Integrative analysis of the intestinal metabolome of childhood asthma
The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology. We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthm...
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| Published in | Journal of allergy and clinical immunology Vol. 144; no. 2; pp. 442 - 454 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.08.2019
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2019.02.032 |
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| Abstract | The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.
We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial.
Metabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other “omics”: the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires.
Several intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = −6.3; 95% CI, −11.3 to −1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites.
Integrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies.
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| AbstractList | The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.
We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial.
Metabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other “omics”: the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires.
Several intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = −6.3; 95% CI, −11.3 to −1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites.
Integrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies.
[Display omitted] Intestinal metabolites, including immune-modulating lipids, are associated with childhood asthma. Specific bacterial taxa, plasma metabolites and dietary factors, including lack of breastfeeding and meat intake, correlate with asthma-associated metabolites. The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology. We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial. Metabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other "omics": the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires. Several intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = -6.3; 95% CI, -11.3 to -1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites. Integrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies. BackgroundThe intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.ObjectiveWe sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial.MethodsMetabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other “omics”: the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires.ResultsSeveral intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = −6.3; 95% CI, −11.3 to −1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites.ConclusionIntegrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies. The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.BACKGROUNDThe intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.We sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial.OBJECTIVEWe sought to perform an untargeted integrative analysis of the intestinal metabolome of childhood asthma in this ancillary study of the Vitamin D Antenatal Asthma Reduction Trial.Metabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other "omics": the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires.METHODSMetabolomic profiling was performed by using mass spectrometry on fecal samples collected from 361 three-year-old subjects. Adjusted logistic regression analyses identified metabolites and modules of highly correlated metabolites associated with asthma diagnosis by age 3 years. Sparse canonical correlation analysis identified associations relevant to asthma between the intestinal metabolome and other "omics": the intestinal microbiome as measured by using 16S rRNA sequencing, the plasma metabolome as measured by using mass spectrometry, and diet as measured by using food frequency questionnaires.Several intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = -6.3; 95% CI, -11.3 to -1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites.RESULTSSeveral intestinal metabolites were associated with asthma at age 3 years, including inverse associations between asthma and polyunsaturated fatty acids (adjusted logistic regression β = -6.3; 95% CI, -11.3 to -1.4; P = .01) and other lipids. Asthma-associated intestinal metabolites were significant mediators of the inverse relationship between exclusive breast-feeding for the first 4 months of life and asthma (P for indirect association = .04) and the positive association between a diet rich in meats and asthma (P = .03). Specific intestinal bacterial taxa, including the family Christensenellaceae, and plasma metabolites, including γ-tocopherol/β-tocopherol, were positively associated with asthma and asthma-associated intestinal metabolites.Integrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies.CONCLUSIONIntegrative analyses revealed significant interrelationships between the intestinal metabolome and the intestinal microbiome, plasma metabolome, and diet in association with childhood asthma. These findings require replication in future studies. |
| Author | Zeiger, Robert S. Beigelman, Avraham Laranjo, Nancy Lee-Sarwar, Kathleen A. Kelly, Rachel S. Gold, Diane R. O'Connor, George T. Weiss, Scott T. Sandel, Megan T. Lasky-Su, Jessica Litonjua, Augusto A. Bacharier, Leonard B. |
| AuthorAffiliation | 3 Departments of Allergy and Research and Evaluation, Kaiser Permanente Southern California, San Diego and Pasadena, CA, USA 2 Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA 8 Division of Pediatric Pulmonary Medicine, Golisano Children’s Hospital at Strong, University of Rochester Medical Center, Rochester, NY, USA 4 Pulmonary Center and Department of Medicine, Boston University School of Medicine, Boston, MA, USA 1 Division of Rheumatology, Immunology and Allergy, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA 7 Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, USA 5 Department of Pediatrics, Boston Medical Center, Boston, MA, USA 6 Division of Pediatric Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St Louis, MO and St Louis Children’s Hospital, St Louis, MO, USA |
