{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T23:57:43Z","timestamp":1793318263955,"version":"4.5.0"},"reference-count":41,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,6,28]],"date-time":"2022-06-28T00:00:00Z","timestamp":1656374400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>In the last 40 years, low pathogenic avian influenza virus (LPAIV) subtype H9N2 has been endemic in most Middle Eastern countries and of course Egypt which is one of the biggest poultry producers in the middle east region. The major losses with the H9N2 virus infections come from complicated infections in commercial broiler chickens, especially <jats:italic>E. coli<\/jats:italic> infection. In this work, 2,36,345 Arbor acres broiler chickens from the same breeder flock were placed equally in four pens, where two pens were vaccinated against LPAIV of subtype H9N2 virus, and the other two pens served as non-vaccinated controls. All were placed on the same farm under the same management conditions. A total of twenty birds from each pen were moved to biosafety level\u22123 chicken isolators (BSL-3) on days 21 and 28 of life and challenged with LPAIV-H9N2 or <jats:italic>E. coli<\/jats:italic>. Seroconversion for H9N2 was evaluated before and after the challenge. The recorded results revealed a significant decrease in clinical manifestations and virus shedding in terms of titers of shedding virus and number of shedders in vaccinated compared to non-vaccinated chickens. In groups early infected with LPAIV-H9N2 virus either vaccinated or not vaccinated, there was no significant difference in clinical sickness or mortalities in both groups, but in late infection groups with H9N2 alone, non-vaccinated infected group showed significantly higher clinical sickness in comparison with infected vaccinated group but also without mortality. In groups co-infected with <jats:italic>E. coli<\/jats:italic> (I\/M) and H9N2, it showed 100% mortalities either in vaccinated or non-vaccinated H9N2 groups and thus reflect the high pathogenicity of used <jats:italic>E. coli<\/jats:italic> isolates, whereas in groups co-infected with <jats:italic>E. coli<\/jats:italic> (per os to mimic the natural route of infection) and LPAIV-H9N2, mortality rates were significantly higher in non-vaccinated groups than those vaccinated with H9N2 vaccine (15 vs. 5%). In conclusion, the use of the LPAIV H9N2 vaccine has significantly impacted the health status, amount of virus shed, and mortality of challenged commercial broilers, as it can minimize the losses and risks after co-infection with <jats:italic>E. coli<\/jats:italic> (orally) and LPAIV-H9N2 virus under similar natural route of infection in commercial broilers.<\/jats:p>","DOI":"10.3389\/fvets.2022.918440","type":"journal-article","created":{"date-parts":[[2022,6,28]],"date-time":"2022-06-28T06:59:45Z","timestamp":1656399585000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":16,"title":["Effect of Co-infection of Low Pathogenic Avian Influenza H9N2 Virus and Avian Pathogenic E. coli on H9N2-Vaccinated Commercial Broiler Chickens"],"prefix":"10.3389","volume":"9","author":[{"given":"Sherif I. A.","family":"Mahmoud","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kamel A.","family":"Zyan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed M.","family":"Hamoud","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eman","family":"Khalifa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shahin","family":"Dardir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rabab","family":"Khalifa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walid H.","family":"Kilany","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wael K.","family":"Elfeil","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,6,28]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"3320","DOI":"10.1017\/S0950268817002576","article-title":"A Brief summary of the epidemiology and genetic relatedness of avian influenza h9n2 virus in birds and mammals in the middle East and North Africa","volume":"145","author":"Nagy","year":"2017","journal-title":"Epidemiol Infect."},{"key":"B2","doi-asserted-by":"publisher","first-page":"18745","DOI":"10.1038\/srep18745","article-title":"Antigenic mapping of an H9n2 avian influenza virus reveals two discrete antigenic sites and a novel mechanism of immune escape","volume":"6","author":"Peacock","year":"2016","journal-title":"Sci Rep."},{"key":"B3","doi-asserted-by":"publisher","first-page":"13432","DOI":"10.1128\/JVI.05266-11","article-title":"Indications that live poultry markets are a major source of human H5N1 influenza virus infection in China","volume":"85","author":"Wan","year":"2011","journal-title":"J Virol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1167","DOI":"10.1007\/s00705-012-1269-z","article-title":"Isolation of H9n2 avian influenza virus from bobwhite quail. (Colinus Virginianus) in Egypt","volume":"157","author":"El-Zoghby","year":"2012","journal-title":"Archives virology."},{"key":"B5","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1007\/s11250-012-0243-9","article-title":"Serological surveillance reveals widespread influenza a H7 and H9 subtypes among chicken flocks in Egypt","volume":"45","author":"Afifi","year":"2013","journal-title":"Trop Anim Health Prod."