Skip to main content
Top
Published in: Clinical and Translational Allergy 1/2019

Open Access 01-12-2019 | Respiratory Microbiota | Research

A specific synbiotic-containing amino acid-based formula restores gut microbiota in non-IgE mediated cow’s milk allergic infants: a randomized controlled trial

Authors: Harm Wopereis, Marleen T. J. van Ampting, Aysun Cetinyurek-Yavuz, Rob Slump, David C. A. Candy, Assad M. Butt, Diego G. Peroni, Yvan Vandenplas, Adam T. Fox, Neil Shah, Guus Roeselers, Lucien F. Harthoorn, Louise J. Michaelis, Jan Knol, Christina E. West, the ASSIGN study group

Published in: Clinical and Translational Allergy | Issue 1/2019

Login to get access

Abstract

Background

Altered gut microbiota is implicated in cow’s milk allergy (CMA) and differs markedly from healthy, breastfed infants. Infants who suffer from severe CMA often rely on cow’s milk protein avoidance and, when breastfeeding is not possible, on specialised infant formulas such as amino-acid based formulas (AAF). Herein, we report the effects of an AAF including specific synbiotics on oral and gastrointestinal microbiota of infants with non-IgE mediated CMA with reference to healthy, breastfed infants.

Methods

In this prospective, randomized, double-blind controlled study, infants with suspected non-IgE mediated CMA received test or control formula. Test formula was AAF with synbiotics (prebiotic fructo-oligosaccharides and probiotic Bifidobacterium breve M-16V). Control formula was AAF without synbiotics. Healthy, breastfed infants were used as a separate reference group (HBR). Bacterial compositions of faecal and salivary samples were analysed by 16S rRNA-gene sequencing. Faecal analysis was complemented with the analysis of pH, short-chain fatty acids (SCFAs) and lactic acids.

Results

The trial included 35 test subjects, 36 controls, and 51 HBR. The 16S rRNA-gene sequencing revealed moderate effects of test formula on oral microbiota. In contrast, the gut microbiota was substantially affected across time comparing test with control. In both groups bacterial diversity increased over time but was characterised by a more gradual increment in test compared to control. Compositionally this reflected an enhancement of Bifidobacterium spp. and Veillonella sp. in the test group. In contrast, the control-fed infants showed increased abundance of adult-like species, mainly within the Lachnospiraceae family, as well as within the Ruminococcus and Alistipes genus. The effects on Bifidobacterium spp. and Lachnospiraceae spp. were previously confirmed through enumeration by fluorescent in situ hybridization and were shown for test to approximate the proportions observed in the HBR. Additionally, microbial activity was affected as evidenced by an increase of l-lactate, a decrease of valerate, and reduced concentrations of branched-chain SCFAs in test versus control.

