DETECTION OF DNA ALTERATIONS IN MUSCOVY DUCKS (CAIRINA MOSCHATA) NATURALLY INFECTED WITH HIGHLY PATHOGENIC AVIAN INFLUENZA VIRUS SUBTYPE H5N1

Authors

  • Iman E. El-Araby
  • Reham M. ElBakrey
  • Haytham Ali
  • Mahmoud H.A. Mohamed
  • Shimaa M.G. Mansour
  • Amal A.M. Eid

DOI:

https://doi.org/10.26873/SVR-660-2018

Abstract

Highly pathogenic avian influenza virus (HPAIV) subtype H5N1 is circulating in Egypt since 2006, with escalating apprehension about its possibility to become more transmissible amongst humans. In this study, three serial outbreaks of HPAIV H5N1 in domestic Muscovy ducks in Sharkia Governorate, Egypt were investigated. Nervous signs with 62% mortality were observed in Muscovy ducklings. Gross examination revealed severely congested meningeal vessels, hemorrhages on the duodenum, pancreas, and coronary fat. Perivascular lymphocytic cuffing, gliosis and vacuolation of the neuropil were observed in the brain microscopically. Viral antigens were identified in the neurons and the glial cells of the cerebral cortex, submucosal Meissner's plexus neurons of the intestine and the hepatic Kupffer cells by immunohistochemistry. The HPAIV subtype H5N1 was isolated from different duck tissues in 66.7% of examined duck samples. Using RAPD-PCR fingerprinting, there were different patterns in the DNA of Muscovy ducks naturally infected with AIV (24, 48 and 72 hours post appearance of clinical signs) compared to uninfected birds. Differences in RAPD-PCR profiles between infected and uninfected ducks, and genomic instability percent (37.7%±1.76) pointed to the incidence of DNA alterations induced at 24 hours following the appearance of clinical signs. Further in vivo and in vitro experiments need to be done to determine the relative importance of these findings.

Key words: GTS %; H5N1; RAPD-PCR; Egypt

References

(1) Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO. New world bats harbor diverse influenza A viruses. PLOS Pathogen 2013; 9:e1003657.

(2) Swayne DE, Suarez DL. Highly pathogenic avian influenza. Revue Scientifique et Technique 2000; 19: 463–82.

(3) Abdelwhab EM, Selim AA, Arafa A, Galal S, Kilany WH, Hassan MK, Aly MM, Hafez MH. Circulation of avian influenza H5N1 in live bird markets in Egypt. Avian Dis 2010; 54: 911–4.

(4) WHO. “H5N1 avian influenza: Timeline of major events.†[Online]. Available: 2011; Accessed December 13, 2011.

(5) Albrecht T, Fons M, Boldogh I, Rabson, AS. Effects on Cells. In: Medical Microbiology, 4th ed S Baron (ed) University of Texas Medical Branch at Galveston, Galveston (TX) publishers 1996; Chapter 44.

(6) Kim JK, Negovetich NJ, Forrest HL, Webster RG. Ducks: the ‘‘Trojan horses’’ of H5N1 influenza. Influenza and Other Respiratory Viruses 2009; 3: 121–8.

(7) Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons R, Holmes EC, Taubenberger JK. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathogen 2008; 4(5):e1000076.

(8) Abdelwhab EM, Arafa AS, Stech J, Grund C, Stech O, Graeber-Gerberding M, Beer M, Hassan MK, Aly MM, Harder TC, Hafez HM. Diversifying evolution of highly pathogenic H5N1 avian influenza virus in Egypt from 2006 to 2011. Virus genes 2012; 45: 14–23.

(9) Arafa A, Suarez D, Kholosy SG, Hassan MK, Nasef S, Selim A, Dauphin G, Kim M, Yilma J, Swayne D, Aly MM. Evolution of highly pathogenic avian influenza H5N1 viruses in Egypt indicating progressive adaptation. Arch Virol 2012; 157: 1931–47.

(10) El-Zoghby EF, Aly MM, Nasef SA, Hassan MK, Arafa AS, Selim AA, Kholousy SG, Kilany WH, Safwat M, Abdelwhab EM, Hafez HM. Surveillance on A/H5N1 virus in domestic poultry and wild birds in Egypt. Virol J 2013; 10: 203.

(11) Swayne DE, Halvorson, DA. Influenza. In: Diseases of poultry, 12th ed YM Saif, JR Glisson, AM Fadly, LR McDougald, L Nolan (ed) Blackwell, Ames, Iowa 2008; 153–84.

(12) Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV. DNA polymorphism amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 1990; 18: 6531–35.

