arboviruses; biosecurity; bluetongue; orbivirus; oryx; vector-borne disease; Immunology and Allergy; Molecular Biology; Immunology and Microbiology (all); Microbiology (medical); Infectious Diseases; General Immunology and Microbiology
Abstract :
[en] From 1975 to 2021, the United Arab Emirates (UAE) imported more than 1300 live Arabian oryxes (AOs) and scimitar-horned oryxes (SHOs) for conservation programs. The objective of this study was to estimate the prevalence of orbiviruses Bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV) in AOs and SHOs from captive herds in the UAE. Between October 2014 and April 2015, 16 AOs and 13 SHOs originating from Texas (USA) and 195 out of about 4000 SHOs from two locations in the UAE were blood sampled to be tested by indirect enzyme-linked immunosorbent assay (ELISA) and real-time reverse transcriptase polymerase chain reaction (RT-qPCR) assays. Eight imported AOs (50% CI [24.7-75.4%]) and eight imported SHOs (61.5% CI [31.6-86.1%]) were found BTV seropositive, in contrast with three out of 195 SHOs (1.5% CI [0.3-4.4%]) from the Emirates. BTV-2 genome was detected in 6/16 of the Arabian Oryx, and amongst those, one out of six was seronegative. None of the tested samples was found positive for EHDV. Our results illustrate the wide local variation regarding BTV seroprevalence in domestic and wild ruminants in the Arabian Peninsula. These results stress the need for pre-import risk assessment when considering translocation of wild ruminant species susceptible to orbiviruses not only in the country of destination but also where transit happens.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Martinelle, Ludovic ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Productions animales durables
Haegeman, Andy ; Sciensano, Infectious Diseases in Animals, Exotic and Particular Diseases, 1050 Brussels, Belgium
Lignereux, Louis ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) ; School of Animal and Veterinary Sciences, University of Adelaide, Adelaide, SA 5005, Australia
Chaber, Anne-Lise ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires ; School of Animal and Veterinary Sciences, University of Adelaide, Adelaide, SA 5005, Australia
Dal Pozzo, Fabiana; CARE-FEPEX Experimental Station, Fundamental and Applied Research for Animals & Health (FARAH) Center, Faculty of Veterinary Medicine, University of Liege, 4000 Liege, Belgium
De Leeuw, Ilse; Sciensano, Infectious Diseases in Animals, Exotic and Particular Diseases, 1050 Brussels, Belgium
De Clercq, Kris ; Sciensano, Infectious Diseases in Animals, Exotic and Particular Diseases, 1050 Brussels, Belgium
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Language :
English
Title :
Orbivirus Screening from Imported Captive Oryx in the United Arab Emirates Stresses the Importance of Pre-Import and Transit Measures.
Ahmed, S.; Mahmoud, M.A.E.; Viarouge, C.; Sailleau, C.; Zientara, S.; Breard, E. Presence of bluetongue and epizootic hemorrhagic disease viruses in Egypt in 2016 and 2017. Infect. Genet. Evol. 2019, 73, 221–226. [CrossRef]
Mellor, P.S.; Boorman, J.; Baylis, M. Culicoides biting midges: Their role as arbovirus vectors. Ann. Rev. Entomol. 2000, 45, 307–340. [CrossRef]
Johnson, D.J.; Ostlund, E.N.; Stallknecht, D.E.; Goekjian, V.H.; Jenkins-Moore, M.; Harris, S.C. First report of bluetongue virus serotype 1 isolated from a white-tailed deer in the United States. J. Vet. Diagn. Investig. 2006, 18, 398–401. [CrossRef]
Parsonson, I.M. Pathology and pathogenesis of bluetongue infections. Curr. Top. Microbiol. Immunol. 1990, 162, 119–141. [CrossRef]