Conclusions

The AAF including specific synbiotics effectively modulates the gut microbiota and its metabolic activity in non-IgE mediated CMA infants bringing it close to a healthy breastfed profile.
Trial registration Registered on 1 May 2013 with Netherlands Trial Register Number NTR3979.
Literature
1.
go back to reference Robbins KA, Wood RA, Keet C. Persistent cow’s milk allergy is associated with decreased growth: a longitudinal study. J Allergy Clin Immunol. 2018;141(2):AB150.CrossRef Robbins KA, Wood RA, Keet C. Persistent cow’s milk allergy is associated with decreased growth: a longitudinal study. J Allergy Clin Immunol. 2018;141(2):AB150.CrossRef
2.
go back to reference Tran MM, Lefebvre DL, Dharma C, Dai D, Lou WYW, Subbarao P, et al. Predicting the atopic March: results from the Canadian Healthy Infant Longitudinal Development Study. J Allergy Clin Immunol. 2018;141(2):601e8–607e8.CrossRef Tran MM, Lefebvre DL, Dharma C, Dai D, Lou WYW, Subbarao P, et al. Predicting the atopic March: results from the Canadian Healthy Infant Longitudinal Development Study. J Allergy Clin Immunol. 2018;141(2):601e8–607e8.CrossRef
3.
go back to reference West CE, Ryden P, Lundin D, Engstrand L, Tulic MK, Prescott SL. Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin Exp Allergy. 2015;45(9):1419–29.CrossRef West CE, Ryden P, Lundin D, Engstrand L, Tulic MK, Prescott SL. Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin Exp Allergy. 2015;45(9):1419–29.CrossRef
4.
go back to reference Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22(10):1187–91.CrossRef Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22(10):1187–91.CrossRef
5.
go back to reference Huang YJ, Marsland BJ, Bunyavanich S, O’Mahony L, Leung DY, Muraro A, et al. The microbiome in allergic disease: current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J Allergy Clin Immunol. 2017;139(4):1099–110.CrossRef Huang YJ, Marsland BJ, Bunyavanich S, O’Mahony L, Leung DY, Muraro A, et al. The microbiome in allergic disease: current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J Allergy Clin Immunol. 2017;139(4):1099–110.CrossRef
6.
go back to reference Bunyavanich S, Shen N, Grishin A, Wood R, Burks W, Dawson P, et al. Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol. 2016;138(4):1122–30.CrossRef Bunyavanich S, Shen N, Grishin A, Wood R, Burks W, Dawson P, et al. Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol. 2016;138(4):1122–30.CrossRef
7.
go back to reference Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, et al. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol. 2014;80(9):2889–900.CrossRef Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, et al. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol. 2014;80(9):2889–900.CrossRef
8.
go back to reference Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703.CrossRef Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703.CrossRef
9.
go back to reference Fiocchi A, Dahda L, Dupont C, Campoy C, Fierro V, Nieto A. Cow’s milk allergy: towards an update of DRACMA guidelines. World Allergy Organ J. 2016;9(1):35.CrossRef Fiocchi A, Dahda L, Dupont C, Campoy C, Fierro V, Nieto A. Cow’s milk allergy: towards an update of DRACMA guidelines. World Allergy Organ J. 2016;9(1):35.CrossRef
10.
go back to reference Al-Shehri SS, Sweeney EL, Cowley DM, Liley HG, Ranasinghe PD, Charles BG, et al. Deep sequencing of the 16S ribosomal RNA of the neonatal oral microbiome: a comparison of breast-fed and formula-fed infants. Sci Rep. 2016;6:38309.CrossRef Al-Shehri SS, Sweeney EL, Cowley DM, Liley HG, Ranasinghe PD, Charles BG, et al. Deep sequencing of the 16S ribosomal RNA of the neonatal oral microbiome: a comparison of breast-fed and formula-fed infants. Sci Rep. 2016;6:38309.CrossRef
11.
go back to reference Timby N, Domellof M, Holgerson PL, West CE, Lonnerdal B, Hernell O, et al. Oral microbiota in infants fed a formula supplemented with bovine milk fat globule membranes—a randomized controlled trial. PLoS ONE. 2017;12(1):e0169831.CrossRef Timby N, Domellof M, Holgerson PL, West CE, Lonnerdal B, Hernell O, et al. Oral microbiota in infants fed a formula supplemented with bovine milk fat globule membranes—a randomized controlled trial. PLoS ONE. 2017;12(1):e0169831.CrossRef
12.
