Proteomics endotyping of infants with severe bronchiolitis and risk of childhood asthma
Background Bronchiolitis is the leading cause of hospitalization in U.S. infants and a major risk factor for childhood asthma. Growing evidence supports clinical heterogeneity within bronchiolitis. We aimed to identify endotypes of infant bronchiolitis by integrating clinical, virus, and serum prote...
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| Veröffentlicht in: | Allergy (Copenhagen) 2022-11, Vol.77 (11), p.3350-3361 |
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| creator | Ooka, Tadao Raita, Yoshihiko Fujiogi, Michimasa Freishtat, Robert J. Gerszten, Robert E. Mansbach, Jonathan M. Zhu, Zhaozhong Camargo, Carlos A. Hasegawa, Kohei |
| description | Background
Bronchiolitis is the leading cause of hospitalization in U.S. infants and a major risk factor for childhood asthma. Growing evidence supports clinical heterogeneity within bronchiolitis. We aimed to identify endotypes of infant bronchiolitis by integrating clinical, virus, and serum proteome data, and examine their relationships with asthma development.
Methods
This is a multicenter prospective cohort study of infants hospitalized for physician‐diagnosis of bronchiolitis. We identified bronchiolitis endotypes by applying unsupervised machine learning (clustering) approaches to integrated clinical, virus (respiratory syncytial virus [RSV], rhinovirus [RV]), and serum proteome data measured at hospitalization. We then examined their longitudinal association with the risk for developing asthma by age 6 years.
Results
In 140 infants hospitalized with bronchiolitis, we identified three endotypes: (1) clinicalatopicvirusRVproteomeNFκB‐dysregulated, (2) clinicalnon‐atopicvirusRSV/RVproteomeTNF‐dysregulated, and (3) clinicalclassicvirusRSVproteomeNFκB/TNF‐regulated endotypes. Endotype 1 infants were characterized by high proportion of IgE sensitization and RV infection. These endotype 1 infants also had dysregulated NFκB pathways (FDR |
| doi_str_mv | 10.1111/all.15390 |
| format | Article |
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Bronchiolitis is the leading cause of hospitalization in U.S. infants and a major risk factor for childhood asthma. Growing evidence supports clinical heterogeneity within bronchiolitis. We aimed to identify endotypes of infant bronchiolitis by integrating clinical, virus, and serum proteome data, and examine their relationships with asthma development.
Methods
This is a multicenter prospective cohort study of infants hospitalized for physician‐diagnosis of bronchiolitis. We identified bronchiolitis endotypes by applying unsupervised machine learning (clustering) approaches to integrated clinical, virus (respiratory syncytial virus [RSV], rhinovirus [RV]), and serum proteome data measured at hospitalization. We then examined their longitudinal association with the risk for developing asthma by age 6 years.
Results
In 140 infants hospitalized with bronchiolitis, we identified three endotypes: (1) clinicalatopicvirusRVproteomeNFκB‐dysregulated, (2) clinicalnon‐atopicvirusRSV/RVproteomeTNF‐dysregulated, and (3) clinicalclassicvirusRSVproteomeNFκB/TNF‐regulated endotypes. Endotype 1 infants were characterized by high proportion of IgE sensitization and RV infection. These endotype 1 infants also had dysregulated NFκB pathways (FDR < 0.001) and significantly higher risks for developing asthma (53% vs. 22%; adjOR 4.04; 95% CI, 1.49–11.0; p = 0.006), compared with endotype 3 (clinically resembling “classic” bronchiolitis). Likewise, endotype 2 infants were characterized by low proportion of IgE sensitization and high proportion of RSV or RV infection. These endotype 2 infants had dysregulated tumor necrosis factor (TNF)‐mediated signaling pathway (FDR <0.001) and significantly higher risks for developing asthma (44% vs. 22%; adjOR 2.71; 95% CI, 1.03–7.11, p = 0.04).
Conclusion
In this multicenter cohort, integrated clustering of clinical, virus, and proteome data identified biologically distinct endotypes of bronchiolitis that have differential risks of asthma development.
