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Experimental Infection of Highly Pathogenic Avian Influenza Virus H5N1 in Black-Headed Gulls (Chroicocephalus Ridibundus)

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Experimental Infection of Highly Pathogenic Avian Influenza Virus H5N1 in Black-Headed Gulls (Chroicocephalus Ridibundus) Ramis et al. Veterinary Research 2014, 45:84 http://www.veterinaryresearch.org/content/45/1/84 VETERINARY RESEARCH RESEARCH Open Access Experimental infection of highly pathogenic avian influenza virus H5N1 in black-headed gulls (Chroicocephalus ridibundus) Antonio Ramis1*, Geert van Amerongen2, Marco van de Bildt2, Loneke Leijten2, Raphael Vanderstichel3, Albert Osterhaus2 and Thijs Kuiken2 Abstract Historically, highly pathogenic avian influenza viruses (HPAIV) rarely resulted in infection or clinical disease in wild birds. However, since 2002, disease and mortality from natural HPAIV H5N1 infection have been observed in wild birds including gulls. We performed an experimental HPAIV H5N1 infection of black-headed gulls (Chroicocephalus ridibundus) to determine their susceptibility to infection and disease from this virus, pattern of viral shedding, clinical signs, pathological changes and viral tissue distribution. We inoculated sixteen black-headed gulls with 1 × 104 median tissue culture infectious dose HPAIV H5N1 (A/turkey/Turkey/1/2005) intratracheally and intraesophageally. Birds were monitored daily until 12 days post inoculation (dpi). Oropharyngeal and cloacal swabs were collected daily to detect viral shedding. Necropsies from birds were performed at 2, 4, 5, 6, 7, and 12 dpi. Sampling from selected tissues was done for histopathology, immunohistochemical detection of viral antigen, PCR, and viral isolation. Our study shows that all inoculated birds were productively infected, developed systemic disease, and had a high morbidity and mortality rate. Virus was detected mainly in the respiratory tract on the first days after inoculation, and then concentrated more in pancreas and central nervous system from 4 dpi onwards. Birds shed infectious virus until 7 dpi from the pharynx and 6 dpi from the cloaca. We conclude that black-headed gulls are highly susceptible to disease with a high mortality rate and are thus more likely to act as sentinel species for the presence of the virus than as long-distance carriers of the virus to new geographical areas. Introduction Since 2002, disease and mortality from natural HPAIV Historically, highly pathogenic avian influenza viruses H5N1 infection have been described for several gull spe- (HPAIV) were rarely found in wild birds, and, if they cies: black-headed gull (Chroicocephalus ridibundus) [2], were, they typically did not cause clinical disease [1]. great black-headed gull (Larus ichthyaetus) and brown- However, in late 2002, HPAIV H5N1 outbreaks were de- headed gull (Larus brunnicephalus) [4]. Also, experimen- scribed in Hong Kong parks causing disease and death tal infections have been performed in laughing gulls in wild local and migratory birds; concurrently with (Larus atricilla) [5] and herring gulls (Larus argentatus) these outbreaks, HPAIV H5N1 were isolated from dead [6] showing that these species were highly susceptible chickens and human beings [2]. It was shown through (100%) to different HPAIV H5N1 isolates (A/Whooper antigenic analysis that these new isolates of HPAIV Swan/Mongolia/244/05 and A/Duck Meat/Anyang/01), H5N1 presented a reactivity pattern different from that presenting a severe and short (4 to 10 dpi) clinical of HPAIV H5N1 isolated in 1997 and 2001 and caused course, consisting mainly of neurologic signs with a high systemic infection in experimentally infected domestic mortality rate (up to 100% in some cases). The main tar- ducks, with high virus titres and lesions in multiple get organs for viral replication were central nervous sys- organs, particularly in the brain [3]. tem (CNS), pancreas, and adrenal gland, and the duration of the viral shedding after inoculation was in a * Correspondence: [email protected] range of 1 to 10 dpi depending on the isolate, the gull 1CReSA and Departament de Sanitat i Anatomia Animals, Universitat Autonoma de Barcelona, Barcelona, Spain species, and inoculation route. In these experiments, Full list of author information is available at the end of the article © 2014 Ramis et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ramis et al. Veterinary Research 2014, 45:84 Page 2 of 10 http://www.veterinaryresearch.org/content/45/1/84 virus dynamics and in-depth pathogenesis were not in- units for 15 days to acclimatize them to the new envir- vestigated. Lastly, in an experimental infection in com- onment. Two days before the experimental inoculation, mon gulls (Larus canus) with a HPAIV H5N1 isolate (A/ they were tested for antibodies against influenza viruses Gull/Chany/P/06) isolated from healthy birds of this spe- by use of a commercially available nucleoprotein-based cies, the virus was shown to replicate in respiratory and ELISA test (European