Drolet, B.S.; Reister-Hendricks, L.M.; Podell, B.K.; Breitenbach, J.E.; McVey, D.S.; van Rijn, P.A.; Bowen, R.A. European bluetongue serotype 8: Disease threat assessment for U.S. sheep. Vector Borne Zoonotic Dis. 2016, 16, 400–407. [CrossRef]
Maclachlan, N.J.; Drew, C.P.; Darpel, K.E.; Worwa, G. The pathology and pathogenesis of bluetongue. J. Comp. Pathol. 2009, 141, 1–16. [CrossRef]
Wilson, A.J.; Mellor, P.S. Bluetongue in Europe: Past, present and future. Philos. Trans. R. Soc. B Biol. Sci. 2009, 364, 2669–2681. [CrossRef]
Dahiya, S.; Prasad, G.; Kovi, R.C. VP2 gene based phylogenetic relationship of Indian isolates of Bluetongue virus serotype 1 and other serotypes from different parts of the world. DNA Seq. 2004, 15, 351–361. [CrossRef]
Ries, C.; Beer, M.; Hoffmann, B. BlueTYPE—A low density TaqMan-RT-qPCR array for the identification of all 24 classical Bluetongue virus serotypes. J. Virol. Methods 2020, 282, 113881. [CrossRef]
Ries, C.; Vogtlin, A.; Hussy, D.; Jandt, T.; Gobet, H.; Hilbe, M.; Burgener, C.; Schweizer, L.; Hafliger-Speiser, S.; Beer, M.; et al. Putative novel atypical BTV serotype ’36’ identified in small ruminants in Switzerland. Viruses 2021, 13, 721. [CrossRef]
Anthony, S.J.; Maan, S.; Maan, N.; Kgosana, L.; Bachanek-Bankowska, K.; Batten, C.; Darpel, K.E.; Sutton, G.; Attoui, H.; Mertens, P.P. Genetic and phylogenetic analysis of the outer-coat proteins VP2 and VP5 of epizootic haemorrhagic disease virus (EHDV): Comparison of genetic and serological data to characterise the EHDV serogroup. Virus Res. 2009, 145, 200–210. [CrossRef]
Mendiola, S.Y.; Mills, M.K.; Maki, E.; Drolet, B.S.; Wilson, W.C.; Berghaus, R.; Stallknecht, D.E.; Breitenbach, J.; McVey, D.S.; Ruder, M.G. EHDV-2 infection prevalence varies in Culicoides sonorensis after feeding on infected white-tailed deer over the course of viremia. Viruses 2019, 11, 371. [CrossRef]
Frolich, K.; Hamblin, C.; Jung, S.; Ostrowski, S.; Mwanzia, J.; Streich, W.J.; Anderson, J.; Armstrong, R.M.; Anajariyah, S. Serologic surveillance for selected viral agents in captive and free-ranging populations of Arabian oryx (Oryx leucoryx) from Saudi Arabia and the United Arab Emirates. J. Wildl. Dis. 2005, 41, 67–79. [CrossRef]
Henderson, D.S. Were they the last arabian oryx? Oryx 1974, 12, 347–350. [CrossRef]
Woodfine, T.; Gilbert, T. The fall and rise of the scimitar-horned oryx: A case study of ex-situ conservation and reintroduction in practice. In Antelope Conservation: From Diagnosis to Action, 1st ed.; Bro-Jorgensen, J., Mallon, D.P., Eds.; Wiley-Blackwell: Hoboken, NJ, USA, 2016; p. 376. [CrossRef]
Courtejoie, N.; Durand, B.; Bournez, L.; Gorlier, A.; Breard, E.; Sailleau, C.; Vitour, D.; Zientara, S.; Baurier, F.; Gourmelen, C.; et al. Circulation of bluetongue virus 8 in French cattle, before and after the re-emergence in 2015. Transbound. Emerg. Dis. 2018, 65, 281–284. [CrossRef]
Caporale, M.; Di Gialleonorado, L.; Janowicz, A.; Wilkie, G.; Shaw, A.; Savini, G.; Van Rijn, P.A.; Mertens, P.; Di Ventura, M.; Palmarini, M. Virus and host factors affecting the clinical outcome of bluetongue virus infection. J. Virol. 2014, 88, 10399–10411. [CrossRef]
Haegeman, A.; Vandaele, L.; De Leeuw, I.; Oliveira, A.P.; Nauwynck, H.; Van Soom, A.; De Clercq, K. Failure to remove bluetongue serotype 8 virus (BTV-8) from in vitro produced and in vivo derived bovine embryos and subsequent transmission of to recipient cows after embryo transfer. Front. Vet. Sci. 2019, 6, 432. [CrossRef]
Saegerman, C.; Berkvens, D.; Mellor, P.S. Bluetongue epidemiology in the European Union. Emerg. Infect. Dis. 2008, 14, 539–544. [CrossRef]
Shimshony, A. Bluetongue in Israel—A brief historical overview. Vet. Ital. 2004, 40, 116–118.
