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Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens

Heather Chick, Lisa K. Williams, Nick Sparks, Farina Khattak, Paul Vermeij, Inge Frantzen, Mandy Peeters, Jetta J. E. Bijlsma, Daniel A. John Orcid Logo, Timothy Ogunrin, KEIONI ESSEX, Caroline Cayrou, Venkat Kanamarlapudi Orcid Logo, Christopher D. Bayliss, Julian M. Ketley, Thomas Humphrey Orcid Logo, Steven P. Rushton, Thomas Wilkinson Orcid Logo

Applied and Environmental Microbiology, Volume: 91, Issue: 3

Swansea University Authors: Heather Chick, Daniel A. John Orcid Logo, Timothy Ogunrin, KEIONI ESSEX, Venkat Kanamarlapudi Orcid Logo, Thomas Humphrey Orcid Logo, Thomas Wilkinson Orcid Logo

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DOI (Published version): 10.1128/aem.01614-24

Abstract

Campylobacter infections in humans and chickens are a significant burden to health services and the poultry industry. In the UK, over 75% of chicken products are Campylobacter-positive at retail, but the knowledge of the mechanisms responsible for extraintestinal spread into edible tissues remains i...

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Published in: Applied and Environmental Microbiology
ISSN: 0099-2240 1098-5336
Published: American Society for Microbiology 2025
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URI: https://cronfa.swan.ac.uk/Record/cronfa68768
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In the UK, over 75% of chicken products are Campylobacter-positive at retail, but the knowledge of the mechanisms responsible for extraintestinal spread into edible tissues remains incomplete. This work aimed to establish if two chicken-associated lineages of Campylobacter jejuni, ST353 and ST464, have the potential for extraintestinal spread. Large- and small-scale chicken colonization trials investigated the infection biology of C. jejuni ST353 (three strains) and ST464 (four strains). Both lineages strongly colonized the ileum and ceca and were detected in liver and spleen. C. jejuni ST353 and ST464 spleen load were significantly increased compared to C. jejuni M1 controls. Immune responses in cecal tonsils exhibited early induction of IFN-&#x3B3; and suppressed TGF&#x3B2; at 7 days post-infection with C. jejuni ST464. Histochemistry of gut tissue demonstrated significant decreases in intestinal crypt depth in ileal tissue with increasing severity relative to Campylobacter lineage, M1 &lt;ST353&lt;ST464. Pairwise correlation analysis confirmed strong interdependencies between &#x201C;cecal Campylobacter load,&#x201D; &#x201C;CXCLi1,&#x201D; &#x201C;CXCLi2,&#x201D; and &#x201C;splenic Campylobacter load.&#x201D; Furthermore, linear discriminant analysis confirmed that cecal tonsil-derived IFN&#x3B3;, TGF&#x3B2;, and CXCLi1 could predict splenic invasion at 71% accuracy. This work demonstrates that two chicken specialist C. jejuni lineages, ST353 and ST464, cause extraintestinal spread to liver and spleen and modeling suggests distinct routes from ileum and cecum, respectively. Recognition of these two routes of Campylobacter extraintestinal spread (ileal/liver and cecal/spleen) provides a better understanding of this food-derived pathogen for academia and the industry.</abstract><type>Journal Article</type><journal>Applied and Environmental Microbiology</journal><volume>91</volume><journalNumber>3</journalNumber><paginationStart/><paginationEnd/><publisher>American Society for Microbiology</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>0099-2240</issnPrint><issnElectronic>1098-5336</issnElectronic><keywords/><publishedDay>19</publishedDay><publishedMonth>3</publishedMonth><publishedYear>2025</publishedYear><publishedDate>2025-03-19</publishedDate><doi>10.1128/aem.01614-24</doi><url/><notes/><college>COLLEGE NANME</college><department>Medical School</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>MEDS</DepartmentCode><institution>Swansea University</institution><apcterm>Other</apcterm><funders>UKRI | Biotechnology and Biological Sciences Research Council (BBSRC)</funders><projectreference/><lastEdited>2025-03-31T16:34:06.8570868</lastEdited><Created>2025-01-30T19:35:12.4247514</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Biomedical Science</level></path><authors><author><firstname>Heather</firstname><surname>Chick</surname><order>1</order></author><author><firstname>Lisa K.