go back to reference Venter C, Brown T, Meyer R, Walsh J, Shah N, Nowak-Wegrzyn A, et al. Better recognition, diagnosis and management of non-IgE-mediated cow’s milk allergy in infancy: iMAP-an international interpretation of the MAP (Milk Allergy in Primary Care) guideline. Clin Transl Allergy. 2017;7(1):26.CrossRef Venter C, Brown T, Meyer R, Walsh J, Shah N, Nowak-Wegrzyn A, et al. Better recognition, diagnosis and management of non-IgE-mediated cow’s milk allergy in infancy: iMAP-an international interpretation of the MAP (Milk Allergy in Primary Care) guideline. Clin Transl Allergy. 2017;7(1):26.CrossRef
13.
go back to reference Harvey BM, Langford JE, Harthoorn LF, Gillman SA, Green TD, Schwartz RH, et al. Effects on growth and tolerance and hypoallergenicity of an amino acid-based formula with synbiotics. Pediatr Res. 2014;75(2):343–51.CrossRef Harvey BM, Langford JE, Harthoorn LF, Gillman SA, Green TD, Schwartz RH, et al. Effects on growth and tolerance and hypoallergenicity of an amino acid-based formula with synbiotics. Pediatr Res. 2014;75(2):343–51.CrossRef
14.
go back to reference Burks AW, Harthoorn LF, Van Ampting MT, Oude Nijhuis MM, Langford JE, Wopereis H, et al. Synbiotics-supplemented amino acid-based formula supports adequate growth in cow’s milk allergic infants. Pediatr Allergy Immunol. 2015;26(4):316–22.CrossRef Burks AW, Harthoorn LF, Van Ampting MT, Oude Nijhuis MM, Langford JE, Wopereis H, et al. Synbiotics-supplemented amino acid-based formula supports adequate growth in cow’s milk allergic infants. Pediatr Allergy Immunol. 2015;26(4):316–22.CrossRef
15.
go back to reference Candy DCA, Van Ampting MTJ, Oude Nijhuis MM, Wopereis H, Butt AM, Peroni DG, et al. A synbiotic-containing amino-acid-based formula improves gut microbiota in non-IgE-mediated allergic infants. Pediatr Res. 2018;83(3):677–86.CrossRef Candy DCA, Van Ampting MTJ, Oude Nijhuis MM, Wopereis H, Butt AM, Peroni DG, et al. A synbiotic-containing amino-acid-based formula improves gut microbiota in non-IgE-mediated allergic infants. Pediatr Res. 2018;83(3):677–86.CrossRef
16.
go back to reference Fox AT, Wopereis H, Van Ampting MTJ, Oude Nijhuis MM, Butt AM, Peroni DG, et al. A specific synbiotic-containing amino acid-based formula in dietary management of cow’s milk allergy: a randomized controlled trial. Clin Transl Allergy. 2019;9(1):5.CrossRef Fox AT, Wopereis H, Van Ampting MTJ, Oude Nijhuis MM, Butt AM, Peroni DG, et al. A specific synbiotic-containing amino acid-based formula in dietary management of cow’s milk allergy: a randomized controlled trial. Clin Transl Allergy. 2019;9(1):5.CrossRef
17.
go back to reference Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998;64(9):3336–45.PubMedPubMedCentral Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol. 1998;64(9):3336–45.PubMedPubMedCentral
18.
go back to reference Sim K, Cox MJ, Wopereis H, Martin R, Knol J, Li MS, et al. Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS ONE. 2012;7(3):e32543.CrossRef Sim K, Cox MJ, Wopereis H, Martin R, Knol J, Li MS, et al. Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS ONE. 2012;7(3):e32543.CrossRef
19.
go back to reference Mischke M, Arora T, Tims S, Engels E, Sommer N, van Limpt K, et al. Specific synbiotics in early life protect against diet-induced obesity in adult mice. Diabetes Obes Metab. 2018;20(6):1408–18.CrossRef Mischke M, Arora T, Tims S, Engels E, Sommer N, van Limpt K, et al. Specific synbiotics in early life protect against diet-induced obesity in adult mice. Diabetes Obes Metab. 2018;20(6):1408–18.CrossRef
20.
go back to reference Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41(1):e1.CrossRef Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41(1):e1.CrossRef
21.
go back to reference Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.CrossRef Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.CrossRef
22.
go back to reference Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30(5):614–20.CrossRef Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30(5):614–20.CrossRef
23.
go back to reference Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.CrossRef Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.CrossRef
24.
go back to reference Rognes T, Flouri T, Nichols B, Quince C, Mahe F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.CrossRef Rognes T, Flouri T, Nichols B, Quince C, Mahe F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.CrossRef
25.
