(Newcastle disease virus genotypes VIg and VIIb

Archives of Virology https://doi.org/10.1007/s00705-018-3815-9

BRIEF REPORT

Genetic diversity of avian avulavirus 1 (Newcastle disease virus genotypes VIg and VIIb) circulating in wild birds in Kazakhstan Mukhit B. Orynbayev1 · Sasan Fereidouni2 · Abylay R. Sansyzbai1 · Bakhytkul A. Seidakhmetova1 · Vitaliy M. Strochkov1 · Askar M. Nametov3 · Sandugash O. Sadikaliyeva1 · Asel Nurgazieva4 · Kaissar K. Tabynov1 · Nurkuysa M. Rametov1 · Kulyaisan T. Sultankulova1 Received: 19 January 2018 / Accepted: 4 March 2018 © Springer-Verlag GmbH Austria, part of Springer Nature 2018

Abstract In order to improve current understanding of the molecular epidemiology of avian avulavirus 1 (AAvV-1, formerly avian paramyxovirus 1) in wild birds in Kazakhstan, 860 cloacal swab samples were evaluated. Samples were collected from 37 families of wild birds in nine different regions in the years 2011 and 2014. Overall, 54 positive samples (4.2%) were detected from 17 different families of wild birds, and 16 AAvV-1 isolates were characterized. Three of the isolates contained the fusion protein cleavage site motif RRQKR, and 13 contained KRQKR, which is typical for pathogenic strains of AAvV-1. The AAvV-1 isolates were found to belong to the genotypes VIg and VIIb. Newcastle disease (ND) is one of the most important viral diseases of birds and is responsible for enormous economic losses to poultry farming worldwide [2]. The causative agent is an RNA virus belonging to the genus Avulavirus, family Paramyxoviridae [3, 18]. It has been shown that 241 species from 27 orders of the avian family are susceptible to Newcastle disease [15]. Clinical signs of infection vary widely from subtle subclinical signs to a systemic infection that may cause up to 100% mortality in bird populations [4]. Avian avulavirus 1 (AAvV-1) (formerly called avian paramyxovirus 1) strains are divided into two classes representing diverse and constantly developing virus groups. Viruses of class I are characterized as viruses of low virulence and Handling Editor: Bert K. Rima. * Mukhit B. Orynbayev [email protected] 1

Research Institute for Biological Safety Problems, Ministry of Education and Science of Republic of KazakhstanScience Committee, Kordaiskiy Rayon, 080409 Gvardeiskiy, Zhambylskaya Oblast, Kazakhstan

2

Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Vienna, Austria

3

National Agrarian Scientific Education Center, Ministry of Agriculture, Astana, Kazakhstan

4

Kyrgyz Research Institute of Veterinary, Bishkek, Kyrgyz Republic

have been isolated from wild birds worldwide. The viruses of this class contain only one genotype [12]. Viruses of class II are divided to 18 genotypes and several sub-genotypes [11, 12, 16]. Wild birds are considered a natural reservoir for AAvV-1. Strains of various genotypes have been isolated from a wide range of wild bird species [8, 10]. Analysis of genetic diversity of AAvV-1 shows that wild birds are probably the main carriers of virulent strains, and constant transmission of the virus may occur between wild and domestic birds. However, compelling evidence to support this assertion is lacking [16]. Circulation of AAvV-1 strains of different pathogenicity among wild birds is a persistent threat for poultry farming and wild and the health of birds, since outbreaks of AAvV-1 infection among wild birds are not unusual. Wetlands located in Kazakhstan and in West and Central Asia in general represent major wintering and stopover sites during the migration of millions of wild water birds from Siberia and northern Russia, and they have been investigated for viruses such as avian influenza virus during spring or autumn migration [14, 19]. However, little information is available about the circulation of AAvV-1 strains and genotypes in wild birds in this region [6]. The current study provides results of the monitoring investigation and genetic characterization of the AAvV-1 strains circulating in the wild bird populations in the Republic of Kazakhstan. Nine cloacal swab samples were collected from pheasants in the Zhambyl region in 2011 within the framework

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of a surveillance study for avian influenza in wild birds. A further 851 cloacal swab samples were collected in 2014 from wild birds of 37 families (Table 1) in nine regions of Kazakhstan within the framework of a national monitoring program of diseases of wild birds. Samples were collected from apparently healthy wild birds. Some of the samples were collected from cormorant and pelican chicks that were in a non-flying stage.

