Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy
Background: Oral immunotherapy (OIT) can ameliorate cow's milk allergy (CMA); however, the achievement of sustained unresponsiveness (SU) is challenging. Regarding the pathogenesis of CMA, recent studies have shown the importance of gut microbiota (Mb) and fecal water-soluble metabolites (WSMs)...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2024-01-01
|
Series: | Allergology International |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S1323893023001053 |
_version_ | 1797365556165214208 |
---|---|
author | Ryohei Shibata Naoka Itoh Yumiko Nakanishi Tamotsu Kato Wataru Suda Mizuho Nagao Tsutomu Iwata Hideo Yoshida Masahira Hattori Takao Fujisawa Naoki Shimojo Hiroshi Ohno |
author_facet | Ryohei Shibata Naoka Itoh Yumiko Nakanishi Tamotsu Kato Wataru Suda Mizuho Nagao Tsutomu Iwata Hideo Yoshida Masahira Hattori Takao Fujisawa Naoki Shimojo Hiroshi Ohno |
author_sort | Ryohei Shibata |
collection | DOAJ |
description | Background: Oral immunotherapy (OIT) can ameliorate cow's milk allergy (CMA); however, the achievement of sustained unresponsiveness (SU) is challenging. Regarding the pathogenesis of CMA, recent studies have shown the importance of gut microbiota (Mb) and fecal water-soluble metabolites (WSMs), which prompted us to determine the change in clinical and gut environmental factors important for acquiring SU after OIT for CMA. Methods: We conducted an ancillary cohort study of a multicenter randomized, parallel-group, delayed-start design study on 32 school-age children with IgE-mediated CMA who underwent OIT for 13 months. We defined SU as the ability to consume cow's milk exceeding the target dose in a double-blind placebo-controlled food challenge after OIT followed by a 2-week-avoidance. We longitudinally collected 175 fecal specimens and clustered the microbiome and metabolome data into 29 Mb- and 12 WSM-modules. Results: During OIT, immunological factors improved in all participants. However, of the 32 participants, 4 withdrew because of adverse events, and only 7 were judged SU. Gut environmental factors shifted during OIT, but only in the beginning, and returned to the baseline at the end. Of these factors, milk- and casein-specific IgE and the Bifidobacterium-dominant module were associated with SU (milk- and casein-specific IgE; OR for 10 kUA/L increments, 0.67 and 0.66; 95%CI, 0.41–0.93 and 0.42–0.90; Bifidobacterium-dominant module; OR for 0.01 increments, 1.40; 95%CI, 1.10–2.03), and these associations were observed until the end of OIT. Conclusions: In this study, we identified the clinical and gut environmental factors associated with SU acquisition in CM-OIT. |
first_indexed | 2024-03-08T16:51:38Z |
format | Article |
id | doaj.art-0abd1b7c42d14a21bffc32327a19b1ff |
institution | Directory Open Access Journal |
issn | 1323-8930 |
language | English |
last_indexed | 2024-03-08T16:51:38Z |
publishDate | 2024-01-01 |
publisher | Elsevier |
record_format | Article |
series | Allergology International |
spelling | doaj.art-0abd1b7c42d14a21bffc32327a19b1ff2024-01-05T04:23:51ZengElsevierAllergology International1323-89302024-01-01731126136Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergyRyohei Shibata0Naoka Itoh1Yumiko Nakanishi2Tamotsu Kato3Wataru Suda4Mizuho Nagao5Tsutomu Iwata6Hideo Yoshida7Masahira Hattori8Takao Fujisawa9Naoki Shimojo10Hiroshi Ohno11Laboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Immunobiology Laboratory, Graduate School of Medical Life Science, Yokohama City University, Kanagawa, Japan; Department of Pediatric Surgery, Graduate School of Medicine, Chiba University, Chiba, JapanDepartment of Pediatrics, National Hospital Organization Kanagawa National Hospital, Kanagawa, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Immunobiology Laboratory, Graduate School of Medical Life Science, Yokohama City University, Kanagawa, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Immunobiology Laboratory, Graduate School of Medical Life Science, Yokohama City University, Kanagawa, JapanLaboratory for Microbiome Sciences, RIKEN Center for Integrative Medical Sciences, Kanagawa, JapanAllergy Center, National Hospital Organization Mie National Hospital, Mie, JapanThe Graduate School of Tokyo Kasei University, Saitama, JapanDepartment of Pediatric Surgery, Graduate School of Medicine, Chiba University, Chiba, JapanLaboratory for Microbiome Sciences, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Graduate