Veterinary Laboratory, Woerden, digestive tracts and to be excreted from pharynx and The Netherlands) to assure they were not previously in- 4 cloaca for 2 weeks after the infection, with no clinical fected. Sixteen birds were inoculated with 1 × 10 TCID50 signs in infected birds [7]. HPAIV H5N1, 1.5 mL intratracheally and 1.5 mL intraoe- The black-headed gull is the most ubiquitous gull in sophageally, which was the same virus, inoculum dose, Europe and Asia, is a peridomestic species that often oc- and inoculation route as in a previous study [10]. We used curs in urban and agricultural environments [8] and is this dose to increase the chance of inducing subclinical in- known to be susceptible to HPAIV H5N1 infection [2]. fection and to simulate field circumstances. In addition, 6 Also, black-headed gulls are listed by the European Food birds that served as negative controls were sham- Safety Authority [9] as having higher probability to be inoculated in the same manner with PBS-diluted sterile al- exposed to Asian linage HPAIV H5N1 during migration lantoic fluid. Daily, a qualified veterinarian scored clinical outside the European Union, because of their gregarious signs of disease in all birds according to a standardized behaviour and their tendency to use both wild areas and list. Also daily, the body weight of each bird was mea- built-up areas. However, it is known neither how long sured, and cloacal and pharyngeal swabs were collected in black-headed gulls can shed HPAIV H5N1 nor how sus- 1 mL transport medium. Birds were euthanatized by ex- ceptible they are to disease from HPAIV H5N1 infection. sanguination under isofluorane anesthesia. After euthan- These are important considerations to decide whether asia, blood samples were taken and necropsies and tissue black-headed gulls are more likely to act as sentinels for sampling were performed. The original plan was to eu- the presence of the virus in the environment, or to act thanatize four HPAIV H5N1-inoculated birds on each of as long-distance vectors of the virus to other geograph- days 2, 4, 6 and 12 post inoculation, two sham-inoculated ical areas [10]. Therefore, we performed an experimental birds at 3 days post inoculation (dpi) and four sham- infection of black-headed gulls using HPAIV A/turkey/ inoculated birds at 12 dpi. Because some H5N1- Turkey/1/2005 (H5N1) to determine the susceptibility of inoculated birds died spontaneously before the planned this host species to infection and disease from this virus; day of euthanasia, we were unable to completely follow the pattern of pharyngeal and cloacal viral shedding; the the original plan, and the timing of necropsies and sam- clinical signs and pathological changes; and lastly the pling for H5N1-inoculated birds was as follows: four birds virus distribution in different tissues. We chose this virus at 2 dpi; five birds at 4 dpi; two birds at 5 dpi; two birds at isolate to allow comparison of the results between black- 6 dpi; one bird at 7 dpi; and two birds at day 12 dpi headed gulls and 6 different wild species of Anseriformes (Table 1). [10], which jointly with Charadriiformes—to which the black-headed gull belongs—have traditionally been con- Pathologic and immunohistologic examination sidered the natural reservoir for avian influenza viruses; Necropsies and tissue sampling were performed according and also because this isolate had spread quickly from to a standard protocol. After fixation in 10% neutral- Asia to Europe in 2005–2006 [11]. buffered formalin and embedding in paraffin, 3-μm-thick tissue sections were made and stained by two methods: Material and methods hematoxylin and eosin staining for histologic evaluation Virus preparation and an immunohistologic method that used a monoclonal A virus stock of HPAIV A/turkey/Turkey 1/2005 (H5N1) antibody against nucleoprotein for influenza A virus as a was prepared by propagation in Madin-Darby canine kid- primary antibody for detection of influenza viral antigen ney (MDCK) cells and titrated according to standard [12]. The positive control was a lung of a HPAIV (H5N1) methods [12]. The fluid had a titre of 1 × 108.1 median tis- infected ferret; negative controls were substitution of the sue culture infectious dose (TCID50)/mL and was diluted primary antibody by an irrelevant monoclonal antibody of with phosphate-buffered saline (PBS) to obtain a final titre the same isotype, and testing of tissues from sham- 4 of 10 TCID50/mL. All the experiments with HPAIV H5N1 inoculated black-headed gulls. The following tissues were were performed under Biosafety level 3 + conditions. examined: brain (cerebrum, cerebellum and brain stem), trachea, bronchus, lung, air sac, oesophagus, proventricu- Experimental design lus, duodenum, pancreas, jejunum, ileum, cecum, colon, We used 22 black-headed gulls (2–3 weeks old) obtained liver, gallbladder, cloaca, cloacal bursa, spleen, thymus, from a breeding colony site at Blauwestad, The kidney (cranial and caudal lobes), gonad, adrenal gland, Netherlands.
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