The baseline immunological and hygienic status of pigs impact disease severity of African swine fever
African Swine Fever virus (ASFV) is a large double-enveloped DNA virus of the Asfarviridae family that causes a lethal hemorrhagic disease in domestic pigs and wild boars. Since 2007, a highly virulent genotype II strain has emerged and spread in Europe and South-East Asia, where millions of animals...
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| description | African Swine Fever virus (ASFV) is a large double-enveloped DNA virus of the Asfarviridae family that causes a lethal hemorrhagic disease in domestic pigs and wild boars. Since 2007, a highly virulent genotype II strain has emerged and spread in Europe and South-East Asia, where millions of animals succumbed to the disease. Field- and laboratory-attenuated strains of ASFV cause highly variable clinical disease severity and survival, and mechanisms remain unclear. We hypothesized that the immunological and hygienic status of pigs is a determinant of ASF disease course. Here we compared the immunological profile at baseline and in response to ASFV infection in specific pathogen-free (SPF) and farm-raised Large White domestic pigs. At steady state, SPF pigs showed lower white blood cell counts and a lower basal inflammatory and antiviral transcriptomic profile compared to farm pigs, associated with profound differences in gut microbiome composition. After inoculation with a highly virulent ASFV genotype II strain (Armenia 2008), severe clinical signs, viremia and pro-inflammatory cytokines appeared sooner in SPF pigs, indicating a reduced capacity to control early virus replication. In contrast, during infection with an attenuated field isolate (Estonia 2014), SPF pigs presented a milder and shorter clinical disease with full recovery, whereas farm pigs presented severe protracted disease with 50% lethality. Interestingly, farm pigs showed higher production of inflammatory cytokines, whereas SPF pigs produced more anti-inflammatory IL-1ra early after infection and presented a stronger expansion of leukocytes in the recovery phase. Altogether, our data indicate that the hygiene-dependent innate immune status has a double-edge sword impact on immune responses in ASF pathogenesis. While the higher baseline innate immune activity helps the host in reducing initial virus replication, it promotes immunopathological cytokine responses, and delays lymphocyte proliferation after infection with an attenuated strain. Such effects should be considered for live vaccine development and vigilance. |
| doi_str_mv | 10.1371/journal.ppat.1010522 |
| format | Article |
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Since 2007, a highly virulent genotype II strain has emerged and spread in Europe and South-East Asia, where millions of animals succumbed to the disease. Field- and laboratory-attenuated strains of ASFV cause highly variable clinical disease severity and survival, and mechanisms remain unclear. We hypothesized that the immunological and hygienic status of pigs is a determinant of ASF disease course. Here we compared the immunological profile at baseline and in response to ASFV infection in specific pathogen-free (SPF) and farm-raised Large White domestic pigs. At steady state, SPF pigs showed lower white blood cell counts and a lower basal inflammatory and antiviral transcriptomic profile compared to farm pigs, associated with profound differences in gut microbiome composition. After inoculation with a highly virulent ASFV genotype II strain (Armenia 2008), severe clinical signs, viremia and pro-inflammatory cytokines appeared sooner in SPF pigs, indicating a reduced capacity to control early virus replication. In contrast, during infection with an attenuated field isolate (Estonia 2014), SPF pigs presented a milder and shorter clinical disease with full recovery, whereas farm pigs presented severe protracted disease with 50% lethality. Interestingly, farm pigs showed higher production of inflammatory cytokines, whereas SPF pigs produced more anti-inflammatory IL-1ra early after infection and presented a stronger expansion of leukocytes in the recovery phase. Altogether, our data indicate that the hygiene-dependent innate immune status has a double-edge sword impact on immune responses in ASF pathogenesis. While the higher baseline innate immune activity helps the host in reducing initial virus replication, it promotes immunopathological cytokine responses, and delays lymphocyte proliferation after infection with an attenuated strain. Such effects should be considered for live vaccine development and vigilance.