(13) Yamamoto K, Murakami R, Takamura Y. Differentiation of thermophilic anaerobic gram positive bacteria by random amplified polymorphic DNA analysis. Microbes and Environments 2001; 16: 91–9.

(14) Mollah MBR, Islam FB, Islam MS, Ali MA, Alam MS. Analysis of genetic diversity in Bangladeshi chicken using RAPD markers. Biotechnology 2009; 8: 462–7.

(15) OIE. “Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Chapter 2.3.4).†[Online]. Available: http://www.oie.int/en/intern ational-standard-setting/terrestrial-manual/access-online/. 2012; Accessed May 25, 2013.

(16) Njouom R, Aubin JT, Bella AL, Demsa BM, Rouquet P, Gake B, Ngangnou A, Foupoua-pouognigni Y, Van Der Werf S, Rocourt J, Rousset D. Highly pathogenic avian influenza virus subtype H5N1 in ducks in the Northern part of Cameroon. Vet Microbiol 2008; 130: 380–4.

(17) Tsukamoto K, Ashizawa T, Nakanishi K, Kaji N, Suzuki K, Shishido M, Okamatsu M, Mase M. Use of reverse transcriptase PCR to subtype N1 to N9 neuraminidase genes of avian influenza viruses. J Clin Microbiol 2009; 47: 2301–3.

(18) Kim MC, Kwon YK, Joh SJ, Kwon JH, Kim JH, Kim SJ. Development of one-step reverse transcriptase-polymerase chain reaction to detect duck hepatitis virus type 1. Avian Dis 2007; 51: 540–5.

(19) Perkins LEL, Swayne DE. Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Vet Pathol 2001; 38: 149–64.

(20) Liu W, Yang YS, Zhou Q, Xie L, Li P, Sun T. Impact assessment of cadmium contamination on rice (Oryza sativa L.) seedlings at molecular and population levels using multiple biomarkers. Chemosphere 2007; 67:1155–63.

(21) Phuong DQ, Dung NT, Jørgensen PH, Handberg KJ, Vinh NT, Christensen JP. Susceptibility of Muscovy (Cairina moschata) and mallard ducks (Anas platyrhynchos) to expe-rimental infections by different genotypes of H5N1 avian influenza viruses. Vet Microbiol 2011; 148: 168–74.

(22) Wasilenko JL, Arafa AM, Selim AA, Hassan MK, Aly MM, Ali A, Nassif S, Elebiary E, Balish A, Klimov A, Suarez DL, Swayne DE, Pantin-Jackwood MJ. Pathogenicity of two Egyptian H5N1 highly pathogenic avian influenza viruses in domestic ducks. Arch Virol 2011; 156: 37–51.

(23) Cagle C, To TL, Nguyen T, Wasilenko J, Adams SC, Cardona CJ, Spackman E, Suarez DL, Pantin-Jackwood MJ. Pekin and Muscovy ducks respond differently to vaccination with a H5N1 highly pathogenic avian influenza (HPAI) commercial inactivated vaccine. Vaccine 2011; 29: 6549–57.

(24) Cagle C, Wasilenko J, Adams SC, Cardona CJ, To TL, Nguyen T, Spackman E, Suarez DL, Smith D, Shepherd E, Roth J, Pantin-Jackwood MJ. Differences in pathogenicity, response to vaccination, and innate immune responses in different types of ducks infected with a virulent H5N1 highly pathogenic avian influenza virus from Vietnam. Avian Dis 2012; 56: 479–87.

(25) Pantin-Jackwood M, Swayne DE, Smith D, Shepherd E. Effect of species, breed and route of virus inoculation on the pathogenicity of H5N1 highly pathogenic influenza (HPAI) viruses in domestic ducks. Vet Res 2013; 44: 62.

(26) Arafa AS, Naguib MM, Luttermann C, Selim AA, Kilany WH, Hagag N, Samy A, Abdelhalim A, Hassan MK, Abdelwhab EM, Makonnen Y, Dauphin G, Lubroth J, Mettenleiter TC, Beer M, Grund C, Harder TC. Emergence of a novel cluster of influenza A (H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Euro Surveill 2015; 20: 2–8.

(27) Capua I, Marangon S, Selli L, Alexander DJ, Swayne DE, Pozza MD, Parenti E, Cancellotti FM. Outbreaks of highly pathogenic avian influenza (H5N2) in Italy during October 1997–January 1998. Avian Pathol 1999; 28: 455–60.

