Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts
Summary Background Eosinophilic gastrointestinal disorders (EGIDs) are hypersensitivity disorders frequently triggered by food allergy and manifested by mucosal eosinophilic infiltration at any level of the gastrointestinal tract. This study established a model of gastric eosinophilia in peanut‐sens...
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| Veröffentlicht in: | Clinical and experimental allergy 2017-12, Vol.47 (12), p.1640-1647 |
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| creator | Mondoulet, L. Kalach, N. Dhelft, V. Larcher, T. Delayre‐Orthez, C. Benhamou, P. H. Spergel, J. Sampson, H. A. Dupont, C. |
| description | Summary
Background
Eosinophilic gastrointestinal disorders (EGIDs) are hypersensitivity disorders frequently triggered by food allergy and manifested by mucosal eosinophilic infiltration at any level of the gastrointestinal tract. This study established a model of gastric eosinophilia in peanut‐sensitized piglets to evaluate the efficacy of epicutaneous immunotherapy (EPIT) for its treatment.
Methods
Experiments were carried out in piglets first sensitized by three intra‐peritoneal injections of peanut protein extract (PPE) with adjuvant, and then given PPE orally for 10 days, a sequence leading to gastric eosinophilia assessed by endoscopy. For 3 months, eight piglets received active EPIT, using Viaskin® loaded with PPE, applied daily on the ear, while eight received placebo EPIT (Placebo). Piglets were exposed to a second 10‐day period of PPE orally. Lesions were scored by endoscopy on the last day of PPE exposure. After killing, all parts of the digestive tract were analysed by a pathologist unaware of the piglets’ status. IgE response was measured, and mechanistic parameters were analysed in the spleen.
Results
After sensitization, a significant increase of total IgE was observed in sensitized compared to naive animals (61.1 ± 13.3 vs 27.8 ± 6 ng/mL, P |
| doi_str_mv | 10.1111/cea.13037 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_01701597v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1945221494</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4227-24847f18ffac729e28371da6435d1198a9a4769ba5f47bd1058a55c5f3c808993</originalsourceid><addsrcrecordid>eNp10U9rFDEYBvAgil2rB7-ABLzoYdr8nSTHZalWWPBSzzGbeaebMjMZk4yyfnpTp1YQfC-B8ONJXh6EXlNyQetcenAXlBOunqAN5a1sWJ2naEOMFI3SRpyhFznfEUK4NPo5OmPatKRleoO-3iRwZYSp4NjjW5dLCh5DzGGK8zEMweHDCcMc_FLcBHHJOIzjMsVyhOTmEw4TnsPtACXjDFMOJfyEDpeIZ3DTUvJL9Kx3Q4ZXD-c5-vLh6mZ33ew_f_y02-4bLxhTDRNaqJ7qvndeMQNMc0U71wouO0qNdsYJ1ZqDk71Qh44SqZ2UXvbca6KN4efo_Zp7dIOdUxhdOtnogr3e7u39HaGKUGnUd1rtu9XOKX5bIBc7huxhGNYNLTVCMkaFEZW-_YfexSVNdZOqWqMpZ1L-fdynmHOC_vEHlNj7imytyP6uqNo3D4nLYYTuUf7ppILLFfwIA5z-n2R3V9s18hdZFpmi</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1969813255</pqid></control><display><type>article</type><title>Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts</title><source>Wiley-Blackwell Journals</source><creator>Mondoulet, L. ; Kalach, N. ; Dhelft, V. ; Larcher, T. ; Delayre‐Orthez, C. ; Benhamou, P. H. ; Spergel, J. ; Sampson, H. A. ; Dupont, C.</creator><creatorcontrib>Mondoulet, L. ; Kalach, N. ; Dhelft, V. ; Larcher, T. ; Delayre‐Orthez, C. ; Benhamou, P. H. ; Spergel, J. ; Sampson, H. A. ; Dupont, C.</creatorcontrib><description>Summary
Background
Eosinophilic gastrointestinal disorders (EGIDs) are hypersensitivity disorders frequently triggered by food allergy and manifested by mucosal eosinophilic infiltration at any level of the gastrointestinal tract. This study established a model of gastric eosinophilia in peanut‐sensitized piglets to evaluate the efficacy of epicutaneous immunotherapy (EPIT) for its treatment.
Methods
Experiments were carried out in piglets first sensitized by three intra‐peritoneal injections of peanut protein extract (PPE) with adjuvant, and then given PPE orally for 10 days, a sequence leading to gastric eosinophilia assessed by endoscopy. For 3 months, eight piglets received active EPIT, using Viaskin® loaded with PPE, applied daily on the ear, while eight received placebo EPIT (Placebo). Piglets were exposed to a second 10‐day period of PPE orally. Lesions were scored by endoscopy on the last day of PPE exposure. After killing, all parts of the digestive tract were analysed by a pathologist unaware of the piglets’ status. IgE response was measured, and mechanistic parameters were analysed in the spleen.