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1010522</identifier><identifier>PMID: 36006954</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>African swine fever ; Animals ; Apathy ; Asfarviridae ; Attenuation ; Biology and Life Sciences ; Blood ; Cell cycle ; Comparative analysis ; Cytokines ; Deoxyribonucleic acid ; Development and progression ; DNA ; DNA viruses ; Domestic animals ; Environmental aspects ; Epidemics ; Experiments ; Farms ; Fever ; Flow cytometry ; Gene expression ; Genotype & phenotype ; Genotypes ; Health aspects ; Hematology ; Hemorrhage ; Hemorrhagic disease ; Hogs ; Hygiene ; Immune response ; Immune status ; Immune system ; Immunology ; Infections ; Inflammation ; Inoculation ; Interleukin 1 receptor antagonist ; Interleukin 1 receptors ; Intestinal microflora ; Lethality ; Leukocytes ; Lymphocytes ; Medicine and Health Sciences ; Microbiomes ; Microbiota ; Pathogenesis ; People and places ; Replication ; Research and Analysis Methods ; Risk factors ; Specific pathogen free ; Swine ; Transcriptomics ; Vaccine development ; Vaccines ; Veterinary hygiene ; Veterinary immunology ; Vigilance ; Viremia ; Virulence ; Viruses ; White blood cells</subject><ispartof>PLoS pathogens, 2022-08, Vol.18 (8), p.e1010522-e1010522</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Radulovic et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 Radulovic et al 2022 Radulovic et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c568t-53c7689a633043b41aeeeb055a6f0fd9c74ad0879af7b05268ef379bca754e203</citedby><cites>FETCH-LOGICAL-c568t-53c7689a633043b41aeeeb055a6f0fd9c74ad0879af7b05268ef379bca754e203</cites><orcidid>0000-0002-2049-7769</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409533/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9409533/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids></links><search><contributor>Dixon, Linda Kathleen</contributor><creatorcontrib>Radulovic, Emilia</creatorcontrib><creatorcontrib>Mehinagic, Kemal</creatorcontrib><creatorcontrib>Wüthrich, Tsering</creatorcontrib><creatorcontrib>Hilty, Markus</creatorcontrib><creatorcontrib>Posthaus, Horst</creatorcontrib><creatorcontrib>Summerfield, Artur</creatorcontrib><creatorcontrib>Ruggli, Nicolas</creatorcontrib><creatorcontrib>Benarafa, Charaf</creatorcontrib><title>The baseline immunological and hygienic status of pigs impact disease severity of African swine fever</title><title>PLoS pathogens</title><description>African Swine Fever virus (ASFV) is a large double-enveloped DNA virus of the Asfarviridae family that causes a lethal hemorrhagic disease in domestic pigs and wild boars. Since 2007, a highly virulent genotype II strain has emerged and spread in Europe and South-East Asia, where millions of animals succumbed to the disease. Field- and laboratory-attenuated strains of ASFV cause highly variable clinical disease severity and survival, and mechanisms remain unclear. We hypothesized that the immunological and hygienic status of pigs is a determinant of ASF disease course. Here we compared the immunological profile at baseline and in response to ASFV infection in specific pathogen-free (SPF) and farm-raised Large White domestic pigs. At steady state, SPF pigs showed lower white blood cell counts and a lower basal inflammatory and antiviral transcriptomic profile compared to farm pigs, associated with profound differences in gut microbiome composition. After inoculation with a highly virulent ASFV genotype II strain (Armenia 2008), severe clinical signs, viremia and pro-inflammatory cytokines appeared sooner in SPF pigs, indicating a reduced capacity to control early virus replication. In contrast, during infection with an attenuated field isolate (Estonia 2014), SPF pigs presented a milder and shorter clinical disease with full recovery, whereas farm pigs presented severe protracted disease with 50% lethality. Interestingly, farm pigs showed higher production of inflammatory cytokines, whereas SPF pigs produced more anti-inflammatory IL-1ra early after infection and presented a stronger expansion of leukocytes in the recovery phase. Altogether, our data indicate that the hygiene-dependent innate immune status has a double-edge sword impact on immune responses in ASF pathogenesis. While the higher baseline innate immune activity helps the host in reducing initial virus replication, it promotes immunopathological cytokine responses, and delays lymphocyte proliferation after infection with an attenuated strain. Such effects should be considered for live vaccine development and vigilance.