We identified three clinically‐meaningful and biologically‐distinct proteomics endotypes by integrating the clinical, virus, and serum proteomic data from a multicenter cohort of infants hospitalized for bronchiolitis. Each endotype had a different risk for developing asthma and recurrent wheeze. Endotype 1—characterized by atopic manifestations, rhinovirus infection, and dysregulated NFκB pathways—had the highest risk for developing asthma and recurrent wheeze. Abbreviations: CI, confidence interval; NFκB, nuclear factor‐κB; RSV, respiratory syncytial virus; RV, rhinovirus; TNF, tumor necrosis factor.</description><identifier>ISSN: 0105-4538</identifier><identifier>EISSN: 1398-9995</identifier><identifier>DOI: 10.1111/all.15390</identifier><identifier>PMID: 35620861</identifier><language>eng</language><publisher>Denmark: Blackwell Publishing Ltd</publisher><subject>Asthma ; Asthma - diagnosis ; Asthma - epidemiology ; Asthma - etiology ; bronchiolitis ; Bronchiolitis - complications ; Bronchopneumonia ; Child ; Childhood ; Children ; Childrens health ; endotyping ; Humans ; Immunoglobulin E ; Infant ; Infants ; NF-κB protein ; Prospective Studies ; Proteome ; Proteomes ; Proteomics ; Respiratory syncytial virus ; Respiratory Syncytial Virus Infections - complications ; Respiratory Syncytial Virus, Human ; Rhinovirus ; Risk Factors ; Signal transduction ; Tumor necrosis factor ; Tumor necrosis factor-TNF ; Viruses</subject><ispartof>Allergy (Copenhagen), 2022-11, Vol.77 (11), p.3350-3361</ispartof><rights>2022 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.</rights><rights>Copyright © 2022 John Wiley & Sons A/S</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4430-2747bed3b82d92327a491548779e6bd8fd02eb724c5644b0dba12d40109b66ec3</citedby><cites>FETCH-LOGICAL-c4430-2747bed3b82d92327a491548779e6bd8fd02eb724c5644b0dba12d40109b66ec3</cites><orcidid>0000-0002-1343-3986 ; 0000-0002-4179-3612</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fall.15390$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fall.15390$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35620861$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ooka, Tadao</creatorcontrib><creatorcontrib>Raita, Yoshihiko</creatorcontrib><creatorcontrib>Fujiogi, Michimasa</creatorcontrib><creatorcontrib>Freishtat, Robert J.</creatorcontrib><creatorcontrib>Gerszten, Robert E.</creatorcontrib><creatorcontrib>Mansbach, Jonathan M.</creatorcontrib><creatorcontrib>Zhu, Zhaozhong</creatorcontrib><creatorcontrib>Camargo, Carlos A.</creatorcontrib><creatorcontrib>Hasegawa, Kohei</creatorcontrib><title>Proteomics endotyping of infants with severe bronchiolitis and risk of childhood asthma</title><title>Allergy (Copenhagen)</title><addtitle>Allergy</addtitle><description>Background
Bronchiolitis is the leading cause of hospitalization in U.S. infants and a major risk factor for childhood asthma. Growing evidence supports clinical heterogeneity within bronchiolitis. We aimed to identify endotypes of infant bronchiolitis by integrating clinical, virus, and serum proteome data, and examine their relationships with asthma development.
Methods
This is a multicenter prospective cohort study of infants hospitalized for physician‐diagnosis of bronchiolitis. We identified bronchiolitis endotypes by applying unsupervised machine learning (clustering) approaches to integrated clinical, virus (respiratory syncytial virus [RSV], rhinovirus [RV]), and serum proteome data measured at hospitalization. We then examined their longitudinal association with the risk for developing asthma by age 6 years.
Results
In 140 infants hospitalized with bronchiolitis, we identified three endotypes: (1) clinicalatopicvirusRVproteomeNFκB‐dysregulated, (2) clinicalnon‐atopicvirusRSV/RVproteomeTNF‐dysregulated, and (3) clinicalclassicvirusRSVproteomeNFκB/TNF‐regulated endotypes. Endotype 1 infants were characterized by high proportion of IgE sensitization and RV infection. These endotype 1 infants also had dysregulated NFκB pathways (FDR < 0.001) and significantly higher risks for developing asthma (53% vs. 22%; adjOR 4.04; 95% CI, 1.49–11.0; p = 0.006), compared with endotype 3 (clinically resembling “classic” bronchiolitis). Likewise, endotype 2 infants were characterized by low proportion of IgE sensitization and high proportion of RSV or RV infection. These endotype 2 infants had dysregulated tumor necrosis factor (TNF)‐mediated signaling pathway (FDR <0.001) and significantly higher risks for developing asthma (44% vs. 22%; adjOR 2.71; 95% CI, 1.03–7.11, p = 0.04).
Conclusion
In this multicenter cohort, integrated clustering of clinical, virus, and proteome data identified biologically distinct endotypes of bronchiolitis that have differential risks of asthma development.