Results
After sensitization, a significant increase of total IgE was observed in sensitized compared to naive animals (61.1 ± 13.3 vs 27.8 ± 6 ng/mL, P < .01). Following oral intake of PPE, sensitized piglets developed moderate gastritis compared to naive piglets (1.5 vs 1.0, median score). After 3 months of immunotherapy, median IgE was significantly reduced in EPIT vs placebo piglets (61.4 ± 16.3 vs 105.9 ± 25.6 ng/mL, P < .01). Active EPIT significantly reduced gastric mucosal lesions induced by PPE oral intake (macroscopic score 0 [0‐2] vs 2 [1‐3], P < .01, respectively, active vs placebo) and gastric mucosa eosinophils counts (239 eosinophils/mm2 [59‐645] vs 2554 eosinophils/mm2 [462‐8057], P < .01, respectively active vs placebo). GATA‐3, IL‐5 and eotaxin mRNA expression decreased significantly after EPIT (P < .05).
Conclusions
This study describes a large animal model of gastric eosinophil in peanut‐sensitized piglets. Utilizing this model, we demonstrated the efficacy of EPIT in treating peanut‐induced EGIDs.</description><identifier>ISSN: 0954-7894</identifier><identifier>EISSN: 1365-2222</identifier><identifier>DOI: 10.1111/cea.13037</identifier><identifier>PMID: 28960628</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>animal models ; Blood diseases ; EGIDs ; Endoscopy ; Eosinophilia ; eosinophils ; Eotaxin ; epicutaneous ; Food allergies ; food allergy ; Gastric mucosa ; Gastritis ; Gastrointestinal diseases ; Gastrointestinal tract ; GATA-3 protein ; Gene expression ; Hypersensitivity ; Immunoglobulin E ; Immunotherapy ; Interleukin 5 ; Lesions ; Leukocytes (eosinophilic) ; Life Sciences ; Nuts ; Peritoneum ; Spleen</subject><ispartof>Clinical and experimental allergy, 2017-12, Vol.47 (12), p.1640-1647</ispartof><rights>2017 The Authors. Clinical & Experimental Allergy published by John Wiley & Sons Ltd</rights><rights>2017 The Authors. Clinical & Experimental Allergy published by John Wiley & Sons Ltd.</rights><rights>Copyright © 2017 John Wiley & Sons Ltd</rights><rights>Attribution - NonCommercial - NoDerivatives</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4227-24847f18ffac729e28371da6435d1198a9a4769ba5f47bd1058a55c5f3c808993</citedby><cites>FETCH-LOGICAL-c4227-24847f18ffac729e28371da6435d1198a9a4769ba5f47bd1058a55c5f3c808993</cites><orcidid>0000-0003-0110-0321 ; 0000-0003-3402-7490 ; 0000-0002-0396-3190</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%2Fcea.13037$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fcea.13037$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1416,27922,27923,45572,45573</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28960628$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01701597$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Mondoulet, L.</creatorcontrib><creatorcontrib>Kalach, N.</creatorcontrib><creatorcontrib>Dhelft, V.</creatorcontrib><creatorcontrib>Larcher, T.</creatorcontrib><creatorcontrib>Delayre‐Orthez, C.</creatorcontrib><creatorcontrib>Benhamou, P. H.</creatorcontrib><creatorcontrib>Spergel, J.</creatorcontrib><creatorcontrib>Sampson, H. A.</creatorcontrib><creatorcontrib>Dupont, C.</creatorcontrib><title>Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts</title><title>Clinical and experimental allergy</title><addtitle>Clin Exp Allergy</addtitle><description>Summary
Background
Eosinophilic gastrointestinal disorders (EGIDs) are hypersensitivity disorders frequently triggered by food allergy and manifested by mucosal eosinophilic infiltration at any level of the gastrointestinal tract. This study established a model of gastric eosinophilia in peanut‐sensitized piglets to evaluate the efficacy of epicutaneous immunotherapy (EPIT) for its treatment.
Methods
Experiments were carried out in piglets first sensitized by three intra‐peritoneal injections of peanut protein extract (PPE) with adjuvant, and then given PPE orally for 10 days, a sequence leading to gastric eosinophilia assessed by endoscopy. For 3 months, eight piglets received active EPIT, using Viaskin® loaded with PPE, applied daily on the ear, while eight received placebo EPIT (Placebo). Piglets were exposed to a second 10‐day period of PPE orally. Lesions were scored by endoscopy on the last day of PPE exposure. After killing, all parts of the digestive tract were analysed by a pathologist unaware of the piglets’ status. IgE response was measured, and mechanistic parameters were analysed in the spleen.
