Investigation of a herpesvirus outbreak in mixed breeds of adult domestic ducks using next generation sequencing

This report characterizes the first lethal outbreak of Marek's disease on a large farm of mixed-breed adult ducks (>18,000) and identifies the pathogen that resulted in high mortality (35%). Clinical signs included inappetence, respiratory distress, depression, muscle weakness, and ataxia. P...

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Veröffentlicht in:PloS one 2023-01, Vol.18 (1), p.e0280923-e0280923
Hauptverfasser: Damir, Hassan Abu, Ahmad, Waqar, Panicker, Neena G, Mohamed, Layla I, Omer, Elhag A, Kinne, Jörg, Wernery, Ulrich, Adem, Abdu, Ali, Mahmoud A, Mustafa, Farah
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container_title PloS one
container_volume 18
creator Damir, Hassan Abu
Ahmad, Waqar
Panicker, Neena G
Mohamed, Layla I
Omer, Elhag A
Kinne, Jörg
Wernery, Ulrich
Adem, Abdu
Ali, Mahmoud A
Mustafa, Farah
description This report characterizes the first lethal outbreak of Marek's disease on a large farm of mixed-breed adult ducks (>18,000) and identifies the pathogen that resulted in high mortality (35%). Clinical signs included inappetence, respiratory distress, depression, muscle weakness, and ataxia. Post mortem revealed enlarged fragile liver mottled with miliary whitish spots and an enlarged spleen. Histopathology revealed hepatocellular necrosis with eosinophilic intra-nuclear inclusion bodies, necrosis of splenic follicles and degeneration/necrosis of renal tubules. The disease was tentatively diagnosed as a herpesvirus infection, confirmed by virus isolation from the liver. DNA was isolated from 15-year-old archival formalin-fixed tissues from infected ducks and subjected to next generation sequencing (NGS). Despite highly degraded DNA, short stretches of G- and C-rich repeats (TTAGGG and TAACCC) were identified as telomeric repeats frequently found in herpesviruses. Megablast and further investigative bioinformatics identified presence of Marek's disease virus (MDV), a Gallid alphaherpesvirus type 2 (GAHV-2), as the cause of the acute fatal infection. The source of infection may be attributed to a dead migratory flamingo found close to the duck enclosures three days prior to the outbreak; hence, GAHV-2 may also be responsible for the fatal infection of the flamingo accentuated by heat stress. Considering the possible spread of this highly contagious and lethal virus from a flamingo to the ducks, and the increasing zoonosis of animal viruses into humans, such as monkey B alphaherpesvirus transmission from macaques to humans with ~80% fatality, this observation has important ramifications for human health and safety of the poultry industry.
doi_str_mv 10.1371/journal.pone.0280923
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Clinical signs included inappetence, respiratory distress, depression, muscle weakness, and ataxia. Post mortem revealed enlarged fragile liver mottled with miliary whitish spots and an enlarged spleen. Histopathology revealed hepatocellular necrosis with eosinophilic intra-nuclear inclusion bodies, necrosis of splenic follicles and degeneration/necrosis of renal tubules. The disease was tentatively diagnosed as a herpesvirus infection, confirmed by virus isolation from the liver. DNA was isolated from 15-year-old archival formalin-fixed tissues from infected ducks and subjected to next generation sequencing (NGS). Despite highly degraded DNA, short stretches of G- and C-rich repeats (TTAGGG and TAACCC) were identified as telomeric repeats frequently found in herpesviruses. Megablast and further investigative bioinformatics identified presence of Marek's disease virus (MDV), a Gallid alphaherpesvirus type 2 (GAHV-2), as the cause of the acute fatal infection. The source of infection may be attributed to a dead migratory flamingo found close to the duck enclosures three days prior to the outbreak; hence, GAHV-2 may also be responsible for the fatal infection of the flamingo accentuated by heat stress. Considering the possible spread of this highly contagious and lethal virus from a flamingo to the ducks, and the increasing zoonosis of animal viruses into humans, such as monkey B alphaherpesvirus transmission from macaques to humans with ~80% fatality, this observation has important ramifications for human health and safety of the poultry industry.