S.
83. Kapiki A, Costalos C, Oikonomidou C, Triantafyllidou A, Loukatou E, Pertrohilou V. The effect of a fructo-oligosaccharide supplemented formula on gut flora of preterm infants. Early Hum Dev 2007;83:335-9.
84. Knol J, Boehm G, Lidestri M, Negretti F, Jelinek J, Agosti M, Stahl B, Marini A, Mosca F. Increase of faecal bifidobacteria due to dietary oligosaccharides induces a reduction of clinically relevant pathogen germs in the faeces of formula-fed preterm infants. Acta Paediatr Suppl 2005;94:31-3.
85. Srinivasjois R, Rao S, Patole S. Prebiotic supplementation in preterm neonates: updated systematic review and meta-analysis of randomised controlled trials. Clin Nutr 2013;32:958-65.
86. Watson D, O'Connell Motherway M, Schoterman MH, van Neerven RJ, Nauta A, van Sinderen D. Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol 2013;114:1132-46.
87. Shoaf K, Mulvey GL, Armstrong GD, Hutkins RW. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect Immun 2006;74:6920-8.
88. Vogt LM, Meyer D, Pullens G, Faas MM, Venema K, Ramasamy U, Schols HA, de Vos P. Toll-like receptor 2 activation by beta2/1-fructans protects barrier function of T84 human intestinal epithelial cells in a chain length-dependent manner. J Nutr 2014;144:1002-8.
89. Akbari P, Braber S, Alizadeh A, Verheijden KA, Schoterman MH, Kraneveld AD, Garssen J, Fink-Gremmels J. Galacto-oligosaccharides protect the intestinal barrier by maintaining the tight junction network and modulating the inflammatory responses after a challenge with the mycotoxin deoxynivalenol in human Caco-2 cell monolayers and B6C3F1 mice. J Nutr 2015;145:1604-13.
90. Ortega-González M, Ocon B, Romero-Calvo I, Anzola A, Guadix E, Zarzuelo A, Suarez MD, Sanchez de Medina F, Martinez-Augustin O. Nondigestible oligosaccharides exert nonprebiotic effects on intestinal epithelial cells enhancing the immune response via activation of TLR4-NFkappaB. Mol Nutr Food Res 2014;58:384-93.
91. Vogt L, Meyer D, Pullens G, Faas M, Smelt M, Venema K, Ramasamy U, Schols HA, De Vos P. Immunological properties of inulin-type fructans. Crit Rev Food Sci Nutr 2015;55:414-36.
92. Dilli D, Aydin B, Fettah ND, Ozyazici E, Beken S, Zenciroglu A, Okumus N, Ozyurt BM, Ipek MS, Akdaq A, et al. The Propre-Save study: effects of probiotics and prebiotics alone or combined on necrotizing enterocolitis in very low birth weight infants. J Pediatr 2015;166:545-51, e1.
93. Armanian AM, Sadeghnia A, Hoseinzadeh M, Mirlohi M, Feizi A, Salehimehr N, Saee N, Nazari J. The effect of neutral oligosaccharides on reducing the incidence of necrotizing enterocolitis in preterm infants: a randomized clinical trial. Int J Prev Med 2014;5:1387-95.
94. Jantscher-Krenn E, Zherebtsov M, Nissan C, Goth K, Guner YS, Naidu N, Choudhury B, Grishin AV, Ford HR, Bode L. The human milk oligosaccharide disialyllacto-N-tetraose prevents necrotising enterocolitis in neonatal rats. Gut 2012;61:1417-25.
95. Marteau P, Seksik P. Tolerance of probiotics and prebiotics. J Clin Gastroenterol 2004;38:S67-9.
96. Kolida S, Gibson GR. Synbiotics in health and disease. Annu Rev Food Sci Technol 2011;2:373-93.
97. Bengmark S. Synbiotic in human medicine. In: Versalovic J, Wilson MD, editors. Therapeutic microbiology: probiotics and related strategies. Washington (DC): ASM Press; 2008. p. 307-21.
98. D'Souza A, Cai CL, Kumar D, Cai F, Fordjour L, Ahmad A, Valencia G, Aranda JV, Beharry KD. Cytokines and Toll-like receptor signaling pathways in the terminal ileum of hypoxic/hyperoxic neonatal rats: benefits of probiotics supplementation. Am J Transl Res 2012;4:187-97.
99. D'Souza A, Fordjour L, Ahmad A, Cai C, Kumar D, Valencia G, Aranda JV, Beharry KD. Effects of probiotics, prebiotics, and synbiotics on messenger RNA expression of caveolin-1, NOS, and genes regulating oxidative stress in the terminal ileum of formula-fed neonatal rats. Pediatr Res 2010;67:526-31.
100. Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 2010;7:503-14.
101. Kadlec R, Jakubec M. The effect of prebiotics on adherence of probiotics. J Dairy Sci 2014;97:1983-90.