Results
After sensitization, a significant increase of total IgE was observed in sensitized compared to naive animals (61.1 ± 13.3 vs 27.8 ± 6 ng/mL, P < .01). Following oral intake of PPE, sensitized piglets developed moderate gastritis compared to naive piglets (1.5 vs 1.0, median score). After 3 months of immunotherapy, median IgE was significantly reduced in EPIT vs placebo piglets (61.4 ± 16.3 vs 105.9 ± 25.6 ng/mL, P < .01). Active EPIT significantly reduced gastric mucosal lesions induced by PPE oral intake (macroscopic score 0 [0‐2] vs 2 [1‐3], P < .01, respectively, active vs placebo) and gastric mucosa eosinophils counts (239 eosinophils/mm2 [59‐645] vs 2554 eosinophils/mm2 [462‐8057], P < .01, respectively active vs placebo). GATA‐3, IL‐5 and eotaxin mRNA expression decreased significantly after EPIT (P < .05).
Conclusions
This study describes a large animal model of gastric eosinophil in peanut‐sensitized piglets. Utilizing this model, we demonstrated the efficacy of EPIT in treating peanut‐induced EGIDs.</description><subject>animal models</subject><subject>Blood diseases</subject><subject>EGIDs</subject><subject>Endoscopy</subject><subject>Eosinophilia</subject><subject>eosinophils</subject><subject>Eotaxin</subject><subject>epicutaneous</subject><subject>Food allergies</subject><subject>food allergy</subject><subject>Gastric mucosa</subject><subject>Gastritis</subject><subject>Gastrointestinal diseases</subject><subject>Gastrointestinal tract</subject><subject>GATA-3 protein</subject><subject>Gene expression</subject><subject>Hypersensitivity</subject><subject>Immunoglobulin E</subject><subject>Immunotherapy</subject><subject>Interleukin 5</subject><subject>Lesions</subject><subject>Leukocytes (eosinophilic)</subject><subject>Life Sciences</subject><subject>Nuts</subject><subject>Peritoneum</subject><subject>Spleen</subject><issn>0954-7894</issn><issn>1365-2222</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><recordid>eNp10U9rFDEYBvAgil2rB7-ABLzoYdr8nSTHZalWWPBSzzGbeaebMjMZk4yyfnpTp1YQfC-B8ONJXh6EXlNyQetcenAXlBOunqAN5a1sWJ2naEOMFI3SRpyhFznfEUK4NPo5OmPatKRleoO-3iRwZYSp4NjjW5dLCh5DzGGK8zEMweHDCcMc_FLcBHHJOIzjMsVyhOTmEw4TnsPtACXjDFMOJfyEDpeIZ3DTUvJL9Kx3Q4ZXD-c5-vLh6mZ33ew_f_y02-4bLxhTDRNaqJ7qvndeMQNMc0U71wouO0qNdsYJ1ZqDk71Qh44SqZ2UXvbca6KN4efo_Zp7dIOdUxhdOtnogr3e7u39HaGKUGnUd1rtu9XOKX5bIBc7huxhGNYNLTVCMkaFEZW-_YfexSVNdZOqWqMpZ1L-fdynmHOC_vEHlNj7imytyP6uqNo3D4nLYYTuUf7ppILLFfwIA5z-n2R3V9s18hdZFpmi</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Mondoulet, L.</creator><creator>Kalach, N.</creator><creator>Dhelft, V.</creator><creator>Larcher, T.</creator><creator>Delayre‐Orthez, C.</creator><creator>Benhamou, P. H.</creator><creator>Spergel, J.</creator><creator>Sampson, H. A.</creator><creator>Dupont, C.</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0003-0110-0321</orcidid><orcidid>https://orcid.org/0000-0003-3402-7490</orcidid><orcidid>https://orcid.org/0000-0002-0396-3190</orcidid></search><sort><creationdate>201712</creationdate><title>Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts</title><author>Mondoulet, L. ; Kalach, N. ; Dhelft, V. ; Larcher, T. ; Delayre‐Orthez, C. ; Benhamou, P. H. ; Spergel, J. ; Sampson, H. A. ; Dupont, C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4227-24847f18ffac729e28371da6435d1198a9a4769ba5f47bd1058a55c5f3c808993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>animal models</topic><topic>Blood diseases</topic><topic>EGIDs</topic><topic>Endoscopy</topic><topic>Eosinophilia</topic><topic>eosinophils</topic><topic>Eotaxin</topic><topic>epicutaneous</topic><topic>Food allergies</topic><topic>food allergy</topic><topic>Gastric mucosa</topic><topic>Gastritis</topic><topic>Gastrointestinal diseases</topic><topic>Gastrointestinal tract</topic><topic>GATA-3 protein</topic><topic>Gene expression</topic><topic>Hypersensitivity</topic><topic>Immunoglobulin E</topic><topic>Immunotherapy</topic><topic>Interleukin 5</topic><topic>Lesions</topic><topic>Leukocytes (eosinophilic)</topic><topic>Life Sciences</topic><topic>Nuts</topic><topic>Peritoneum</topic><topic>Spleen</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mondoulet, L.</creatorcontrib><creatorcontrib>Kalach, N.