| AuthorAffiliation_xml | – name: 5 Department of Pediatrics, Boston Medical Center, Boston, MA, USA – name: 4 Pulmonary Center and Department of Medicine, Boston University School of Medicine, Boston, MA, USA – name: 6 Division of Pediatric Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St Louis, MO and St Louis Children’s Hospital, St Louis, MO, USA – name: 3 Departments of Allergy and Research and Evaluation, Kaiser Permanente Southern California, San Diego and Pasadena, CA, USA – name: 8 Division of Pediatric Pulmonary Medicine, Golisano Children’s Hospital at Strong, University of Rochester Medical Center, Rochester, NY, USA – name: 1 Division of Rheumatology, Immunology and Allergy, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – name: 2 Channing Division of Network Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA – name: 7 Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, USA |
| Author_xml | – sequence: 1 givenname: Kathleen A. surname: Lee-Sarwar fullname: Lee-Sarwar, Kathleen A. email: klee-sarwar@partners.org organization: Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 2 givenname: Rachel S. surname: Kelly fullname: Kelly, Rachel S. organization: Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 3 givenname: Jessica surname: Lasky-Su fullname: Lasky-Su, Jessica organization: Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 4 givenname: Robert S. surname: Zeiger fullname: Zeiger, Robert S. organization: Departments of Allergy and Research and Evaluation, Kaiser Permanente Southern California, San Diego and Pasadena, Calif – sequence: 5 givenname: George T. surname: O'Connor fullname: O'Connor, George T. organization: Pulmonary Center and Department of Medicine, Boston University School of Medicine, Boston, Mass – sequence: 6 givenname: Megan T. surname: Sandel fullname: Sandel, Megan T. organization: Department of Pediatrics, Boston Medical Center, Boston, Mass – sequence: 7 givenname: Leonard B. surname: Bacharier fullname: Bacharier, Leonard B. organization: Division of Pediatric Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St Louis, and St Louis Children's Hospital, St Louis, Mo – sequence: 8 givenname: Avraham surname: Beigelman fullname: Beigelman, Avraham organization: Division of Pediatric Allergy, Immunology and Pulmonary Medicine, Department of Pediatrics, Washington University School of Medicine, St Louis, and St Louis Children's Hospital, St Louis, Mo – sequence: 9 givenname: Nancy surname: Laranjo fullname: Laranjo, Nancy organization: Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 10 givenname: Diane R. surname: Gold fullname: Gold, Diane R. organization: Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 11 givenname: Scott T. surname: Weiss fullname: Weiss, Scott T. organization: Channing Division of Network Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass – sequence: 12 givenname: Augusto A. surname: Litonjua fullname: Litonjua, Augusto A. email: augusto_litonjua@urmc.rochester.edu organization: Division of Pediatric Pulmonary Medicine, Golisano Children's Hospital at Strong, University of Rochester Medical Center, Rochester, NY |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30914378$$D View this record in MEDLINE/PubMed |
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| Copyright | 2019 American Academy of Allergy, Asthma & Immunology Copyright © 2019 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. 2019. American Academy of Allergy, Asthma & Immunology |
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| Keywords | nutrition breast-feeding PUFA vitamin E Christensenellaceae diet microbiome VDAART metabolome Asthma |
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| PublicationDate | 2019-08-01 |
| PublicationDateYYYYMMDD | 2019-08-01 |
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| PublicationTitle | Journal of allergy and clinical immunology |
| PublicationTitleAlternate | J Allergy Clin Immunol |
| PublicationYear | 2019 |
| Publisher | Elsevier Inc Elsevier Limited |
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| Snippet | The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.
We sought to perform... BackgroundThe intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.ObjectiveWe... The intestinal metabolome reflects the biological consequences of diverse exposures and might provide insight into asthma pathophysiology.BACKGROUNDThe... Intestinal metabolites, including immune-modulating lipids, are associated with childhood asthma. Specific bacterial taxa, plasma metabolites and dietary... |
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| SubjectTerms | Age Antibiotics Asthma Asthma - metabolism Asthma - microbiology Bacteria - classification Bacteria - genetics Bacteria - metabolism Breast breast-feeding Breastfeeding & lactation Child, Preschool Childhood Children Children & youth Christensenellaceae Correlation analysis Diet Eigenvalues Feces - microbiology Female Gastrointestinal Microbiome Humans Infant Infant, Newborn Intestine Lipid metabolism Male Mass spectroscopy Metabolites Metabolome Metabolomics microbiome Microbiomes nutrition Parent educational background Polyunsaturated fatty acids Precision medicine Principal components analysis Questionnaires RNA, Bacterial - genetics RNA, Bacterial - metabolism RNA, Ribosomal, 16S - genetics RNA, Ribosomal, 16S - metabolism rRNA 16S Vitamin D vitamin E |
| Title | Integrative analysis of the intestinal metabolome of childhood asthma |
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