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Integrated gut metabolome and microbiome fingerprinting reveals that dysbiosis precedes allergic inflammation in IgE-mediated pediatric cow's milk allergy

Ellen De Paepe (UGent) , Vera Plekhova (UGent) , Pablo Vangeenderhuysen (UGent) , Nele Baeck, Dominique Bullens, Tania Claeys, Marilyn De Graeve (UGent) , Kristien Kamoen, Anneleen Notebaert, Tom Van de Wiele (UGent) , et al.
(2024) ALLERGY. 79(4). p.949-963
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Abstract
Background: IgE-mediated cow's milk allergy (IgE-CMA) is one of the first allergies to arise in early childhood and may result from exposure to various milk allergens, of which beta-lactoglobulin (BLG) and casein are the most important. Understanding the underlying mechanisms behind IgE-CMA is imperative for the discovery of novel biomarkers and the design of innovative treatment and prevention strategies.Methods: We report a longitudinal in vivo murine model, in which two mice strains (BALB/c and C57Bl/6) were sensitized to BLG using either cholera toxin or an oil emulsion (n = 6 per group). After sensitization, mice were challenged orally, their clinical signs monitored, antibody (IgE and IgG1) and cytokine levels (IL-4 and IFN-gamma) measured, and fecal samples subjected to metabolomics. The results of the murine models were further extrapolated to fecal microbiome-metabolome data from our population of IgE-CMA (n = 22) and healthy (n = 23) children (Trial: NCT04249973), on which polar metabolomics, lipidomics and 16S rRNA metasequencing were performed. In vitro gastrointestinal digestions and multi-omics corroborated the microbial origin of proposed metabolic changes.Results: During mice sensitization, we observed multiple microbially derived metabolic alterations, most importantly bile acid, energy and tryptophan metabolites, that preceded allergic inflammation. We confirmed microbial dysbiosis, and its associated effect on metabolic alterations in our patient cohort, through in vitro digestions and multi-omics, which was accompanied by metabolic signatures of low-grade inflammation.Conclusion: Our results indicate that gut dysbiosis precedes allergic inflammation and nurtures a chronic low-grade inflammation in children on elimination diets, opening important new opportunities for future prevention and treatment strategies.
Keywords
multi-omics, metabolomics, cow's milk allergy, 16S rRNA sequencing

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MLA
De Paepe, Ellen, et al. “Integrated Gut Metabolome and Microbiome Fingerprinting Reveals That Dysbiosis Precedes Allergic Inflammation in IgE-Mediated Pediatric Cow’s Milk Allergy.” ALLERGY, vol. 79, no. 4, 2024, pp. 949–63, doi:10.1111/all.16005.
APA
De Paepe, E., Plekhova, V., Vangeenderhuysen, P., Baeck, N., Bullens, D., Claeys, T., … Vanhaecke, L. (2024). Integrated gut metabolome and microbiome fingerprinting reveals that dysbiosis precedes allergic inflammation in IgE-mediated pediatric cow’s milk allergy. ALLERGY, 79(4), 949–963. https://doi.org/10.1111/all.16005
Chicago author-date
De Paepe, Ellen, Vera Plekhova, Pablo Vangeenderhuysen, Nele Baeck, Dominique Bullens, Tania Claeys, Marilyn De Graeve, et al. 2024. “Integrated Gut Metabolome and Microbiome Fingerprinting Reveals That Dysbiosis Precedes Allergic Inflammation in IgE-Mediated Pediatric Cow’s Milk Allergy.” ALLERGY 79 (4): 949–63. https://doi.org/10.1111/all.16005.
Chicago author-date (all authors)
De Paepe, Ellen, Vera Plekhova, Pablo Vangeenderhuysen, Nele Baeck, Dominique Bullens, Tania Claeys, Marilyn De Graeve, Kristien Kamoen, Anneleen Notebaert, Tom Van de Wiele, Wim Van Den Broeck, Koen Vanlede, Myriam Van Winckel, Lars Vereecke, Chris Elliott, Eric Cox, and Lynn Vanhaecke. 2024. “Integrated Gut Metabolome and Microbiome Fingerprinting Reveals That Dysbiosis Precedes Allergic Inflammation in IgE-Mediated Pediatric Cow’s Milk Allergy.” ALLERGY 79 (4): 949–963. doi:10.1111/all.16005.
Vancouver
1.
De Paepe E, Plekhova V, Vangeenderhuysen P, Baeck N, Bullens D, Claeys T, et al. Integrated gut metabolome and microbiome fingerprinting reveals that dysbiosis precedes allergic inflammation in IgE-mediated pediatric cow’s milk allergy. ALLERGY. 2024;79(4):949–63.
IEEE
[1]
E. De Paepe et al., “Integrated gut metabolome and microbiome fingerprinting reveals that dysbiosis precedes allergic inflammation in IgE-mediated pediatric cow’s milk allergy,” ALLERGY, vol. 79, no. 4, pp. 949–963, 2024.
@article{01HREHE7B1FQ4VYA0NDDE75SDG,
  abstract     = {{Background: IgE-mediated cow's milk allergy (IgE-CMA) is one of the first allergies to arise in early childhood and may result from exposure to various milk allergens, of which beta-lactoglobulin (BLG) and casein are the most important. Understanding the underlying mechanisms behind IgE-CMA is imperative for the discovery of novel biomarkers and the design of innovative treatment and prevention strategies.Methods: We report a longitudinal in vivo murine model, in which two mice strains (BALB/c and C57Bl/6) were sensitized to BLG using either cholera toxin or an oil emulsion (n = 6 per group). After sensitization, mice were challenged orally, their clinical signs monitored, antibody (IgE and IgG1) and cytokine levels (IL-4 and IFN-gamma) measured, and fecal samples subjected to metabolomics. The results of the murine models were further extrapolated to fecal microbiome-metabolome data from our population of IgE-CMA (n = 22) and healthy (n = 23) children (Trial: NCT04249973), on which polar metabolomics, lipidomics and 16S rRNA metasequencing were performed. In vitro gastrointestinal digestions and multi-omics corroborated the microbial origin of proposed metabolic changes.Results: During mice sensitization, we observed multiple microbially derived metabolic alterations, most importantly bile acid, energy and tryptophan metabolites, that preceded allergic inflammation. We confirmed microbial dysbiosis, and its associated effect on metabolic alterations in our patient cohort, through in vitro digestions and multi-omics, which was accompanied by metabolic signatures of low-grade inflammation.Conclusion: Our results indicate that gut dysbiosis precedes allergic inflammation and nurtures a chronic low-grade inflammation in children on elimination diets, opening important new opportunities for future prevention and treatment strategies.}},
  author       = {{De Paepe, Ellen and Plekhova, Vera and Vangeenderhuysen, Pablo and Baeck, Nele and Bullens, Dominique and Claeys, Tania and De Graeve, Marilyn and Kamoen, Kristien and Notebaert, Anneleen and Van de Wiele, Tom and Van Den Broeck, Wim and Vanlede, Koen and Van Winckel, Myriam and Vereecke, Lars and Elliott, Chris and Cox, Eric and Vanhaecke, Lynn}},
  issn         = {{0105-4538}},
  journal      = {{ALLERGY}},
  keywords     = {{multi-omics,metabolomics,cow's milk allergy,16S rRNA sequencing}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{949--963}},
  title        = {{Integrated gut metabolome and microbiome fingerprinting reveals that dysbiosis precedes allergic inflammation in IgE-mediated pediatric cow's milk allergy}},
  url          = {{http://doi.org/10.1111/all.16005}},
  volume       = {{79}},
  year         = {{2024}},
}
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