</description><subject>African swine fever</subject><subject>Animals</subject><subject>Apathy</subject><subject>Asfarviridae</subject><subject>Attenuation</subject><subject>Biology and Life Sciences</subject><subject>Blood</subject><subject>Cell cycle</subject><subject>Comparative analysis</subject><subject>Cytokines</subject><subject>Deoxyribonucleic acid</subject><subject>Development and progression</subject><subject>DNA</subject><subject>DNA viruses</subject><subject>Domestic animals</subject><subject>Environmental aspects</subject><subject>Epidemics</subject><subject>Experiments</subject><subject>Farms</subject><subject>Fever</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Genotype & phenotype</subject><subject>Genotypes</subject><subject>Health aspects</subject><subject>Hematology</subject><subject>Hemorrhage</subject><subject>Hemorrhagic disease</subject><subject>Hogs</subject><subject>Hygiene</subject><subject>Immune response</subject><subject>Immune status</subject><subject>Immune system</subject><subject>Immunology</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Inoculation</subject><subject>Interleukin 1 receptor antagonist</subject><subject>Interleukin 1 receptors</subject><subject>Intestinal microflora</subject><subject>Lethality</subject><subject>Leukocytes</subject><subject>Lymphocytes</subject><subject>Medicine and Health Sciences</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Pathogenesis</subject><subject>People and places</subject><subject>Replication</subject><subject>Research and Analysis Methods</subject><subject>Risk factors</subject><subject>Specific pathogen free</subject><subject>Swine</subject><subject>Transcriptomics</subject><subject>Vaccine development</subject><subject>Vaccines</subject><subject>Veterinary hygiene</subject><subject>Veterinary immunology</subject><subject>Vigilance</subject><subject>Viremia</subject><subject>Virulence</subject><subject>Viruses</subject><subject>White blood 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severity of African swine fever</title><author>Radulovic, Emilia ; Mehinagic, Kemal ; Wüthrich, Tsering ; Hilty, Markus ; Posthaus, Horst ; Summerfield, Artur ; Ruggli, Nicolas ; Benarafa, Charaf</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c568t-53c7689a633043b41aeeeb055a6f0fd9c74ad0879af7b05268ef379bca754e203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>African swine fever</topic><topic>Animals</topic><topic>Apathy</topic><topic>Asfarviridae</topic><topic>Attenuation</topic><topic>Biology and Life Sciences</topic><topic>Blood</topic><topic>Cell cycle</topic><topic>Comparative analysis</topic><topic>Cytokines</topic><topic>Deoxyribonucleic acid</topic><topic>Development and progression</topic><topic>DNA</topic><topic>DNA viruses</topic><topic>Domestic animals</topic><topic>Environmental aspects</topic><topic>Epidemics</topic><topic>Experiments</topic><topic>Farms</topic><topic>Fever</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Genotype & phenotype</topic><topic>Genotypes</topic><topic>Health aspects</topic><topic>Hematology</topic><topic>Hemorrhage</topic><topic>Hemorrhagic disease</topic><topic>Hogs</topic><topic>Hygiene</topic><topic>Immune response</topic><topic>Immune status</topic><topic>Immune system</topic><topic>Immunology</topic><topic>Infections</topic><topic>Inflammation</topic><topic>Inoculation</topic><topic>Interleukin 1 receptor antagonist</topic><topic>Interleukin 1 receptors</topic><topic>Intestinal microflora</topic><topic>Lethality</topic><topic>Leukocytes</topic><topic>Lymphocytes</topic><topic>Medicine and Health Sciences</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Pathogenesis</topic><topic>People and places</topic><topic>Replication</topic><topic>Research and Analysis Methods</topic><topic>Risk 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Edition</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Radulovic, Emilia</au><au>Mehinagic, Kemal</au><au>Wüthrich, Tsering</au><au>Hilty, Markus</au><au>Posthaus, Horst</au><au>Summerfield, Artur</au><au>Ruggli, Nicolas</au><au>Benarafa, Charaf</au><au>Dixon, Linda Kathleen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The