We identified three clinically‐meaningful and biologically‐distinct proteomics endotypes by integrating the clinical, virus, and serum proteomic data from a multicenter cohort of infants hospitalized for bronchiolitis. Each endotype had a different risk for developing asthma and recurrent wheeze. Endotype 1—characterized by atopic manifestations, rhinovirus infection, and dysregulated NFκB pathways—had the highest risk for developing asthma and recurrent wheeze. Abbreviations: CI, confidence interval; NFκB, nuclear factor‐κB; RSV, respiratory syncytial virus; RV, rhinovirus; TNF, tumor necrosis factor.</description><subject>Asthma</subject><subject>Asthma - diagnosis</subject><subject>Asthma - epidemiology</subject><subject>Asthma - etiology</subject><subject>bronchiolitis</subject><subject>Bronchiolitis - complications</subject><subject>Bronchopneumonia</subject><subject>Child</subject><subject>Childhood</subject><subject>Children</subject><subject>Childrens health</subject><subject>endotyping</subject><subject>Humans</subject><subject>Immunoglobulin E</subject><subject>Infant</subject><subject>Infants</subject><subject>NF-κB protein</subject><subject>Prospective Studies</subject><subject>Proteome</subject><subject>Proteomes</subject><subject>Proteomics</subject><subject>Respiratory syncytial virus</subject><subject>Respiratory Syncytial Virus Infections - complications</subject><subject>Respiratory Syncytial Virus, Human</subject><subject>Rhinovirus</subject><subject>Risk Factors</subject><subject>Signal transduction</subject><subject>Tumor necrosis factor</subject><subject>Tumor necrosis factor-TNF</subject><subject>Viruses</subject><issn>0105-4538</issn><issn>1398-9995</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUFLHDEYhkOp1NX20D9QAr3Yw2iSyUwmF0HEqrCgh5YeQzL5xonNJGsyq-y_N3ataKG5BJKHh_f7XoQ-U3JIyznS3h_SppbkHVrQWnaVlLJ5jxaEkqbiTd3tor2cbwkhgknyAe3WTctI19IF-nWd4gxxcn3GEGycNysXbnAcsAuDDnPGD24ecYZ7SIBNiqEfXfRudhnrYHFy-fcTXV69HWO0WOd5nPRHtDNon-HT872Pfn4_-3F6US2vzi9PT5ZVz3lNKia4MGBr0zErWc2E5pI2vBNCQmtsN1jCwAjG-6bl3BBrNGWWl8GkaVvo6310vPWu1mYC20OYk_Zqldyk00ZF7dTbn-BGdRPvlWypEKIrgoNnQYp3a8izmlzuwXsdIK6zYq2gJSWXpKBf_0Fv4zqFMp5iZbG8FNDxQn3bUn2KOScYXsJQop7qUqUu9aeuwn55nf6F_NtPAY62wIPzsPm_SZ0sl1vlI_RXn8A</recordid><startdate>202211</startdate><enddate>202211</enddate><creator>Ooka, Tadao</creator><creator>Raita, Yoshihiko</creator><creator>Fujiogi, Michimasa</creator><creator>Freishtat, Robert J.</creator><creator>Gerszten, Robert E.</creator><creator>Mansbach, Jonathan M.</creator><creator>Zhu, Zhaozhong</creator><creator>Camargo, Carlos A.</creator><creator>Hasegawa, Kohei</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1343-3986</orcidid><orcidid>https://orcid.org/0000-0002-4179-3612</orcidid></search><sort><creationdate>202211</creationdate><title>Proteomics endotyping of infants with severe bronchiolitis and risk of childhood asthma</title><author>Ooka, Tadao ; Raita, Yoshihiko ; Fujiogi, Michimasa ; Freishtat, Robert J. ; Gerszten, Robert E. ; Mansbach, Jonathan M. ; Zhu, Zhaozhong ; Camargo, Carlos A. ; Hasegawa, Kohei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4430-2747bed3b82d92327a491548779e6bd8fd02eb724c5644b0dba12d40109b66ec3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Asthma</topic><topic>Asthma - diagnosis</topic><topic>Asthma - epidemiology</topic><topic>Asthma - etiology</topic><topic>bronchiolitis</topic><topic>Bronchiolitis - complications</topic><topic>Bronchopneumonia</topic><topic>Child</topic><topic>Childhood</topic><topic>Children</topic><topic>Childrens health</topic><topic>endotyping</topic><topic>Humans</topic><topic>Immunoglobulin E</topic><topic>Infant</topic><topic>Infants</topic><topic>NF-κB protein</topic><topic>Prospective Studies</topic><topic>Proteome</topic><topic>Proteomes</topic><topic>Proteomics</topic><topic>Respiratory syncytial virus</topic><topic>Respiratory Syncytial Virus Infections - complications</topic><topic>Respiratory Syncytial Virus, Human</topic><topic>Rhinovirus</topic><topic>Risk Factors</topic><topic>Signal transduction</topic><topic>Tumor necrosis factor</topic><topic>Tumor necrosis factor-TNF</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ooka, Tadao</creatorcontrib><creatorcontrib>Raita, Yoshihiko</creatorcontrib><creatorcontrib>Fujiogi, Michimasa</creatorcontrib><creatorcontrib>Freishtat, Robert J.</creatorcontrib><creatorcontrib>Gerszten, Robert E.</creatorcontrib><creatorcontrib>Mansbach, Jonathan M.