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0280923</identifier><identifier>PMID: 36706167</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adolescent ; Adult ; Analysis ; Animals ; Appetite loss ; Aquatic birds ; Ataxia ; Biochemistry ; Bioinformatics ; Biology and Life Sciences ; Bird migration ; Chickens - genetics ; Degeneration ; Dehydrogenases ; Deoxyribonucleic acid ; Disease ; Disease Outbreaks - veterinary ; Diseases ; Distribution ; DNA ; DNA sequencing ; Ducks ; Ducks - genetics ; Ethylenediaminetetraacetic acid ; Follicles ; Formaldehyde ; Gene sequencing ; Genetic aspects ; Genomes ; Growth ; Heat stress ; Heat tolerance ; Hematology ; Herpes ; Herpes viruses ; Herpesviridae - genetics ; Herpesvirus 2, Gallid - genetics ; Herpesvirus diseases ; High-Throughput Nucleotide Sequencing ; Histopathology ; Humans ; Inclusion bodies ; Infection ; Infections ; Investigations ; Laboratories ; Leukocytes (eosinophilic) ; Liver ; Marek Disease - diagnosis ; Marek Disease - epidemiology ; Marek Disease - pathology ; Marek's disease ; Medicine and Health Sciences ; Mortality ; Muscles ; Necrosis ; Next-generation sequencing ; Nuclear safety ; Nucleotide sequencing ; Outbreaks ; Poultry Diseases ; Poultry farming ; Prevention ; Renal tubules ; Research and Analysis Methods ; Risk factors ; Spleen ; Viruses ; Waterfowl ; Zoonoses</subject><ispartof>PloS one, 2023-01, Vol.18 (1), p.e0280923-e0280923</ispartof><rights>Copyright: © 2023 Damir et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Damir 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>2023 Damir et al 2023 Damir et al</rights><rights>2023 Damir 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-b1e190ee225e0fbd33398c72c7b1acb96e4f41098ad27d7cdd8f391180d5def63</citedby><cites>FETCH-LOGICAL-c692t-b1e190ee225e0fbd33398c72c7b1acb96e4f41098ad27d7cdd8f391180d5def63</cites><orcidid>0000-0002-1081-3756</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/PMC9882916/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882916/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36706167$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Woźniakowski, Grzegorz</contributor><creatorcontrib>Damir, Hassan Abu</creatorcontrib><creatorcontrib>Ahmad, Waqar</creatorcontrib><creatorcontrib>Panicker, Neena G</creatorcontrib><creatorcontrib>Mohamed, Layla I</creatorcontrib><creatorcontrib>Omer, Elhag A</creatorcontrib><creatorcontrib>Kinne, Jörg</creatorcontrib><creatorcontrib>Wernery, Ulrich</creatorcontrib><creatorcontrib>Adem, Abdu</creatorcontrib><creatorcontrib>Ali, Mahmoud A</creatorcontrib><creatorcontrib>Mustafa, Farah</creatorcontrib><title>Investigation of a herpesvirus outbreak in mixed breeds of adult domestic ducks using next generation sequencing</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>This report characterizes the first lethal outbreak of Marek's disease on a large farm of mixed-breed adult ducks (&gt;18,000) and identifies the pathogen that resulted in high mortality (35%). Clinical signs included inappetence, respiratory distress, depression, muscle weakness, and ataxia. Post mortem revealed enlarged fragile liver mottled with miliary whitish spots and an enlarged spleen. Histopathology revealed hepatocellular necrosis with eosinophilic intra-nuclear inclusion bodies, necrosis of splenic follicles and degeneration/necrosis of renal tubules. The disease was tentatively diagnosed as a herpesvirus infection, confirmed by virus isolation from the liver. DNA was isolated from 15-year-old archival formalin-fixed tissues from infected ducks and subjected to next generation sequencing (NGS). Despite highly degraded DNA, short stretches of G- and C-rich repeats (TTAGGG and TAACCC) were identified as telomeric repeats frequently found in herpesviruses. Megablast and further investigative bioinformatics identified presence of Marek's disease virus (MDV), a Gallid alphaherpesvirus type 2 (GAHV-2), as the cause of the acute fatal infection. The source of infection may be attributed to a dead migratory flamingo found close to the duck enclosures three days prior to the outbreak; hence, GAHV-2 may also be responsible for the fatal infection of the flamingo accentuated by heat stress. Considering the possible spread of this highly contagious and lethal virus from a flamingo to the ducks, and the increasing zoonosis of animal viruses into humans, such as monkey B alphaherpesvirus transmission from macaques to humans with ~80% fatality, this observation has important ramifications for human health and safety of the poultry industry.