</creatorcontrib><creatorcontrib>Dhelft, V.</creatorcontrib><creatorcontrib>Larcher, T.</creatorcontrib><creatorcontrib>Delayre‐Orthez, C.</creatorcontrib><creatorcontrib>Benhamou, P. H.</creatorcontrib><creatorcontrib>Spergel, J.</creatorcontrib><creatorcontrib>Sampson, H. A.</creatorcontrib><creatorcontrib>Dupont, C.</creatorcontrib><collection>Wiley Open Access</collection><collection>Wiley Online Library Journals</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>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Clinical and experimental allergy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mondoulet, L.</au><au>Kalach, N.</au><au>Dhelft, V.</au><au>Larcher, T.</au><au>Delayre‐Orthez, C.</au><au>Benhamou, P. H.</au><au>Spergel, J.</au><au>Sampson, H. A.</au><au>Dupont, C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts</atitle><jtitle>Clinical and experimental allergy</jtitle><addtitle>Clin Exp Allergy</addtitle><date>2017-12</date><risdate>2017</risdate><volume>47</volume><issue>12</issue><spage>1640</spage><epage>1647</epage><pages>1640-1647</pages><issn>0954-7894</issn><eissn>1365-2222</eissn><abstract>Summary
Background
Eosinophilic gastrointestinal disorders (EGIDs) are hypersensitivity disorders frequently triggered by food allergy and manifested by mucosal eosinophilic infiltration at any level of the gastrointestinal tract. This study established a model of gastric eosinophilia in peanut‐sensitized piglets to evaluate the efficacy of epicutaneous immunotherapy (EPIT) for its treatment.
Methods
Experiments were carried out in piglets first sensitized by three intra‐peritoneal injections of peanut protein extract (PPE) with adjuvant, and then given PPE orally for 10 days, a sequence leading to gastric eosinophilia assessed by endoscopy. For 3 months, eight piglets received active EPIT, using Viaskin® loaded with PPE, applied daily on the ear, while eight received placebo EPIT (Placebo). Piglets were exposed to a second 10‐day period of PPE orally. Lesions were scored by endoscopy on the last day of PPE exposure. After killing, all parts of the digestive tract were analysed by a pathologist unaware of the piglets’ status. IgE response was measured, and mechanistic parameters were analysed in the spleen.
Results
After sensitization, a significant increase of total IgE was observed in sensitized compared to naive animals (61.1 ± 13.3 vs 27.8 ± 6 ng/mL, P < .01). Following oral intake of PPE, sensitized piglets developed moderate gastritis compared to naive piglets (1.5 vs 1.0, median score). After 3 months of immunotherapy, median IgE was significantly reduced in EPIT vs placebo piglets (61.4 ± 16.3 vs 105.9 ± 25.6 ng/mL, P < .01). Active EPIT significantly reduced gastric mucosal lesions induced by PPE oral intake (macroscopic score 0 [0‐2] vs 2 [1‐3], P < .01, respectively, active vs placebo) and gastric mucosa eosinophils counts (239 eosinophils/mm2 [59‐645] vs 2554 eosinophils/mm2 [462‐8057], P < .01, respectively active vs placebo). GATA‐3, IL‐5 and eotaxin mRNA expression decreased significantly after EPIT (P < .05).
Conclusions
This study describes a large animal model of gastric eosinophil in peanut‐sensitized piglets. Utilizing this model, we demonstrated the efficacy of EPIT in treating peanut‐induced EGIDs.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28960628</pmid><doi>10.1111/cea.13037</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0003-0110-0321</orcidid><orcidid>https://orcid.org/0000-0003-3402-7490</orcidid><orcidid>https://orcid.org/0000-0002-0396-3190</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Wiley-Blackwell Journals |
| subjects | animal models Blood diseases EGIDs Endoscopy Eosinophilia eosinophils Eotaxin epicutaneous Food allergies food allergy Gastric mucosa Gastritis Gastrointestinal diseases Gastrointestinal tract GATA-3 protein Gene expression Hypersensitivity Immunoglobulin E Immunotherapy Interleukin 5 Lesions Leukocytes (eosinophilic) Life Sciences Nuts Peritoneum Spleen |
| title | Treatment of gastric eosinophilia by epicutaneous immunotherapy in piglets sensitized to peanuts |
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