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Immunological changes at point-of-lay increase susceptibility to Salmonella enterica Serovar enteritidis infection in vaccinated chickens
Chicken eggs are the main source of human Salmonella enterica serovar Enteritidis infection. S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved...
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Published in: | PloS one 2012-10, Vol.7 (10), p.e48195-e48195 |
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description | Chicken eggs are the main source of human Salmonella enterica serovar Enteritidis infection. S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved successful in control strategies in United Kingdom leading to a 70% drop in human cases since introduced. However, as hens reach sexual maturity they become immunosuppressed and it has been postulated this leads to increased susceptibility to Salmonella infection. In this study we define the changes to the systemic and reproductive tract-associated immune system of hens throughout sexual development by flow cytometry and histology and determine changes in susceptibility to experimental S. Enteritidis challenge in naive and vaccinated hens. Changes to both systemic and local immune systems occur in chickens at sexual development around 140 days of age. The population of several leukocyte classes drop, with the greatest fall in CD4+ lymphocyte numbers. Within the developing reproductive tract there an organised structure of lymphocytic aggregates with γδ-T lymphocytes associated with the mucosa. At point-of-lay, this organised structure disappears and only scattered lymphocytes remain. Protection against Salmonella challenge is significantly reduced in vaccinated birds at point-of-lay, coinciding with the drop in CD4+ lymphocytes. Susceptibility to reproductive tract infection by Salmonella increased in vaccinated and naïve animals at 140 and 148 days of age. We hypothesise that the drop in γδ-T lymphocytes in the tract leads to decreased innate protection of the mucosa to infection. These findings indicate that systemic and local changes to the immune system increase the susceptibility of hens to S. Enteritidis infection. The loss of protective immunity in vaccinated birds demonstrates that Salmonella control should not rely on vaccination alone, but as part of an integrated control strategy including biosecurity and improved animal welfare. |
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S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved successful in control strategies in United Kingdom leading to a 70% drop in human cases since introduced. However, as hens reach sexual maturity they become immunosuppressed and it has been postulated this leads to increased susceptibility to Salmonella infection. In this study we define the changes to the systemic and reproductive tract-associated immune system of hens throughout sexual development by flow cytometry and histology and determine changes in susceptibility to experimental S. Enteritidis challenge in naive and vaccinated hens. Changes to both systemic and local immune systems occur in chickens at sexual development around 140 days of age. The population of several leukocyte classes drop, with the greatest fall in CD4+ lymphocyte numbers. Within the developing reproductive tract there an organised structure of lymphocytic aggregates with γδ-T lymphocytes associated with the mucosa. At point-of-lay, this organised structure disappears and only scattered lymphocytes remain. Protection against Salmonella challenge is significantly reduced in vaccinated birds at point-of-lay, coinciding with the drop in CD4+ lymphocytes. Susceptibility to reproductive tract infection by Salmonella increased in vaccinated and naïve animals at 140 and 148 days of age. We hypothesise that the drop in γδ-T lymphocytes in the tract leads to decreased innate protection of the mucosa to infection. These findings indicate that systemic and local changes to the immune system increase the susceptibility of hens to S. Enteritidis infection. The loss of protective immunity in vaccinated birds demonstrates that Salmonella control should not rely on vaccination alone, but as part of an integrated control strategy including biosecurity and improved animal welfare.