},{"key":"B6","doi-asserted-by":"publisher","first-page":"308","DOI":"10.21608\/jvmr.2017.43266","article-title":"Epidemiology of viral components causing respiratory problems in broilers in six egyptian governorates","volume":"24","author":"Taher","year":"2017","journal-title":"J Vet Med Res."},{"key":"B7","doi-asserted-by":"publisher","first-page":"444","DOI":"10.3382\/ps.2007-00415","article-title":"Molecular survey of avian respiratory pathogens in commercial broiler chicken flocks with respiratory diseases in Jordan","volume":"87","author":"Roussan","year":"2008","journal-title":"Poult Sci."},{"key":"B8","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1007\/s00705-008-0033-x","article-title":"Coinfection of avian influenza virus. (H9n2 Subtype) with infectious bronchitis live vaccine","volume":"153","author":"Haghighat-Jahromi","year":"2008","journal-title":"Archives virology."},{"key":"B9","doi-asserted-by":"crossref","DOI":"10.1002\/9781119371199","volume-title":"Diseases of Poultry","author":"Swayne","year":"2020"},{"key":"B10","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1515\/jvetres-2017-0035","article-title":"Pathological alterations in respiratory system during co-infection with low pathogenic avian influenza virus (H9N2) and escherichia coli in broiler chickens","volume":"61","author":"Jaleel","year":"2017","journal-title":"J veterinary research."},{"key":"B11","doi-asserted-by":"publisher","first-page":"183","DOI":"10.21608\/zvjz.2014.59483","article-title":"Studies on virulence genes of e. coli from different sources and their relation to antibiotic resistance pattern","volume":"42","author":"Ammar","year":"2014","journal-title":"Zagazig Veterinary J."},{"key":"B12","doi-asserted-by":"publisher","first-page":"152","DOI":"10.4172\/1747-0862.1000027","article-title":"Molecular quantitation of H9N2 avian influenza virus in various organs of broiler chickens using taqman real time pcr","volume":"3","author":"Mosleh","year":"2009","journal-title":"J Mol Genet Med."},{"key":"B13","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1111\/tbed.13281","article-title":"Respiratory disease due to mixed viral infections in poultry flocks in egypt between 2017 and 2018: upsurge of highly pathogenic avian influenza virus subtype H5n8 since 2018","volume":"68","author":"Hassan","year":"2019","journal-title":"Transbound Emerg Dis."},{"key":"B14","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.vetmic.2017.11.003","article-title":"Screening host proteins required for bacterial adherence after H9N2 virus infection","volume":"213","author":"Ma","year":"2018","journal-title":"Vet Microbiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"670688","DOI":"10.3389\/fmicb.2021.670688","article-title":"Co-infection of h9n2 influenza a virus and escherichia coli in a Balb\/C mouse model aggravates lung injury by synergistic effects","volume":"12","author":"Wang","year":"2021","journal-title":"Frontiers microbiology"},{"key":"B16","first-page":"86","article-title":"Evaluation of the timing of the escherichia coli co-infection on pathogenecity of h9n2 avian influenza virus in broiler chickens","volume":"18","author":"Mosleh","year":"2017","journal-title":"Iranian j veterinary research."},{"key":"B17","doi-asserted-by":"publisher","first-page":"980","DOI":"10.1093\/oxfordjournals.jbchem.a022216","article-title":"Escherichia coli prlc gene encodes a trypsin-like proteinase regulating the cell cycle","volume":"124","author":"Jiang","year":"1998","journal-title":"J Biochem."},{"key":"B18","doi-asserted-by":"publisher","first-page":"712","DOI":"10.1177\/030098588602300610","article-title":"Lymphocytic depletion of bursa of fabricius and thymus in chickens inoculated with escherichia coli","volume":"23","author":"Nakamura","year":"1986","journal-title":"Vet Pathol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2","DOI":"10.4081\/vsd.2014.5416","article-title":"Evaluation of the effect of simultaneous infection with e. coli O2 and H9N2 influenza virus on inflammatory factors in broiler chickens","volume":"4","author":"Dadras","year":"2014","journal-title":"Veterinary Science Development"},{"key":"B20","first-page":"317","article-title":"Standardisation of a new model of H9n2\/escherichia coli challenge in broilers in the lebanon","volume":"45","author":"Barbour","year":"2009","journal-title":"Vet Ital."},{"key":"B21","article-title":"Newcastle Disease. In: 2012 VabtWaoDotOi, editor","volume-title":"Oie Manual of Standers for Diagnosis Test and Vaccines","year":"2012"},{"key":"B22","volume-title":"Manual of Diagnostic Tests and Vaccines for Terrestrial Animals- Avian Influenza. Oie Terrestrial Manual 2015","year":"2015"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/ani10101875","article-title":"Comparison of the effectiveness of two different vaccination regimes for avian influenza H9N2 in broiler chicken","volume":"10","author":"Talat","year":"2020","journal-title":"Animals."