(28) Capua I, Mutinelli F,Terregino C, Cattoli G, Manvell RJ, Burlini F. Highly pathogenic avian influenza (H7N1) in ostriches farmed in Italy. Vet Rec 2000; 146: 356.

(29) Swayne DE, Pantin-Jackwood MJ. Pathogenicity of avian influenza viruses in poultry. Dev Biol (Basel) 2006; 124: 61–7.

(30) Pfeiffer J, Pantin-Jackwood M, To T, Nguyen T, Suarez D. Phylogenetic and biological characterization of highly pathogenic H5N1 avian influenza viruses (Vietnam 2005) in chickens and ducks. Virus Res 2009; 142 :108–20.

(31) Tang Y, Wu P, Peng D, Wang X, Wan H, Zhang P, Long J, Zhang W, Li Y, Wang W, Zhang X, Liu X. Characterization of duck H5N1 influenza viruses with differing pathogenicity in mallard (Anas platyrhynchos) ducks. Avian Pathol 2009; 38: 457–67.

(32) Goletic T, Gagic A, Rešidbegovic E, Kustura A, Kavazovic A, Savic V, Harder T, Starick E, Prasovic S. Highly pathogenic avian influenza virus subtype H5N1 in mute swans (Cygnus olor) in central Bosnia. Avian Dis 2010; 54(1 Suppl): 496–501.

(33) Pantin-Jackwood MJ, Suarez DL, Spackman E, Swayne DE. Age at infection affects the pathogenicity of Asian highly pathogenic avian influenza H5N1 viruses in ducks. Virus Res 2007; 130: 151–61.

(34) Pantin-Jackwood MJ, Swayne DE. Patho-biology of Asian highly pathogenic avian influenza H5N1 virus infections in ducks. Avian Dis 2007; 51: 250–9.

(35) Bröjer C, Ågren EO, Uhlhorn H, Bernodt K, Mörner T, Jansson DS, Mattsson R, Zohari S, Thorén P, Berg M, Gavier-Widén D. Pathology of natural highly pathogenic avian influenza H5N1 infection in wild tufted ducks (Aythya fuligula). J Vet Diagn Invest 2009; 21: 579–87.

(36) Hagag IT, Mansour SM, Zhang Z, Ali AA, Ismaiel EM, Salama AA, Cardona CJ, Collins J, Xing Z. Pathogenicity of highly pathogenic avian influenza virus H5N1 in naturally infected poultry in Egypt. PLoS One 2015; 10: e0120061.

(37) Mansour SMG, Ali H, ElBakrey RM, El-Araby IE, Knudsen DEB, Eid AAM. Co-infection of highly pathogenic avian influenza and duck hepatitis viruses in Egyptian backyard and commercial ducks. International Journal of Veterinary Science and Medicine 2018; doi.org/10.1016/j.ijvsm.2018.07.004

(38) Rocco L, Valentino IV, Peluso C, Stingo V. Genomic Template Stability Variation in Zebrafish Exposed to Pharmacological Agents. IJEP 2013; 3: 1–6.

(39) Atienzar FA, Venier P, Jha AN, Depledge MH. Evaluation of the random amplified polymorphic DNA (RAPD) assay for the detection of DNA damage and mutations. Mutat Res 2002; 521: 151–63.

(40) Zhiyi R, Haowen Y. A method for geno-toxicity detection using random amplified polymo-rphisms DNA with Danio rerio. Ecotoxicol Environ Saf 2004; 58: 96–103.

(41) Atienzar FA, Jha AN. The random amplified polymorphic DNA (RAPD) techniques applied to genotoxicity and carcinogenesis studies: A critical review. Mutat Res 2006; 613: 76–102.

(42) Atienzar FA, Cordi B, Evenden AJ. Qualitative assessment of genotoxicity using random amplified polymorphic DNA: comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Environ. Toxicol Chem 1999; 18: 2275–82.

(43) Rocco L, Izzo A, Zito G, Peluso C, Stingo V. Genotoxicity in zebrafish (Danio rerio) exposed to two pharmacological products from an impacted Italian river. J Environ Anal Toxicol 2011; 1: 103.

(44) Akaike T, Noguchi Y, Ijiri S, Setoguchi K, Suga M, Zheng YM, Dietzschold B, Maeda H. Pathogenesis of influenza virus-induced pneumonia: Involvement of both nitric oxide and oxygen radicals. Proc Natl Acad Sci USA 1996; 93: 2448–53.

(45) Brydon EW, Morris SJ, Sweet C. Role of apoptosis and cytokines in influenza virus morbi-dity. FEMS Microbiol Rev 2005; 29: 837–50.

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2018-11-10

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