Noninvasive biomarkers identify eosinophilic esophagitis: A prospective longitudinal study in children
ABSTRACT Background Esophageal histology is critical for diagnosis and surveillance of disease activity in eosinophilic esophagitis (EoE). A validated noninvasive biomarker has not been identified. We aimed to determine the utility of blood and urine eosinophil‐associated proteins to diagnose EoE an...
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| Veröffentlicht in: | Allergy (Copenhagen) 2021-12, Vol.76 (12), p.3755-3765 |
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| creator | Wechsler, Joshua B. Ackerman, Steven J. Chehade, Mirna Amsden, Katie Riffle, Mary E. Wang, Ming‐Yu Du, Jian Kleinjan, Matt L. Alumkal, Preeth Gray, Elizabeth Kim, Kwang‐Youn A. Wershil, Barry K. Kagalwalla, Amir F. |
| description | ABSTRACT
Background
Esophageal histology is critical for diagnosis and surveillance of disease activity in eosinophilic esophagitis (EoE). A validated noninvasive biomarker has not been identified. We aimed to determine the utility of blood and urine eosinophil‐associated proteins to diagnose EoE and predict esophageal eosinophilia.
Methods
Blood and urine were collected from children undergoing endoscopy with biopsy. Absolute eosinophil count (AEC), plasma eosinophil‐derived neurotoxin (EDN), eosinophil cationic protein (ECP), major basic protein‐1 (MBP‐1), galectin‐10 (CLC/GAL‐10), Eotaxin‐2 and Eotaxin‐3, and urine osteopontin (OPN) and matrix metalloproteinase‐9 (MMP‐9) were determined. Differences were assessed between EoE and control, and with treatment response. The capacity to predict EoE diagnosis and esophageal eosinophil counts was assessed.
Results
Of 183 specimens were collected from 56 EoE patients and 15 non‐EoE controls with symptoms of esophageal dysfunction; 33 EoE patients had paired pre‐ and post‐treatment specimens. Plasma (CLC/GAL‐10, ECP, EDN, Eotaxin‐3, MBP‐1) and urine (OPN) biomarkers were increased in EoE compared to control. A panel comprising CLC/GAL‐10, Eotaxin‐3, ECP, EDN, MBP‐1, and AEC was superior to AEC alone in distinguishing EoE from control. AEC, CLC/GAL‐10, ECP, and MBP‐1 were significantly decreased in patients with esophageal eosinophil counts |
| doi_str_mv | 10.1111/all.14874 |
| format | Article |
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Background
Esophageal histology is critical for diagnosis and surveillance of disease activity in eosinophilic esophagitis (EoE). A validated noninvasive biomarker has not been identified. We aimed to determine the utility of blood and urine eosinophil‐associated proteins to diagnose EoE and predict esophageal eosinophilia.
Methods
Blood and urine were collected from children undergoing endoscopy with biopsy. Absolute eosinophil count (AEC), plasma eosinophil‐derived neurotoxin (EDN), eosinophil cationic protein (ECP), major basic protein‐1 (MBP‐1), galectin‐10 (CLC/GAL‐10), Eotaxin‐2 and Eotaxin‐3, and urine osteopontin (OPN) and matrix metalloproteinase‐9 (MMP‐9) were determined. Differences were assessed between EoE and control, and with treatment response. The capacity to predict EoE diagnosis and esophageal eosinophil counts was assessed.
Results
Of 183 specimens were collected from 56 EoE patients and 15 non‐EoE controls with symptoms of esophageal dysfunction; 33 EoE patients had paired pre‐ and post‐treatment specimens. Plasma (CLC/GAL‐10, ECP, EDN, Eotaxin‐3, MBP‐1) and urine (OPN) biomarkers were increased in EoE compared to control. A panel comprising CLC/GAL‐10, Eotaxin‐3, ECP, EDN, MBP‐1, and AEC was superior to AEC alone in distinguishing EoE from control. AEC, CLC/GAL‐10, ECP, and MBP‐1 were significantly decreased in patients with esophageal eosinophil counts <15/hpf in response to treatment. AEC, CLC/GAL‐10, ECP, EDN, OPN, and MBP‐1 each predicted esophageal eosinophil counts utilizing mixed models controlled for age, gender, treatment, and atopy; AEC combined with MBP‐1 best predicted the counts.
Conclusions
We identified novel panels of eosinophil‐associated proteins that along with AEC are superior to AEC alone in distinguishing EoE from controls and predicting esophageal eosinophil counts.