},{"key":"B24","first-page":"369","article-title":"Experimental infection of chickens by avian influenza H9n2 virus: monitoring of tissue tropism and pathogenicity","volume":"78","author":"Elfeil","year":"2018","journal-title":"J Egypt Vet Med Assoc."},{"key":"B25","article-title":"The Protective Role of Coli-Vac, a Heptavalent Vaccine against Extraintestinal Avian Pathogenic Escherichia Coli. (Apec) Infection","volume-title":"American Assocaition of Avian Pthologist 2022-Meeting","author":"Elfeil","year":"2022"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1559","DOI":"10.1038\/nprot.2006.236","article-title":"Quantification of mrna using real-time rt-pcr","volume":"1","author":"Nolan","year":"2006","journal-title":"Nat Protoc."},{"key":"B27","doi-asserted-by":"publisher","first-page":"304","DOI":"10.3390\/pathogens11030304","article-title":"Experimental infection and in-contact transmission of H9N2 avian influenza virus in crows","volume":"11","author":"Verma","year":"2022","journal-title":"Pathogens"},{"key":"B28","volume-title":"Principles and Procedures of Statics","author":"Steel","year":"1960"},{"key":"B29","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1016\/j.bjbas.2018.07.005","article-title":"Pathogenicity of escherichia coli O157 in commercial broiler chickens","volume":"7","author":"El-Sawah","year":"2018","journal-title":"beni-suef university. J Basic Applied Sciences."},{"key":"B30","article-title":"Evaluation protection of H5 vaccination regimes in commercail broilers with maternal immunity against early challenge with HPAI-H5N1. International Poultry Scientific Forum (IPSF); Georgia World Congress Center","author":"Elfeil","year":"2022","journal-title":"Atlanta, Georgia: Southern Poultry Science Society, USA"},{"key":"B31","first-page":"50","article-title":"The effect of some pathogenic bacterial proteases on avian influenza viruses H5N1 and H9N2","volume":"5","author":"Awwad","year":"2018","journal-title":"European J Pharmaceutical Medical Research."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1388","DOI":"10.3382\/ps.2008-00549","article-title":"Proteolytic bacteria in the lower digestive tract of poultry may affect avian influenza virus pathogenicity","volume":"88","author":"King","year":"2009","journal-title":"Poult Sci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/2049-632X.12053","article-title":"Activation of influenza viruses by proteases from host cells and bacteria in the human airway epithelium","volume":"69","author":"B\u00f6ttcher-Friebertsh\u00e4user","year":"2013","journal-title":"Pathog Dis."},{"key":"B34","volume-title":"Protective Efficacy of Mefluvac H9 in Turkey Poults in Both Lab and Field Condition. XXI-World Veterinary Poultry Association Congress","author":"Elfeil","year":"2019"},{"key":"B35","doi-asserted-by":"publisher","first-page":"29","DOI":"10.3390\/vaccines10010029","article-title":"Efficacy of the newcastle disease virus genotype vii11-matched vaccines in commercial broilers","volume":"10","author":"Sultan","year":"2022","journal-title":"Vaccines"},{"key":"B36","doi-asserted-by":"publisher","first-page":"677","DOI":"10.14202\/vetworld.2019.677-683","article-title":"Prevalence, molecular typing, and antimicrobial resistance of bacterial pathogens isolated from ducks","volume":"12","author":"Eid","year":"2019","journal-title":"Veterinary World."},{"key":"B37","doi-asserted-by":"publisher","first-page":"350","DOI":"10.3923\/ajava.2016.350.356","article-title":"Genetic variation among avian pathogenic e. coli strains isolated from broiler chickens Asian","volume":"11","author":"Eid","year":"2016","journal-title":"J Animal Veterinary Advances."},{"key":"B38","doi-asserted-by":"publisher","first-page":"2163","DOI":"10.12681\/jhvms.23645","article-title":"Correlation between Es\u03b2l salmonella serovars isolated from broilers and their virulence genes","volume":"71","author":"Rady","year":"2020","journal-title":"J Hellenic Veterinary Medical Society."},{"key":"B39","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1016\/j.rvsc.2017.06.024","article-title":"Experimental co-infection of infectious bronchitis and low pathogenic avian influenza H9N2 viruses in commercial broiler chickens","volume":"115","author":"Hassan","year":"2017","journal-title":"Res Vet Sci."},{"key":"B40","doi-asserted-by":"publisher","first-page":"76","DOI":"10.3844\/ajavsp.2018.76.86","article-title":"Variations in pathogenicity and molecular characterization of infectious bursal disease virus. (IBDV) in Egypt","volume":"13","author":"Sedeik","year":"2018","journal-title":"AmJ Animal Veterinary Sciences."},{"key":"B41","volume-title":"Evaluation Protection of H5 Vaccination Regimes Against Early Challenge with Hpai-H5N8 Clade 2.3.4.4.","author":"Elfeil","year":"2022"}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.918440\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,6,28]],"date-time":"2022-06-28T06:59:56Z","timestamp":1656399596000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.918440\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,28]]},"references-count":41,"alternative-id":["10.3389\/fvets.2022.918440"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2022.918440","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,28]]},"article-number":"918440"}}