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Analysis</subject><subject>Animals</subject><subject>Appetite loss</subject><subject>Aquatic birds</subject><subject>Ataxia</subject><subject>Biochemistry</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Bird migration</subject><subject>Chickens - genetics</subject><subject>Degeneration</subject><subject>Dehydrogenases</subject><subject>Deoxyribonucleic acid</subject><subject>Disease</subject><subject>Disease Outbreaks - 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(eosinophilic)</subject><subject>Liver</subject><subject>Marek Disease - diagnosis</subject><subject>Marek Disease - epidemiology</subject><subject>Marek Disease - pathology</subject><subject>Marek's disease</subject><subject>Medicine and Health Sciences</subject><subject>Mortality</subject><subject>Muscles</subject><subject>Necrosis</subject><subject>Next-generation sequencing</subject><subject>Nuclear safety</subject><subject>Nucleotide sequencing</subject><subject>Outbreaks</subject><subject>Poultry Diseases</subject><subject>Poultry farming</subject><subject>Prevention</subject><subject>Renal tubules</subject><subject>Research and Analysis Methods</subject><subject>Risk 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Damir, Hassan Abu</au><au>Ahmad, Waqar</au><au>Panicker, Neena G</au><au>Mohamed, Layla I</au><au>Omer, Elhag A</au><au>Kinne, Jörg</au><au>Wernery, Ulrich</au><au>Adem, Abdu</au><au>Ali, Mahmoud A</au><au>Mustafa, Farah</au><au>Woźniakowski, Grzegorz</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Investigation of a herpesvirus outbreak in mixed breeds of adult domestic ducks using next generation sequencing</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-01-27</date><risdate>2023</risdate><volume>18</volume><issue>1</issue><spage>e0280923</spage><epage>e0280923</epage><pages>e0280923-e0280923</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>This report characterizes the first lethal outbreak of Marek's disease on a large farm of mixed-breed adult ducks (&gt;18,000) and identifies the pathogen that resulted in high mortality (35%). Clinical signs included inappetence, respiratory distress, depression, muscle weakness, and ataxia. Post mortem revealed enlarged fragile liver mottled with miliary whitish spots and an enlarged spleen. Histopathology revealed hepatocellular necrosis with eosinophilic intra-nuclear inclusion bodies, necrosis of splenic follicles and degeneration/necrosis of renal tubules. The disease was tentatively diagnosed as a herpesvirus infection, confirmed by virus isolation from the liver. DNA was isolated from 15-year-old archival formalin-fixed tissues from infected ducks and subjected to next generation sequencing (NGS). Despite highly degraded DNA, short stretches of G- and C-rich repeats (TTAGGG and TAACCC) were identified as telomeric repeats frequently found in herpesviruses. Megablast and further investigative bioinformatics identified presence of Marek's disease virus (MDV), a Gallid alphaherpesvirus type 2 (GAHV-2), as the cause of the acute fatal infection. The source of infection may be attributed to a dead migratory flamingo found close to the duck enclosures three days prior to the outbreak; hence, GAHV-2 may also be responsible for the fatal infection of the flamingo accentuated by heat stress. Considering the possible spread of this highly contagious and lethal virus from a flamingo to the ducks, and the increasing zoonosis of animal viruses into humans, such as monkey B alphaherpesvirus transmission from macaques to humans with ~80% fatality, this observation has important ramifications for human health and safety of the poultry industry.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36706167</pmid><doi>10.1371/journal.pone.0280923</doi><tpages>e0280923</tpages><orcidid>https://orcid.org/0000-0002-1081-3756</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
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issn 1932-6203
1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS)
subjects Adolescent
Adult
Analysis
Animals
Appetite loss
Aquatic birds
Ataxia
Biochemistry
Bioinformatics
Biology and Life Sciences
Bird migration
Chickens - genetics
Degeneration
Dehydrogenases
Deoxyribonucleic acid
Disease
Disease Outbreaks - veterinary
Diseases
Distribution
DNA
DNA sequencing
Ducks
Ducks - genetics
Ethylenediaminetetraacetic acid
Follicles
Formaldehyde
Gene sequencing
Genetic aspects
Genomes
Growth
Heat stress
Heat tolerance
Hematology
Herpes
Herpes viruses
Herpesviridae - genetics
Herpesvirus 2, Gallid - genetics
Herpesvirus diseases
High-Throughput Nucleotide Sequencing
Histopathology
Humans
Inclusion bodies
Infection
Infections
Investigations
Laboratories
Leukocytes (eosinophilic)
Liver
Marek Disease - diagnosis
Marek Disease - epidemiology
Marek Disease - pathology
Marek's disease
Medicine and Health Sciences
Mortality
Muscles
Necrosis
Next-generation sequencing
Nuclear safety
Nucleotide sequencing
Outbreaks
Poultry Diseases
Poultry farming
Prevention
Renal tubules
Research and Analysis Methods
Risk factors
Spleen
Viruses
Waterfowl
Zoonoses
title Investigation of a herpesvirus outbreak in mixed breeds of adult domestic ducks using next generation sequencing
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