School of Advanced Science and Engineering, Waseda University, Tokyo, JapanAllergy Center, National Hospital Organization Mie National Hospital, Mie, JapanCenter for Preventive Medical Sciences, Chiba University, Chiba, JapanLaboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Immunobiology Laboratory, Graduate School of Medical Life Science, Yokohama City University, Kanagawa, Japan; Laboratory for Microbiome Sciences, RIKEN Center for Integrative Medical Sciences, Kanagawa, Japan; Corresponding author. Laboratory for Intestinal Ecosystem, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa 230-0045, Japan.Background: Oral immunotherapy (OIT) can ameliorate cow's milk allergy (CMA); however, the achievement of sustained unresponsiveness (SU) is challenging. Regarding the pathogenesis of CMA, recent studies have shown the importance of gut microbiota (Mb) and fecal water-soluble metabolites (WSMs), which prompted us to determine the change in clinical and gut environmental factors important for acquiring SU after OIT for CMA. Methods: We conducted an ancillary cohort study of a multicenter randomized, parallel-group, delayed-start design study on 32 school-age children with IgE-mediated CMA who underwent OIT for 13 months. We defined SU as the ability to consume cow's milk exceeding the target dose in a double-blind placebo-controlled food challenge after OIT followed by a 2-week-avoidance. We longitudinally collected 175 fecal specimens and clustered the microbiome and metabolome data into 29 Mb- and 12 WSM-modules. Results: During OIT, immunological factors improved in all participants. However, of the 32 participants, 4 withdrew because of adverse events, and only 7 were judged SU. Gut environmental factors shifted during OIT, but only in the beginning, and returned to the baseline at the end. Of these factors, milk- and casein-specific IgE and the Bifidobacterium-dominant module were associated with SU (milk- and casein-specific IgE; OR for 10 kUA/L increments, 0.67 and 0.66; 95%CI, 0.41–0.93 and 0.42–0.90; Bifidobacterium-dominant module; OR for 0.01 increments, 1.40; 95%CI, 1.10–2.03), and these associations were observed until the end of OIT. Conclusions: In this study, we identified the clinical and gut environmental factors associated with SU acquisition in CM-OIT.http://www.sciencedirect.com/science/article/pii/S1323893023001053Casein-specific IgECow's milk allergyFecal metabolitesGut microbiotaOral immunotherapy |
spellingShingle | Ryohei Shibata Naoka Itoh Yumiko Nakanishi Tamotsu Kato Wataru Suda Mizuho Nagao Tsutomu Iwata Hideo Yoshida Masahira Hattori Takao Fujisawa Naoki Shimojo Hiroshi Ohno Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy Allergology International Casein-specific IgE Cow's milk allergy Fecal metabolites Gut microbiota Oral immunotherapy |
title | Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy |
title_full | Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy |
title_fullStr | Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy |
title_full_unstemmed | Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy |
title_short | Gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school-age children with cow's milk allergy |
title_sort | gut microbiota and fecal metabolites in sustained unresponsiveness by oral immunotherapy in school age children with cow s milk allergy |
topic | Casein-specific IgE Cow's milk allergy Fecal metabolites Gut microbiota Oral immunotherapy |
url | http://www.sciencedirect.com/science/article/pii/S1323893023001053 |
work_keys_str_mv | AT ryoheishibata gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT naokaitoh gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT yumikonakanishi gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT tamotsukato gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT watarusuda gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT mizuhonagao gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT tsutomuiwata gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT hideoyoshida gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT masahirahattori gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT takaofujisawa gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT naokishimojo gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy AT hiroshiohno gutmicrobiotaandfecalmetabolitesinsustainedunresponsivenessbyoralimmunotherapyinschoolagechildrenwithcowsmilkallergy |