baseline immunological and hygienic status of pigs impact disease severity of African swine fever</atitle><jtitle>PLoS pathogens</jtitle><date>2022-08-25</date><risdate>2022</risdate><volume>18</volume><issue>8</issue><spage>e1010522</spage><epage>e1010522</epage><pages>e1010522-e1010522</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>African Swine Fever virus (ASFV) is a large double-enveloped DNA virus of the Asfarviridae family that causes a lethal hemorrhagic disease in domestic pigs and wild boars. Since 2007, a highly virulent genotype II strain has emerged and spread in Europe and South-East Asia, where millions of animals succumbed to the disease. Field- and laboratory-attenuated strains of ASFV cause highly variable clinical disease severity and survival, and mechanisms remain unclear. We hypothesized that the immunological and hygienic status of pigs is a determinant of ASF disease course. Here we compared the immunological profile at baseline and in response to ASFV infection in specific pathogen-free (SPF) and farm-raised Large White domestic pigs. At steady state, SPF pigs showed lower white blood cell counts and a lower basal inflammatory and antiviral transcriptomic profile compared to farm pigs, associated with profound differences in gut microbiome composition. After inoculation with a highly virulent ASFV genotype II strain (Armenia 2008), severe clinical signs, viremia and pro-inflammatory cytokines appeared sooner in SPF pigs, indicating a reduced capacity to control early virus replication. In contrast, during infection with an attenuated field isolate (Estonia 2014), SPF pigs presented a milder and shorter clinical disease with full recovery, whereas farm pigs presented severe protracted disease with 50% lethality. Interestingly, farm pigs showed higher production of inflammatory cytokines, whereas SPF pigs produced more anti-inflammatory IL-1ra early after infection and presented a stronger expansion of leukocytes in the recovery phase. Altogether, our data indicate that the hygiene-dependent innate immune status has a double-edge sword impact on immune responses in ASF pathogenesis. While the higher baseline innate immune activity helps the host in reducing initial virus replication, it promotes immunopathological cytokine responses, and delays lymphocyte proliferation after infection with an attenuated strain. Such effects should be considered for live vaccine development and vigilance.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>36006954</pmid><doi>10.1371/journal.ppat.1010522</doi><tpages>e1010522</tpages><orcidid>https://orcid.org/0000-0002-2049-7769</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | African swine fever Animals Apathy Asfarviridae Attenuation Biology and Life Sciences Blood Cell cycle Comparative analysis Cytokines Deoxyribonucleic acid Development and progression DNA DNA viruses Domestic animals Environmental aspects Epidemics Experiments Farms Fever Flow cytometry Gene expression Genotype & phenotype Genotypes Health aspects Hematology Hemorrhage Hemorrhagic disease Hogs Hygiene Immune response Immune status Immune system Immunology Infections Inflammation Inoculation Interleukin 1 receptor antagonist Interleukin 1 receptors Intestinal microflora Lethality Leukocytes Lymphocytes Medicine and Health Sciences Microbiomes Microbiota Pathogenesis People and places Replication Research and Analysis Methods Risk factors Specific pathogen free Swine Transcriptomics Vaccine development Vaccines Veterinary hygiene Veterinary immunology Vigilance Viremia Virulence Viruses White blood cells |
| title | The baseline immunological and hygienic status of pigs impact disease severity of African swine fever |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-18T06%3A05%3A46IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20baseline%20immunological%20and%20hygienic%20status%20of%20pigs%20impact%20disease%20severity%20of%20African%20swine%20fever&rft.jtitle=PLoS%20pathogens&rft.au=Radulovic,%20Emilia&rft.date=2022-08-25&rft.volume=18&rft.issue=8&rft.spage=e1010522&rft.epage=e1010522&rft.pages=e1010522-e1010522&rft.issn=1553-7374&rft.eissn=1553-7374&rft_id=info:doi/10.1371/journal.ppat.1010522&rft_dat=%3Cgale_plos_%3EA715936839%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2715142441&rft_id=info:pmid/36006954&rft_galeid=A715936839&rft_doaj_id=oai_doaj_org_article_64820d5f5ec94a8e8b28cad289876b59&rfr_iscdi=true |