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0048195</identifier><identifier>PMID: 23133568</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Animal welfare ; Animals ; Biology ; Biosecurity ; Birds ; CD4 antigen ; CD4-Positive T-Lymphocytes - microbiology ; Chickens ; Chickens - immunology ; Cytokines ; Cytokines - biosynthesis ; Cytometry ; Disease susceptibility ; Eggs ; Female ; Flow cytometry ; Flow Cytometry - methods ; Histology ; Immune system ; Immunity ; Immunology ; Infection ; Infections ; Integrated control ; Interferon ; Interleukin-4 - biosynthesis ; Interleukin-6 - biosynthesis ; Legislation ; Leukocytes ; Leukocytes - cytology ; Lymphocytes ; Lymphocytes T ; Medicine ; Mucosa ; Ovary - microbiology ; Oviduct ; Oviducts - microbiology ; Poultry ; Poultry Diseases - immunology ; Poultry Diseases - prevention & control ; Poultry industry ; Poultry production ; Public health ; Receptors, Antigen, T-Cell, gamma-delta - metabolism ; Reproductive system ; Risk factors ; Salmonella ; Salmonella Enteritidis ; Salmonella enteritidis - immunology ; Salmonella enteritidis - metabolism ; Salmonella Infections, Animal - complications ; Salmonella Infections, Animal - immunology ; Salmonella Typhimurium ; Science ; Sexual maturity ; T cells ; Vaccination ; Vaccines ; Veterinary Science ; Zoonoses</subject><ispartof>PloS one, 2012-10, Vol.7 (10), p.e48195-e48195</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Johnston et al. 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S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved successful in control strategies in United Kingdom leading to a 70% drop in human cases since introduced. However, as hens reach sexual maturity they become immunosuppressed and it has been postulated this leads to increased susceptibility to Salmonella infection. In this study we define the changes to the systemic and reproductive tract-associated immune system of hens throughout sexual development by flow cytometry and histology and determine changes in susceptibility to experimental S. Enteritidis challenge in naive and vaccinated hens. Changes to both systemic and local immune systems occur in chickens at sexual development around 140 days of age. The population of several leukocyte classes drop, with the greatest fall in CD4+ lymphocyte numbers. 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The loss of protective immunity in vaccinated birds demonstrates that Salmonella control should not rely on vaccination alone, but as part of an integrated control strategy including biosecurity and improved animal welfare.</description><subject>Agriculture</subject><subject>Animal welfare</subject><subject>Animals</subject><subject>Biology</subject><subject>Biosecurity</subject><subject>Birds</subject><subject>CD4 antigen</subject><subject>CD4-Positive T-Lymphocytes - microbiology</subject><subject>Chickens</subject><subject>Chickens - immunology</subject><subject>Cytokines</subject><subject>Cytokines - biosynthesis</subject><subject>Cytometry</subject><subject>Disease susceptibility</subject><subject>Eggs</subject><subject>Female</subject><subject>Flow cytometry</subject><subject>Flow Cytometry - methods</subject><subject>Histology</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Immunology</subject><subject>Infection</subject><subject>Infections</subject><subject>Integrated control</subject><subject>Interferon</subject><subject>Interleukin-4 - 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immunology</subject><subject>Salmonella Typhimurium</subject><subject>Science</subject><subject>Sexual maturity</subject><subject>T cells</subject><subject>Vaccination</subject><subject>Vaccines</subject><subject>Veterinary Science</subject><subject>Zoonoses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9-K1DAUxoso7rr6BqIFQfSiY9KkTXojLIt_BhYWHPU2pGk6kzFtxiQdnEfwrT11ustU9kJ60XD6O985-U5PkjzHaIEJw--2bvC9tIud6_UCIcpxVTxIznFF8qzMEXl4cj5LnoSwRaggvCwfJ2c5wYQUJT9Pfi-7buiddWujpE3VRvZrHVIZ050zfcxcm1l5SE2vvJZBp2EISu-iqY018ZBGl66k7aAFa2Wq-6g96KQr7d1e-ikQTWMCSLRaReN6OKV7qZTpZdQNlDTqh-7D0-RRK23Qz6b3RfLt44evV5-z65tPy6vL60yxgseMkapCBWpYxZhua7hRxWnZMlVzrhElJSryomJIMkYZ45zWJYdgjqjmqmoJuUheHnV31gUxuRgEJjnDBFM-Essj0Ti5FTtvOukPwkkj_gacXwvpo1FWi7pRuOG0raqSUo5qrmoQQTJvVFM3dQla76dqQ93pRoEjXtqZ6PxLbzZi7faCUF4gMjbzZhLw7uegQxSdgRGA3b12A_SNKeGY5aQC9NU_6P23m6i1hAvAVBzUVaOouATHEMUF50At7qHgaXRnFMy7NRCfJbydJQAT9a-4lkMIYrn68v_szfc5-_qE3Whp4yY4O4x_UpiD9Agq70Lwur0zGSMxbsytG2LcGDFtDKS9OB3QXdLtipA_qvASOw</recordid><startdate>20121025</startdate><enddate>20121025</enddate><creator>Johnston, Claire E</creator><creator>Hartley, Catherine</creator><creator>Salisbury, Anne-Marie</creator><creator>Wigley, Paul</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20121025</creationdate><title>Immunological changes at point-of-lay increase susceptibility to Salmonella enterica Serovar enteritidis infection in vaccinated chickens</title><author>Johnston, Claire E ; Hartley, Catherine ; Salisbury, Anne-Marie ; Wigley, Paul</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-7399050d7977efb5389846f7cb88e04360525970a77477884b68360204e8c9f33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Agriculture</topic><topic>Animal welfare</topic><topic>Animals</topic><topic>Biology</topic><topic>Biosecurity</topic><topic>Birds</topic><topic>CD4 antigen</topic><topic>CD4-Positive T-Lymphocytes - 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metabolism</topic><topic>Reproductive system</topic><topic>Risk factors</topic><topic>Salmonella</topic><topic>Salmonella Enteritidis</topic><topic>Salmonella enteritidis - immunology</topic><topic>Salmonella enteritidis - metabolism</topic><topic>Salmonella Infections, Animal - complications</topic><topic>Salmonella Infections, Animal - immunology</topic><topic>Salmonella Typhimurium</topic><topic>Science</topic><topic>Sexual maturity</topic><topic>T cells</topic><topic>Vaccination</topic><topic>Vaccines</topic><topic>Veterinary Science</topic><topic>Zoonoses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Johnston, Claire E</creatorcontrib><creatorcontrib>Hartley, Catherine</creatorcontrib><creatorcontrib>Salisbury, Anne-Marie</creatorcontrib><creatorcontrib>Wigley, Paul</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints Resource Center</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>ProQuest Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Johnston, Claire E</au><au>Hartley, Catherine</au><au>Salisbury, Anne-Marie</au><au>Wigley, Paul</au><au>Zhou, Huaijun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Immunological changes at point-of-lay increase susceptibility to Salmonella enterica Serovar enteritidis infection in vaccinated chickens</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-10-25</date><risdate>2012</risdate><volume>7</volume><issue>10</issue><spage>e48195</spage><epage>e48195</epage><pages>e48195-e48195</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Chicken eggs are the main source of human Salmonella enterica serovar Enteritidis infection. S. Enteritidis infects the oviduct and ovary of the chicken leading to infection of developing eggs. Therefore, control in poultry production is a major public health priority. Vaccination of hens has proved successful in control strategies in United Kingdom leading to a 70% drop in human cases since introduced. However, as hens reach sexual maturity they become immunosuppressed and it has been postulated this leads to increased susceptibility to Salmonella infection. In this study we define the changes to the systemic and reproductive tract-associated immune system of hens throughout sexual development by flow cytometry and histology and determine changes in susceptibility to experimental S. Enteritidis challenge in naive and vaccinated hens. Changes to both systemic and local immune systems occur in chickens at sexual development around 140 days of age. The population of several leukocyte classes drop, with the greatest fall in CD4+ lymphocyte numbers. Within the developing reproductive tract there an organised structure of lymphocytic aggregates with γδ-T lymphocytes associated with the mucosa. At point-of-lay, this organised structure disappears and only scattered lymphocytes remain. Protection against Salmonella challenge is significantly reduced in vaccinated birds at point-of-lay, coinciding with the drop in CD4+ lymphocytes. Susceptibility to reproductive tract infection by Salmonella increased in vaccinated and naïve animals at 140 and 148 days of age. We hypothesise that the drop in γδ-T lymphocytes in the tract leads to decreased innate protection of the mucosa to infection. These findings indicate that systemic and local changes to the immune system increase the susceptibility of hens to S. Enteritidis infection. The loss of protective immunity in vaccinated birds demonstrates that Salmonella control should not rely on vaccination alone, but as part of an integrated control strategy including biosecurity and improved animal welfare.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23133568</pmid><doi>10.1371/journal.pone.0048195</doi><tpages>e48195</tpages><oa>free_for_read</oa></addata></record> |
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source | Publicly Available Content Database; PubMed Central |
subjects | Agriculture Animal welfare Animals Biology Biosecurity Birds CD4 antigen CD4-Positive T-Lymphocytes - microbiology Chickens Chickens - immunology Cytokines Cytokines - biosynthesis Cytometry Disease susceptibility Eggs Female Flow cytometry Flow Cytometry - methods Histology Immune system Immunity Immunology Infection Infections Integrated control Interferon Interleukin-4 - biosynthesis Interleukin-6 - biosynthesis Legislation Leukocytes Leukocytes - cytology Lymphocytes Lymphocytes T Medicine Mucosa Ovary - microbiology Oviduct Oviducts - microbiology Poultry Poultry Diseases - immunology Poultry Diseases - prevention & control Poultry industry Poultry production Public health Receptors, Antigen, T-Cell, gamma-delta - metabolism Reproductive system Risk factors Salmonella Salmonella Enteritidis Salmonella enteritidis - immunology Salmonella enteritidis - metabolism Salmonella Infections, Animal - complications Salmonella Infections, Animal - immunology Salmonella Typhimurium Science Sexual maturity T cells Vaccination Vaccines Veterinary Science Zoonoses |
title | Immunological changes at point-of-lay increase susceptibility to Salmonella enterica Serovar enteritidis infection in vaccinated chickens |
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