A panel of eosinophil‐associated plasma proteins along with AEC are superior to AEC alone in distinguishing EoE from non‐EoE. A panel of AEC and MBP‐1 predicted esophageal eosinophil counts superior to AEC alone longitudinally. Histologic responders to EoE treatment have a greater reduction in AEC, CLC/GAL‐10, ECP, and MBP‐1 than non‐responders. Abbreviations: EoE, eosinophilic esophagitis; AEC, absolute eosinophil count; CLC/GAL10, galectin‐10; ECP, eosinophil cationic protein; EDN, eosinophil‐derived neurotoxin; MBP‐1, major basic protein.
</description><identifier>ISSN: 0105-4538</identifier><identifier>EISSN: 1398-9995</identifier><identifier>DOI: 10.1111/all.14874</identifier><identifier>PMID: 33905577</identifier><language>eng</language><publisher>Denmark: Blackwell Publishing Ltd</publisher><subject>Allergies ; Atopy ; Autoimmune diseases ; biomarker ; Biomarkers ; Biopsy ; blood ; Blood diseases ; Child ; Children ; Diagnosis ; Endoscopy ; eosinophil ; Eosinophil cationic protein ; Eosinophil-Derived Neurotoxin - metabolism ; Eosinophilia ; eosinophilic esophagitis ; Eosinophilic Esophagitis - metabolism ; Eosinophils - metabolism ; Eotaxin ; Esophageal diseases ; Esophagitis ; Esophagus ; Gastrointestinal diseases ; Humans ; Leukocytes ; Leukocytes (eosinophilic) ; Longitudinal Studies ; Matrix metalloproteinase ; Metalloproteinase ; noninvasive ; Osteopontin ; Patients ; Prospective Studies ; Urine</subject><ispartof>Allergy (Copenhagen), 2021-12, Vol.76 (12), p.3755-3765</ispartof><rights>2021 European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd</rights><rights>2021 European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.</rights><rights>2021 EAACI and John Wiley and Sons A/S</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5094-decb56a697a91f2102d110d9116e5bfc5bdb71835137837059fb248dec504f413</citedby><cites>FETCH-LOGICAL-c5094-decb56a697a91f2102d110d9116e5bfc5bdb71835137837059fb248dec504f413</cites><orcidid>0000-0002-7177-2791 ; 0000-0002-1275-3275 ; 0000-0001-9298-6927 ; 0000-0002-4168-757X ; 0000-0002-8183-4693 ; 0000-0002-5401-2571</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.14874$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fall.14874$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33905577$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wechsler, Joshua B.</creatorcontrib><creatorcontrib>Ackerman, Steven J.</creatorcontrib><creatorcontrib>Chehade, Mirna</creatorcontrib><creatorcontrib>Amsden, Katie</creatorcontrib><creatorcontrib>Riffle, Mary E.</creatorcontrib><creatorcontrib>Wang, Ming‐Yu</creatorcontrib><creatorcontrib>Du, Jian</creatorcontrib><creatorcontrib>Kleinjan, Matt L.</creatorcontrib><creatorcontrib>Alumkal, Preeth</creatorcontrib><creatorcontrib>Gray, Elizabeth</creatorcontrib><creatorcontrib>Kim, Kwang‐Youn A.</creatorcontrib><creatorcontrib>Wershil, Barry K.</creatorcontrib><creatorcontrib>Kagalwalla, Amir F.</creatorcontrib><title>Noninvasive biomarkers identify eosinophilic esophagitis: A prospective longitudinal study in children</title><title>Allergy (Copenhagen)</title><addtitle>Allergy</addtitle><description>ABSTRACT
Background
Esophageal histology is critical for diagnosis and surveillance of disease activity in eosinophilic esophagitis (EoE). A validated noninvasive biomarker has not been identified. We aimed to determine the utility of blood and urine eosinophil‐associated proteins to diagnose EoE and predict esophageal eosinophilia.
Methods
Blood and urine were collected from children undergoing endoscopy with biopsy. Absolute eosinophil count (AEC), plasma eosinophil‐derived neurotoxin (EDN), eosinophil cationic protein (ECP), major basic protein‐1 (MBP‐1), galectin‐10 (CLC/GAL‐10), Eotaxin‐2 and Eotaxin‐3, and urine osteopontin (OPN) and matrix metalloproteinase‐9 (MMP‐9) were determined. Differences were assessed between EoE and control, and with treatment response. The capacity to predict EoE diagnosis and esophageal eosinophil counts was assessed.