go back to reference Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011;21(3):494–504.CrossRef Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011;21(3):494–504.CrossRef
26.
go back to reference Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261–7.CrossRef Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261–7.CrossRef
27.
go back to reference Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96.CrossRef Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188–96.CrossRef
28.
go back to reference Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26(2):266–7.CrossRef Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26(2):266–7.CrossRef
29.
go back to reference Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26(7):1641–50.CrossRef Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26(7):1641–50.CrossRef
30.
go back to reference Faith DP, Baker AM. Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges. Evol Bioinform Online. 2007;2:121–8.PubMedPubMedCentral Faith DP, Baker AM. Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges. Evol Bioinform Online. 2007;2:121–8.PubMedPubMedCentral
31.
go back to reference Shannon CE. A mathematical theory of communication (parts I and II). Bell Syst Tech J. 1948;27:379–423.CrossRef Shannon CE. A mathematical theory of communication (parts I and II). Bell Syst Tech J. 1948;27:379–423.CrossRef
32.
go back to reference Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 2015;9(4):968–79.CrossRef Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J. 2015;9(4):968–79.CrossRef
33.
go back to reference Wopereis H, Sim K, Shaw A, Warner JO, Knol J, Kroll JS. Intestinal microbiota in infants at high risk for allergy: effects of prebiotics and role in eczema development. J Allergy Clin Immunol. 2018;141(4):1334e5–1342e5.CrossRef Wopereis H, Sim K, Shaw A, Warner JO, Knol J, Kroll JS. Intestinal microbiota in infants at high risk for allergy: effects of prebiotics and role in eczema development. J Allergy Clin Immunol. 2018;141(4):1334e5–1342e5.CrossRef
34.
go back to reference Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, et al. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol. 1995;61(8):3069–75.PubMedPubMedCentral Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, et al. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol. 1995;61(8):3069–75.PubMedPubMedCentral
35.
go back to reference Satokari RM, Vaughan EE, Akkermans AD, Saarela M, De Vos WM. Polymerase chain reaction and denaturing gradient gel electrophoresis monitoring of fecal Bifidobacterium populations in a prebiotic and probiotic feeding trial. Syst Appl Microbiol. 2001;24(2):227–31.CrossRef Satokari RM, Vaughan EE, Akkermans AD, Saarela M, De Vos WM. Polymerase chain reaction and denaturing gradient gel electrophoresis monitoring of fecal Bifidobacterium populations in a prebiotic and probiotic feeding trial. Syst Appl Microbiol. 2001;24(2):227–31.CrossRef
37.
go back to reference Wagner BD, Robertson CE, Harris JK. Application of two-part statistics for comparison of sequence variant counts. PLoS ONE. 2011;6(5):e20296.CrossRef Wagner BD, Robertson CE, Harris JK. Application of two-part statistics for comparison of sequence variant counts. PLoS ONE. 2011;6(5):e20296.CrossRef
38.
go back to reference Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol). 1995;57(1):289–300. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol). 1995;57(1):289–300.
39.
go back to reference Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7.CrossRef Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7.CrossRef
40.
go back to reference Van den Brink PJ, Braak CJFT. Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem. 1999;18(2):138–48.CrossRef Van den Brink PJ, Braak CJFT. Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem. 1999;18(2):138–48.CrossRef
41.
go back to reference Laursen MF, Andersen LBB, Michaelsen KF, Mølgaard C, Trolle E, Bahl MI, et al. Infant gut microbiota development is driven by transition to family foods independent of maternal obesity. mSphere. 2016;1(1):e00069.CrossRef Laursen MF, Andersen LBB, Michaelsen KF, Mølgaard C, Trolle E, Bahl MI, et al. Infant gut microbiota development is driven by transition to family foods independent of maternal obesity. mSphere. 2016;1(1):e00069.CrossRef
42.