United States Department of Agriculture. Bluetongue Standard Operating Procedures: Overview of Etiology and Ecology; US Department of Agriculture: Riverdale, MD, USA, 2016.
Gaudreault, N.N.; Mayo, C.E.; Jasperson, D.C.; Crossley, B.M.; Breitmeyer, R.E.; Johnson, D.J.; Ostlund, E.N.; MacLachlan, N.J.; Wilson, W.C. Whole genome sequencing and phylogenetic analysis of Bluetongue virus serotype 2 strains isolated in the Americas including a novel strain from the western United States. J. Vet. Diagn. Investig 2014, 26, 553–557. [CrossRef]
Maclachlan, N.J.; Wilson, W.C.; Crossley, B.M.; Mayo, C.E.; Jasperson, D.C.; Breitmeyer, R.E.; Whiteford, A.M. Novel serotype of bluetongue virus, western North America. Emerg. Infect. Dis. 2013, 19, 665–666. [CrossRef]
Stevens, G.; McCluskey, B.; King, A.; O’Hearn, E.; Mayr, G. Review of the 2012 Epizootic hemorrhagic disease outbreak in domestic ruminants in the United States. PLoS ONE 2015, 10, e0133359. [CrossRef]
Sun, D.; Cho, Y.I.; Comyn, P.; Yoon, K.J. Use of blood collected onto and dried on filter paper for diagnosing pregnancy in cattle. Vet. J. 2013, 198, 494–497. [CrossRef]
Yoon, K.J.; Cho, Y.I.; Kim, W.I.; Pittman, J.S.; Brinkman, M.; Winton, C. Experimental and field trial of TEGO™ Animal Blood Collection kit for PRRS testing. In Proceedings of the Annual Meeting of American Association of Swine Veterinarians, Omaha, NE, USA, 6–9 March 2010; pp. 211–214.
Fenollar, F.; Raoult, D. Diagnosis of rickettsial diseases using samples dried on blotting paper. Clin. Diagn. Lab Immunol. 1999, 6, 483–488. [CrossRef]
Mejri, S.; Dhaou, S.B.; Jemli, M.; Breard, E.; Sailleau, C.; Sghaier, S.; Zouari, M.; Lorusso, A.; Savini, G.; Zientara, S.; et al. Epizootic haemorrhagic disease virus circulation in Tunisia. Vet. Ital. 2018, 54, 87–90. [CrossRef]
Kramps, J.A.; van Maanen, K.; Mars, M.H.; Popma, J.K.; van Rijn, P.A. Validation of a commercial ELISA for the detection of bluetongue virus (BTV)-specific antibodies in individual milk samples of Dutch dairy cows. Vet. Microbiol. 2008, 130, 80–87. [CrossRef]
Martinelle, L.; Dal Pozzo, F.; Sarradin, P.; De Leeuw, I.; De Clercq, K.; Thys, C.; Ziant, D.; Thiry, E.; Saegerman, C. Two alternative inocula to reproduce bluetongue virus serotype 8 disease in calves. Vaccine 2011, 29, 3600–3609. [CrossRef]
Vandenbussche, F.; Vandemeulebroucke, E.; De Clercq, K. Simultaneous detection of bluetongue virus RNA, internal control GAPDH mRNA, and external control synthetic RNA by multiplex real-time PCR. Methods Mol. Biol. 2010, 630, 97–108. [CrossRef]
Martinelle, L.; Dal Pozzo, F.; Thys, C.; De Leeuw, I.; Van Campe, W.; De Clercq, K.; Thiry, E.; Saegerman, C. Assessment of cross-protection induced by a bluetongue virus (BTV) serotype 8 vaccine towards other BTV serotypes in experimental conditions. Vet. Res. 2018, 49, 63. [CrossRef] [PubMed]
Vandenbussche, F.; De Leeuw, I.; Vandemeulebroucke, E.; De Clercq, K. Emergence of bluetongue serotypes in Europe, part 1: Description and validation of four real-time RT-PCR assays for the serotyping of bluetongue viruses BTV-1, BTV-6, BTV-8 and BTV-11. Transbound. Emerg. Dis. 2009, 56, 346–354. [CrossRef] [PubMed]
Tatusova, T.A.; Madden, T.L. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 1999, 174, 247–250. [CrossRef]
Sergeant, E.S.G. Epitools Epidemiological Calculators. Available online: https://epitools.ausvet.com.au/(accessed on 22 June 2019).