Results
Of 183 specimens were collected from 56 EoE patients and 15 non‐EoE controls with symptoms of esophageal dysfunction; 33 EoE patients had paired pre‐ and post‐treatment specimens. Plasma (CLC/GAL‐10, ECP, EDN, Eotaxin‐3, MBP‐1) and urine (OPN) biomarkers were increased in EoE compared to control. A panel comprising CLC/GAL‐10, Eotaxin‐3, ECP, EDN, MBP‐1, and AEC was superior to AEC alone in distinguishing EoE from control. AEC, CLC/GAL‐10, ECP, and MBP‐1 were significantly decreased in patients with esophageal eosinophil counts <15/hpf in response to treatment. AEC, CLC/GAL‐10, ECP, EDN, OPN, and MBP‐1 each predicted esophageal eosinophil counts utilizing mixed models controlled for age, gender, treatment, and atopy; AEC combined with MBP‐1 best predicted the counts.
Conclusions
We identified novel panels of eosinophil‐associated proteins that along with AEC are superior to AEC alone in distinguishing EoE from controls and predicting esophageal eosinophil counts.
A panel of eosinophil‐associated plasma proteins along with AEC are superior to AEC alone in distinguishing EoE from non‐EoE. A panel of AEC and MBP‐1 predicted esophageal eosinophil counts superior to AEC alone longitudinally. Histologic responders to EoE treatment have a greater reduction in AEC, CLC/GAL‐10, ECP, and MBP‐1 than non‐responders. Abbreviations: EoE, eosinophilic esophagitis; AEC, absolute eosinophil count; CLC/GAL10, galectin‐10; ECP, eosinophil cationic protein; EDN, eosinophil‐derived neurotoxin; MBP‐1, major basic protein.
</description><subject>Allergies</subject><subject>Atopy</subject><subject>Autoimmune diseases</subject><subject>biomarker</subject><subject>Biomarkers</subject><subject>Biopsy</subject><subject>blood</subject><subject>Blood diseases</subject><subject>Child</subject><subject>Children</subject><subject>Diagnosis</subject><subject>Endoscopy</subject><subject>eosinophil</subject><subject>Eosinophil cationic protein</subject><subject>Eosinophil-Derived Neurotoxin - metabolism</subject><subject>Eosinophilia</subject><subject>eosinophilic esophagitis</subject><subject>Eosinophilic Esophagitis - metabolism</subject><subject>Eosinophils - metabolism</subject><subject>Eotaxin</subject><subject>Esophageal diseases</subject><subject>Esophagitis</subject><subject>Esophagus</subject><subject>Gastrointestinal diseases</subject><subject>Humans</subject><subject>Leukocytes</subject><subject>Leukocytes (eosinophilic)</subject><subject>Longitudinal Studies</subject><subject>Matrix metalloproteinase</subject><subject>Metalloproteinase</subject><subject>noninvasive</subject><subject>Osteopontin</subject><subject>Patients</subject><subject>Prospective Studies</subject><subject>Urine</subject><issn>0105-4538</issn><issn>1398-9995</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1UU1PAyEUJEZja_XgHzAknjxs-1iWsngwaRq_kkYveibsLttSV1ihrem_l9ra6EEu74U3M49hEDon0CfxDFTT9EmW8-wAdQkVeSKEYIeoCwRYkjGad9BJCHMA4KmAY9ShVABjnHdR_eSssSsVzErjwrh35d-0D9hU2i5MvcbaBWNdOzONKbEOsVNTszDhGo9w611odbnYcBtn4_2yMlY1OMRmjY3FZeRVXttTdFSrJuizXe2h17vbl_FDMnm-fxyPJknJQGRJpcuCDdVQcCVInRJIK0KgEoQMNSvqkhVVwUlOGaE8pxyYqIs0yyONQVZnhPbQzVa3XRbvuiqjCa8a2XoTja2lU0b-nVgzk1O3kgIIZzlEgcudgHcfSx0Wcu6WPnoKMh0CzTlkcX8PXW1RZfyB4HW930BAbiKRMRL5HUnEXvx-0h75k0EEDLaAT9Po9f9KcjSZbCW_AEDymHw</recordid><startdate>202112</startdate><enddate>202112</enddate><creator>Wechsler, Joshua B.</creator><creator>Ackerman, Steven J.</creator><creator>Chehade, Mirna</creator><creator>Amsden, Katie</creator><creator>Riffle, Mary E.</creator><creator>Wang, Ming‐Yu</creator><creator>Du, Jian</creator><creator>Kleinjan, Matt L.</creator><creator>Alumkal, Preeth</creator><creator>Gray, Elizabeth</creator><creator>Kim, Kwang‐Youn A.</creator><creator>Wershil, Barry K.</creator><creator>Kagalwalla, Amir F.