</firstname><surname>Williams</surname><order>2</order></author><author><firstname>Nick</firstname><surname>Sparks</surname><order>3</order></author><author><firstname>Farina</firstname><surname>Khattak</surname><order>4</order></author><author><firstname>Paul</firstname><surname>Vermeij</surname><order>5</order></author><author><firstname>Inge</firstname><surname>Frantzen</surname><order>6</order></author><author><firstname>Mandy</firstname><surname>Peeters</surname><order>7</order></author><author><firstname>Jetta J. 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spelling 2025-03-31T16:34:06.8570868 v2 68768 2025-01-30 Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens 00e95531dda8486188b1e44f7d27af77 Heather Chick Heather Chick true false 6420df4866142d2c5823d7d759a50a94 NULL Daniel A. John Daniel A. John true true d80a31d32f5cacc2343bb81dedadefcb Timothy Ogunrin Timothy Ogunrin true false cbc0d4197020272eb74db22a5e8e6434 KEIONI ESSEX KEIONI ESSEX true false 63741801137148abfa4c00cd547dcdfa 0000-0002-8739-1483 Venkat Kanamarlapudi Venkat Kanamarlapudi true false 22e06f3cf2556ac1e4f7428394aa5c3a 0000-0001-7965-8988 Thomas Humphrey Thomas Humphrey true false 86cca6bf31bfe8572de27c1b441420d8 0000-0003-0397-6079 Thomas Wilkinson Thomas Wilkinson true false 2025-01-30 MEDS Campylobacter infections in humans and chickens are a significant burden to health services and the poultry industry. In the UK, over 75% of chicken products are Campylobacter-positive at retail, but the knowledge of the mechanisms responsible for extraintestinal spread into edible tissues remains incomplete. This work aimed to establish if two chicken-associated lineages of Campylobacter jejuni, ST353 and ST464, have the potential for extraintestinal spread. Large- and small-scale chicken colonization trials investigated the infection biology of C. jejuni ST353 (three strains) and ST464 (four strains). Both lineages strongly colonized the ileum and ceca and were detected in liver and spleen. C. jejuni ST353 and ST464 spleen load were significantly increased compared to C. jejuni M1 controls. Immune responses in cecal tonsils exhibited early induction of IFN-γ and suppressed TGFβ at 7 days post-infection with C. jejuni ST464. Histochemistry of gut tissue demonstrated significant decreases in intestinal crypt depth in ileal tissue with increasing severity relative to Campylobacter lineage, M1 <ST353<ST464. Pairwise correlation analysis confirmed strong interdependencies between “cecal Campylobacter load,” “CXCLi1,” “CXCLi2,” and “splenic Campylobacter load.” Furthermore, linear discriminant analysis confirmed that cecal tonsil-derived IFNγ, TGFβ, and CXCLi1 could predict splenic invasion at 71% accuracy. This work demonstrates that two chicken specialist C. jejuni lineages, ST353 and ST464, cause extraintestinal spread to liver and spleen and modeling suggests distinct routes from ileum and cecum, respectively. Recognition of these two routes of Campylobacter extraintestinal spread (ileal/liver and cecal/spleen) provides a better understanding of this food-derived pathogen for academia and the industry. Journal Article Applied and Environmental Microbiology 91 3 American Society for Microbiology 0099-2240 1098-5336 19 3 2025 2025-03-19 10.1128/aem.01614-24 COLLEGE NANME Medical School COLLEGE CODE MEDS Swansea University Other UKRI | Biotechnology and Biological Sciences Research Council (BBSRC) 2025-03-31T16:34:06.8570868 2025-01-30T19:35:12.4247514 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Heather Chick 1 Lisa K. Williams 2 Nick Sparks 3 Farina Khattak 4 Paul Vermeij 5 Inge Frantzen 6 Mandy Peeters 7 Jetta J. E. Bijlsma 8 Daniel A. John NULL 9 Timothy Ogunrin 10 KEIONI ESSEX 11 Caroline Cayrou 12 Venkat Kanamarlapudi 0000-0002-8739-1483 13 Christopher D. Bayliss 14 Julian M. Ketley 15 Thomas Humphrey 0000-0001-7965-8988 16 Steven P. Rushton 17 Thomas Wilkinson 0000-0003-0397-6079 18 68768__33690__43243f9fee1c40c5a923268292107969.pdf 68768.VoR.pdf 2025-02-27T12:36:12.6360066 Output 3407828 application/pdf Version of Record true Copyright © 2025 Chick et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. true eng https://creativecommons.org/licenses/by/4.0/
title Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
spellingShingle Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
Heather Chick
Daniel A. John
Timothy Ogunrin
KEIONI ESSEX
Venkat Kanamarlapudi
Thomas Humphrey
Thomas Wilkinson
title_short Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
title_full Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
title_fullStr Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
title_full_unstemmed Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
title_sort Campylobacter jejuni ST353 and ST464 cause localized gut inflammation, crypt damage, and extraintestinal spread during large- and small-scale infection in broiler chickens
author_id_str_mv 00e95531dda8486188b1e44f7d27af77
6420df4866142d2c5823d7d759a50a94
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author_id_fullname_str_mv 00e95531dda8486188b1e44f7d27af77_***_Heather Chick
6420df4866142d2c5823d7d759a50a94_***_Daniel A. John
d80a31d32f5cacc2343bb81dedadefcb_***_Timothy Ogunrin
cbc0d4197020272eb74db22a5e8e6434_***_KEIONI ESSEX
63741801137148abfa4c00cd547dcdfa_***_Venkat Kanamarlapudi
22e06f3cf2556ac1e4f7428394aa5c3a_***_Thomas Humphrey
86cca6bf31bfe8572de27c1b441420d8_***_Thomas Wilkinson
author Heather Chick
Daniel A. John
Timothy Ogunrin
KEIONI ESSEX
Venkat Kanamarlapudi
Thomas Humphrey
Thomas Wilkinson
author2 Heather Chick
Lisa K. Williams
Nick Sparks
Farina Khattak
Paul Vermeij
Inge Frantzen
Mandy Peeters
Jetta J. E. Bijlsma
Daniel A. John
Timothy Ogunrin
KEIONI ESSEX
Caroline Cayrou
Venkat Kanamarlapudi
Christopher D. Bayliss
Julian M. Ketley
Thomas Humphrey
Steven P. Rushton
Thomas Wilkinson
format Journal article
container_title Applied and Environmental Microbiology
container_volume 91
container_issue 3
publishDate 2025
institution Swansea University
issn 0099-2240
1098-5336
doi_str_mv 10.1128/aem.01614-24
publisher American Society for Microbiology
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
document_store_str 1
active_str 0
description Campylobacter infections in humans and chickens are a significant burden to health services and the poultry industry. In the UK, over 75% of chicken products are Campylobacter-positive at retail, but the knowledge of the mechanisms responsible for extraintestinal spread into edible tissues remains incomplete. This work aimed to establish if two chicken-associated lineages of Campylobacter jejuni, ST353 and ST464, have the potential for extraintestinal spread. Large- and small-scale chicken colonization trials investigated the infection biology of C. jejuni ST353 (three strains) and ST464 (four strains). Both lineages strongly colonized the ileum and ceca and were detected in liver and spleen. C. jejuni ST353 and ST464 spleen load were significantly increased compared to C. jejuni M1 controls. Immune responses in cecal tonsils exhibited early induction of IFN-γ and suppressed TGFβ at 7 days post-infection with C. jejuni ST464. Histochemistry of gut tissue demonstrated significant decreases in intestinal crypt depth in ileal tissue with increasing severity relative to Campylobacter lineage, M1 <ST353<ST464. Pairwise correlation analysis confirmed strong interdependencies between “cecal Campylobacter load,” “CXCLi1,” “CXCLi2,” and “splenic Campylobacter load.” Furthermore, linear discriminant analysis confirmed that cecal tonsil-derived IFNγ, TGFβ, and CXCLi1 could predict splenic invasion at 71% accuracy. This work demonstrates that two chicken specialist C. jejuni lineages, ST353 and ST464, cause extraintestinal spread to liver and spleen and modeling suggests distinct routes from ileum and cecum, respectively. Recognition of these two routes of Campylobacter extraintestinal spread (ileal/liver and cecal/spleen) provides a better understanding of this food-derived pathogen for academia and the industry.
published_date 2025-03-19T08:30:49Z
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