go back to reference Thompson AL, Monteagudo-Mera A, Cadenas MB, Lampl ML, Azcarate-Peril MA. Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome. Front Cell Infect Microbiol. 2015;5:3.CrossRef Thompson AL, Monteagudo-Mera A, Cadenas MB, Lampl ML, Azcarate-Peril MA. Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome. Front Cell Infect Microbiol. 2015;5:3.CrossRef
43.
go back to reference Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CCGM, Troost FJ, et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 2012;6(7):1415–26.CrossRef Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CCGM, Troost FJ, et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 2012;6(7):1415–26.CrossRef
44.
go back to reference Rasmussen HS, Holtug K, Mortensen PB. Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scand J Gastroenterol. 1988;23(2):178–82.CrossRef Rasmussen HS, Holtug K, Mortensen PB. Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scand J Gastroenterol. 1988;23(2):178–82.CrossRef
45.
go back to reference Macfarlane GT, Cummings JH, Allison C. Protein degradation by human intestinal bacteria. J Gen Microbiol. 1986;132(6):1647–56.PubMed Macfarlane GT, Cummings JH, Allison C. Protein degradation by human intestinal bacteria. J Gen Microbiol. 1986;132(6):1647–56.PubMed
46.
go back to reference Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062–72.CrossRef Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr. 2011;93(5):1062–72.CrossRef
47.
go back to reference Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52–60.CrossRef Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52–60.CrossRef
48.
go back to reference Thompson-Chagoyan OC, Fallani M, Maldonado J, Vieites JM, Khanna S, Edwards C, et al. Faecal microbiota and short-chain fatty acid levels in faeces from infants with cow’s milk protein allergy. Int Arch Allergy Immunol. 2011;156(3):325–32.CrossRef Thompson-Chagoyan OC, Fallani M, Maldonado J, Vieites JM, Khanna S, Edwards C, et al. Faecal microbiota and short-chain fatty acid levels in faeces from infants with cow’s milk protein allergy. Int Arch Allergy Immunol. 2011;156(3):325–32.CrossRef
49.
go back to reference Berni Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, et al. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2016;10(3):742–50.CrossRef Berni Canani R, Sangwan N, Stefka AT, Nocerino R, Paparo L, Aitoro R, et al. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2016;10(3):742–50.CrossRef
50.
go back to reference Guo L, Bai H, Dong Y, Huang DX, Zhang X, Gong S, et al. Comparative analysis of fecal microbiota in 5–8-year-old children with and without cow milk protein allergy. Iran J Pediatr. 2016;139:e6397. Guo L, Bai H, Dong Y, Huang DX, Zhang X, Gong S, et al. Comparative analysis of fecal microbiota in 5–8-year-old children with and without cow milk protein allergy. Iran J Pediatr. 2016;139:e6397.
51.
go back to reference Dong P, Feng J-J, Yan D-Y, Lyu Y-J, Xu X. Early-life gut microbiome and cow’s milk allergy—a prospective case–control 6-month follow-up study. Saudi J Biol Sci. 2017;138:1122–30. Dong P, Feng J-J, Yan D-Y, Lyu Y-J, Xu X. Early-life gut microbiome and cow’s milk allergy—a prospective case–control 6-month follow-up study. Saudi J Biol Sci. 2017;138:1122–30.
52.
go back to reference Thompson-Chagoyan OC, Vieites JM, Maldonado J, Edwards C, Gil A. Changes in faecal microbiota of infants with cow’s milk protein allergy—a Spanish prospective case–control 6-month follow-up study. Pediatr Allergy Immunol. 2010;21(2 Pt 2):e394–400.CrossRef Thompson-Chagoyan OC, Vieites JM, Maldonado J, Edwards C, Gil A. Changes in faecal microbiota of infants with cow’s milk protein allergy—a Spanish prospective case–control 6-month follow-up study. Pediatr Allergy Immunol. 2010;21(2 Pt 2):e394–400.CrossRef
Metadata
Title
A specific synbiotic-containing amino acid-based formula restores gut microbiota in non-IgE mediated cow’s milk allergic infants: a randomized controlled trial
Authors
Harm Wopereis
Marleen T. J. van Ampting
Aysun Cetinyurek-Yavuz
Rob Slump
David C. A. Candy
Assad M. Butt
Diego G. Peroni
Yvan Vandenplas
Adam T. Fox
Neil Shah
Guus Roeselers
Lucien F. Harthoorn
Louise J. Michaelis
Jan Knol
Christina E. West
the ASSIGN study group
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Clinical and Translational Allergy / Issue 1/2019
Electronic ISSN: 2045-7022
DOI
https://doi.org/10.1186/s13601-019-0267-6

Other articles of this Issue 1/2019

Clinical and Translational Allergy 1/2019 Go to the issue