</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>5PM</scope><orcidid>https://orcid.org/0000-0002-7177-2791</orcidid><orcidid>https://orcid.org/0000-0002-1275-3275</orcidid><orcidid>https://orcid.org/0000-0001-9298-6927</orcidid><orcidid>https://orcid.org/0000-0002-4168-757X</orcidid><orcidid>https://orcid.org/0000-0002-8183-4693</orcidid><orcidid>https://orcid.org/0000-0002-5401-2571</orcidid></search><sort><creationdate>202112</creationdate><title>Noninvasive biomarkers identify eosinophilic esophagitis: A prospective longitudinal study in children</title><author>Wechsler, Joshua B. ; Ackerman, Steven J. ; Chehade, Mirna ; Amsden, Katie ; Riffle, Mary E. ; Wang, Ming‐Yu ; Du, Jian ; Kleinjan, Matt L. ; Alumkal, Preeth ; Gray, Elizabeth ; Kim, Kwang‐Youn A. ; Wershil, Barry K. ; Kagalwalla, Amir F.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5094-decb56a697a91f2102d110d9116e5bfc5bdb71835137837059fb248dec504f413</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Allergies</topic><topic>Atopy</topic><topic>Autoimmune diseases</topic><topic>biomarker</topic><topic>Biomarkers</topic><topic>Biopsy</topic><topic>blood</topic><topic>Blood diseases</topic><topic>Child</topic><topic>Children</topic><topic>Diagnosis</topic><topic>Endoscopy</topic><topic>eosinophil</topic><topic>Eosinophil cationic protein</topic><topic>Eosinophil-Derived Neurotoxin - metabolism</topic><topic>Eosinophilia</topic><topic>eosinophilic esophagitis</topic><topic>Eosinophilic Esophagitis - metabolism</topic><topic>Eosinophils - metabolism</topic><topic>Eotaxin</topic><topic>Esophageal diseases</topic><topic>Esophagitis</topic><topic>Esophagus</topic><topic>Gastrointestinal diseases</topic><topic>Humans</topic><topic>Leukocytes</topic><topic>Leukocytes (eosinophilic)</topic><topic>Longitudinal Studies</topic><topic>Matrix metalloproteinase</topic><topic>Metalloproteinase</topic><topic>noninvasive</topic><topic>Osteopontin</topic><topic>Patients</topic><topic>Prospective Studies</topic><topic>Urine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wechsler, Joshua B.</creatorcontrib><creatorcontrib>Ackerman, Steven J.</creatorcontrib><creatorcontrib>Chehade, Mirna</creatorcontrib><creatorcontrib>Amsden, Katie</creatorcontrib><creatorcontrib>Riffle, Mary E.</creatorcontrib><creatorcontrib>Wang, Ming‐Yu</creatorcontrib><creatorcontrib>Du, Jian</creatorcontrib><creatorcontrib>Kleinjan, Matt L.</creatorcontrib><creatorcontrib>Alumkal, Preeth</creatorcontrib><creatorcontrib>Gray, Elizabeth</creatorcontrib><creatorcontrib>Kim, Kwang‐Youn A.</creatorcontrib><creatorcontrib>Wershil, Barry K.</creatorcontrib><creatorcontrib>Kagalwalla, Amir F.</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>PubMed Central (Full Participant titles)</collection><jtitle>Allergy (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wechsler, Joshua B.</au><au>Ackerman, Steven J.</au><au>Chehade, Mirna</au><au>Amsden, Katie</au><au>Riffle, Mary E.</au><au>Wang, Ming‐Yu</au><au>Du, Jian</au><au>Kleinjan, Matt L.</au><au>Alumkal, Preeth</au><au>Gray, Elizabeth</au><au>Kim, Kwang‐Youn A.</au><au>Wershil, Barry K.</au><au>Kagalwalla, Amir F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Noninvasive biomarkers identify eosinophilic esophagitis: A prospective longitudinal study in children</atitle><jtitle>Allergy (Copenhagen)</jtitle><addtitle>Allergy</addtitle><date>2021-12</date><risdate>2021</risdate><volume>76</volume><issue>12</issue><spage>3755</spage><epage>3765</epage><pages>3755-3765</pages><issn>0105-4538</issn><eissn>1398-9995</eissn><abstract>ABSTRACT
Background
Esophageal histology is critical for diagnosis and surveillance of disease activity in eosinophilic esophagitis (EoE). A validated noninvasive biomarker has not been identified. We aimed to determine the utility of blood and urine eosinophil‐associated proteins to diagnose EoE and predict esophageal eosinophilia.