Chaignat, V.; Nitzsche, S.; Scharrer, S.; Feyer, D.; Schwermer, H.; Thur, B. Milk concentration improves Bluetongue antibody detection by use of an indirect ELISA. Vet. Microbiol. 2010, 143, 179–183. [CrossRef] [PubMed]
Martinelle, L.; Chaber, A.L.; Dal Pozzo, F.; Lignereux, L.; Saegerman, C. Dried Blood Spots are Valuable to Perform Bluetongue Virus Diagnostic Tests; University of Liege: Liège, Belgium, 2021; manuscript in preparation.
Zanella, G.; Martinelle, L.; Guyot, H.; Mauroy, A.; De Clercq, K.; Saegerman, C. Clinical pattern characterization of cattle naturally infected by BTV-8. Transbound. Emerg. Dis. 2013, 60, 231–237. [CrossRef]
Katz, J.; Alstad, D.; Gustafson, G.; Evermann, J. Diagnostic analysis of the prolonged bluetongue virus RNA presence found in the blood of naturally infected cattle and experimentally infected sheep. J. Vet. Diagn. Investig. 1994, 6, 139–142. [CrossRef]
Falconi, C.; Lopez-Olvera, J.R.; Gortazar, C. BTV infection in wild ruminants, with emphasis on red deer: A review. Vet. Microbiol. 2011, 151, 209–219. [CrossRef]
De Clercq, K.; De Leeuw, I.; Verheyden, B.; Vandemeulebroucke, E.; Vanbinst, T.; Herr, C.; Meroc, E.; Bertels, G.; Steurbaut, N.; Miry, C.; et al. Transplacental infection and apparently immunotolerance induced by a wild-type bluetongue virus serotype 8 natural infection. Transbound. Emerg. Dis. 2008, 55, 352–359. [CrossRef]
Stallknecht, D.E.; Luttrell, M.P.; Smith, K.E.; Nettles, V.F. Hemorrhagic disease in white-tailed deer in Texas: A case for enzootic stability. J. Wildl. Dis. 1996, 32, 695–700. [CrossRef]
Mayo, C.; McDermott, E.; Kopanke, J.; Stenglein, M.; Lee, J.; Mathiason, C.; Carpenter, M.; Reed, K.; Perkins, T.A. Ecological dynamics impacting bluetongue virus transmission in North America. Front. Vet. Sci. 2020, 7, 186. [CrossRef] [PubMed]
Schirtzinger, E.E.; Jasperson, D.C.; Ostlund, E.N.; Johnson, D.J.; Wilson, W.C. Recent US Bluetongue virus serotype 3 isolates found outside of Florida indicate evidence of reassortment with co-circulating endemic serotypes. J. Gen. Virol. 2018, 99, 157–168. [CrossRef] [PubMed]
Gibbs, P.; McVey, D.S. Report of the Committee on Bluetongue and Related Orbiviruses; United States Animal Health Association (USAHA): Providence, RI, USA, 2015.
Allison, A.B.; Goekjian, V.H.; Potgieter, A.C.; Wilson, W.C.; Johnson, D.J.; Mertens, P.P.; Stallknecht, D.E. Detection of a novel reassortant epizootic hemorrhagic disease virus (EHDV) in the USA containing RNA segments derived from both exotic (EHDV-6) and endemic (EHDV-2) serotypes. J. Gen. Virol. 2010, 91, 430–439. [CrossRef] [PubMed]
Golender, N.; Khinich, Y.; Gorohov, A.; Abramovitz, I.; Bumbarov, V. Epizootic hemorrhagic disease virus serotype 6 outbreak in Israeli cattle in 2015. J. Vet. Diagn. Investig. 2017, 29, 885–888. [CrossRef]
Baldet, T.; Delecolle, J.C.; Cetre-Sossah, C.; Mathieu, B.; Meiswinkel, R.; Gerbier, G. Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of northern France during autumn 2006. Prev. Vet. Med. 2008, 87, 84–97. [CrossRef]
Walton, T.E. The history of bluetongue and a current global overview. Vet. Ital. 2004, 40, 31–38.