</creatorcontrib><creatorcontrib>Zhu, Zhaozhong</creatorcontrib><creatorcontrib>Camargo, Carlos A.</creatorcontrib><creatorcontrib>Hasegawa, Kohei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Allergy (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ooka, Tadao</au><au>Raita, Yoshihiko</au><au>Fujiogi, Michimasa</au><au>Freishtat, Robert J.</au><au>Gerszten, Robert E.</au><au>Mansbach, Jonathan M.</au><au>Zhu, Zhaozhong</au><au>Camargo, Carlos A.</au><au>Hasegawa, Kohei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proteomics endotyping of infants with severe bronchiolitis and risk of childhood asthma</atitle><jtitle>Allergy (Copenhagen)</jtitle><addtitle>Allergy</addtitle><date>2022-11</date><risdate>2022</risdate><volume>77</volume><issue>11</issue><spage>3350</spage><epage>3361</epage><pages>3350-3361</pages><issn>0105-4538</issn><eissn>1398-9995</eissn><abstract>Background
Bronchiolitis is the leading cause of hospitalization in U.S. infants and a major risk factor for childhood asthma. Growing evidence supports clinical heterogeneity within bronchiolitis. We aimed to identify endotypes of infant bronchiolitis by integrating clinical, virus, and serum proteome data, and examine their relationships with asthma development.
Methods
This is a multicenter prospective cohort study of infants hospitalized for physician‐diagnosis of bronchiolitis. We identified bronchiolitis endotypes by applying unsupervised machine learning (clustering) approaches to integrated clinical, virus (respiratory syncytial virus [RSV], rhinovirus [RV]), and serum proteome data measured at hospitalization. We then examined their longitudinal association with the risk for developing asthma by age 6 years.
Results
In 140 infants hospitalized with bronchiolitis, we identified three endotypes: (1) clinicalatopicvirusRVproteomeNFκB‐dysregulated, (2) clinicalnon‐atopicvirusRSV/RVproteomeTNF‐dysregulated, and (3) clinicalclassicvirusRSVproteomeNFκB/TNF‐regulated endotypes. Endotype 1 infants were characterized by high proportion of IgE sensitization and RV infection. These endotype 1 infants also had dysregulated NFκB pathways (FDR < 0.001) and significantly higher risks for developing asthma (53% vs. 22%; adjOR 4.04; 95% CI, 1.49–11.0; p = 0.006), compared with endotype 3 (clinically resembling “classic” bronchiolitis). Likewise, endotype 2 infants were characterized by low proportion of IgE sensitization and high proportion of RSV or RV infection. These endotype 2 infants had dysregulated tumor necrosis factor (TNF)‐mediated signaling pathway (FDR <0.001) and significantly higher risks for developing asthma (44% vs. 22%; adjOR 2.71; 95% CI, 1.03–7.11, p = 0.04).
Conclusion
In this multicenter cohort, integrated clustering of clinical, virus, and proteome data identified biologically distinct endotypes of bronchiolitis that have differential risks of asthma development.
We identified three clinically‐meaningful and biologically‐distinct proteomics endotypes by integrating the clinical, virus, and serum proteomic data from a multicenter cohort of infants hospitalized for bronchiolitis. Each endotype had a different risk for developing asthma and recurrent wheeze. Endotype 1—characterized by atopic manifestations, rhinovirus infection, and dysregulated NFκB pathways—had the highest risk for developing asthma and recurrent wheeze. Abbreviations: CI, confidence interval; NFκB, nuclear factor‐κB; RSV, respiratory syncytial virus; RV, rhinovirus; TNF, tumor necrosis factor.</abstract><cop>Denmark</cop><pub>Blackwell Publishing Ltd</pub><pmid>35620861</pmid><doi>10.1111/all.15390</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-1343-3986</orcidid><orcidid>https://orcid.org/0000-0002-4179-3612</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Asthma Asthma - diagnosis Asthma - epidemiology Asthma - etiology bronchiolitis Bronchiolitis - complications Bronchopneumonia Child Childhood Children Childrens health endotyping Humans Immunoglobulin E Infant Infants NF-κB protein Prospective Studies Proteome Proteomes Proteomics Respiratory syncytial virus Respiratory Syncytial Virus Infections - complications Respiratory Syncytial Virus, Human Rhinovirus Risk Factors Signal transduction Tumor necrosis factor Tumor necrosis factor-TNF Viruses |
| title | Proteomics endotyping of infants with severe bronchiolitis and risk of childhood asthma |
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