Methods
Blood and urine were collected from children undergoing endoscopy with biopsy. Absolute eosinophil count (AEC), plasma eosinophil‐derived neurotoxin (EDN), eosinophil cationic protein (ECP), major basic protein‐1 (MBP‐1), galectin‐10 (CLC/GAL‐10), Eotaxin‐2 and Eotaxin‐3, and urine osteopontin (OPN) and matrix metalloproteinase‐9 (MMP‐9) were determined. Differences were assessed between EoE and control, and with treatment response. The capacity to predict EoE diagnosis and esophageal eosinophil counts was assessed.
Results
Of 183 specimens were collected from 56 EoE patients and 15 non‐EoE controls with symptoms of esophageal dysfunction; 33 EoE patients had paired pre‐ and post‐treatment specimens. Plasma (CLC/GAL‐10, ECP, EDN, Eotaxin‐3, MBP‐1) and urine (OPN) biomarkers were increased in EoE compared to control. A panel comprising CLC/GAL‐10, Eotaxin‐3, ECP, EDN, MBP‐1, and AEC was superior to AEC alone in distinguishing EoE from control. AEC, CLC/GAL‐10, ECP, and MBP‐1 were significantly decreased in patients with esophageal eosinophil counts <15/hpf in response to treatment. AEC, CLC/GAL‐10, ECP, EDN, OPN, and MBP‐1 each predicted esophageal eosinophil counts utilizing mixed models controlled for age, gender, treatment, and atopy; AEC combined with MBP‐1 best predicted the counts.
Conclusions
We identified novel panels of eosinophil‐associated proteins that along with AEC are superior to AEC alone in distinguishing EoE from controls and predicting esophageal eosinophil counts.
A panel of eosinophil‐associated plasma proteins along with AEC are superior to AEC alone in distinguishing EoE from non‐EoE. A panel of AEC and MBP‐1 predicted esophageal eosinophil counts superior to AEC alone longitudinally. Histologic responders to EoE treatment have a greater reduction in AEC, CLC/GAL‐10, ECP, and MBP‐1 than non‐responders. Abbreviations: EoE, eosinophilic esophagitis; AEC, absolute eosinophil count; CLC/GAL10, galectin‐10; ECP, eosinophil cationic protein; EDN, eosinophil‐derived neurotoxin; MBP‐1, major basic protein.
</abstract><cop>Denmark</cop><pub>Blackwell Publishing Ltd</pub><pmid>33905577</pmid><doi>10.1111/all.14874</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-7177-2791</orcidid><orcidid>https://orcid.org/0000-0002-1275-3275</orcidid><orcidid>https://orcid.org/0000-0001-9298-6927</orcidid><orcidid>https://orcid.org/0000-0002-4168-757X</orcidid><orcidid>https://orcid.org/0000-0002-8183-4693</orcidid><orcidid>https://orcid.org/0000-0002-5401-2571</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley Free Content; MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
| subjects | Allergies Atopy Autoimmune diseases biomarker Biomarkers Biopsy blood Blood diseases Child Children Diagnosis Endoscopy eosinophil Eosinophil cationic protein Eosinophil-Derived Neurotoxin - metabolism Eosinophilia eosinophilic esophagitis Eosinophilic Esophagitis - metabolism Eosinophils - metabolism Eotaxin Esophageal diseases Esophagitis Esophagus Gastrointestinal diseases Humans Leukocytes Leukocytes (eosinophilic) Longitudinal Studies Matrix metalloproteinase Metalloproteinase noninvasive Osteopontin Patients Prospective Studies Urine |
| title | Noninvasive biomarkers identify eosinophilic esophagitis: A prospective longitudinal study in children |
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