Mist nets were used to capture the resident and migrating birds in Shakpak ornithological station. Samples were also collected from hunted wild birds during the licensed seasonal hunting period. Cloacal swabs were collected based on standard sampling procedures to reduce the risk of cross-contamination and were stored and transported in liquid nitrogen. The specimens were maintained at − 40 °C after arrival at the laboratory. Virus isolation was carried out

Table 1 Wild birds sampled in different regions of Kazakhstan #

Bird family

Number of positives/total number of samples collected in the each region Almaty

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37

Strigidae Accipitridae Corvidae Phasianidae Caprimulgidae Fringillidae Emberizidae Motacillidae Columbidae Sturnidae Falconidae Turdidae Passeridae Paridae Meropidae Hirundinidae Acrocephalidae Laniidae Scolopacidae Charadriidae Picidae Ibidorhynchidae Aegithalidae Phalacrocoracidae Laridae Pelecanidae Anatidae Gruidae Muscicapidae Rallidae Otis tarda Threskiornithidae Recurvirostridae Ardeidae Upupidae Podicipedidae Stenostiridae Total

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Akmola

0/3

Ak-Tyobe

Atyrau

EKR

0/2

0/3 0/2 0/5 0/1

1/1

0/1

1/48 0/2 0/25 1/12 0/1 0/1 0/3 16/68 0/5 1/7 0/17 0/23 1/28 0/19

0/1

0/3

0/9

0/2

0/3 0/1

0/3 0/45 0/5 0/3 1/4 21/331

0/9

0/20 1/14 0/14

Zhambyl

Total WKR

Pavlodar

NKR

0/3 1/30 0/48 6/9 0/2 0/24 0/15 1/20 10/20 2/36 0/12 0/12 0/15 0/7 1/117 1/17 0/1 0/1 0/18 0/1

0/3

1/1

0/1

1/10

2/2

0/7

1/1

1/8

1/1

1/13

1/1

1/14

1/1

0/15

1/48

2/14

27/413

1/15

0/3 1/30 0/51 6/11 0/2 0/27 0/17 1/25 11/22 2/36 0/12 0/13 0/15 0/7 1/117 1/17 1/49 0/3 0/43 1/13 0/1 0/1 0/3 16/69 1/30 2/21 5/76 0/23 1/28 2/33 0/1 0/3 1/1 0/45 0/5 0/3 1/4 54/860

Avian avulavirus 1 in wild birds in Kazakhstan

in specific-pathogen-free (SPF) embryonated chicken eggs based on standard procedures [24]. RNA extraction was performed using a QIAmp Viral RNA Mini Kit (QIAGEN, USA) according to the manufacturer’s instructions. The samples were analyzed using a TaqMan one-step real-time RT-PCR assay targeting the matrix [23], polymerase [13] and fusion genes [5], using a Rotor-Gene Q cycler (QIAGEN, Germany). Oligonucleotide microarray for rapid diagnosis of avian viral diseases including AIV, NDV (AAvV-1), IBV and IBDV was used as an additional tool to confirm NDV (AAvV-1) identification [28]. The test was performed on an InnoScan 710 DNA microarray scanner (Innopsys, France) using the Cy5 channel. The PCR products of the anticipated size range were purified and cycle sequenced in both directions using the same

primers as for RT-PCR [12]. A Prism Big Dye Terminator v1.1 cycle sequencing kit (Applied Biosystems) was used, and amplicons were analyzed on an automatic sequencer (ABI-3130, Applied Biosystems). Phylogenetic analysis was carried out for 16 complete F genes obtained in this study and selected sequences available in the GenBank database, using the neighbor-joining method with 500 bootstrap replicates as implemented in MEGA v6 software (Fig. 1). In summary, 54 out of 860 cloacal swab samples collected from various regions of Kazakhstan tested positive for AAvV-1 using real-time RT-PCR (specific for the matrix, polymerase and fusion genes) and microarray assays. AAvV-1 was detected in samples from wild birds of 17 families (Table 1). Positive samples were selected for virus isolation in SPF eggs, and, as a result, 16 AAvV-1 isolates were obtained from samples from 10 bird species collected from

Fig. 1 Genetic diversity of the AAvV-1 isolated from wild birds in Kazakhstan. A. Phylogenetic tree of F-gene nucleotide sequences using the neighbor-joining method, with 500 bootstrap replicates. B. Geographic distribution of AAvV-1 among wild birds in Kazakhstan

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five regions of Kazakhstan. Characteristics of the isolated viruses are shown in Table 2. Three viruses (numbers 9-11 in Table 2) were predicted to contain the specific motif 112RRQKRF117 at the cleavage site, and 13 other viruses were predicted to contain the motif of 112KRQKRF117. Analysis of F-gene nucleotide sequences of the isolates indicated that the same three viruses (isolated from wild birds in the Almaty region in 2014) belonged to the VIIb genotype, and another 13 viruses (isolated from wild birds in the Almaty, Zhambyl, Pavlodar, West Kazakhstan and East Kazakhstan regions in 2011 and 2014) belonged to the VIg genotype (Fig. 1). Monitoring of wild birds for infectious agents such as avian paramyxoviruses (avulaviruses) in their natural habitats and in areas that pose a risk for transmission between domestic poultry and wild birds will increase the knowledge of epidemiology, ecology and genetic relationships of such viruses. This knowledge may provide information on currently circulating viruses and facilitate risk assessments concerning poultry and wild bird populations. Kazakhstan’s location places it at the intersection of the main migration

routes of wild birds in the Eurasian continent. Therefore, studying the epidemiology, ecology and molecular genetics of paramyxoviruses (and in particular AAvV-1) circulating in wild birds has great significance. AAvV-1 have been isolated and investigated in wild birds in many countries, including China, the USA, Canada, Russia and several African countries [17, 20]. However, little information is available about the prevalence and molecular epidemiology of AAvV-1 in wild birds in Kazakhstan, although outbreaks of ND in domestic birds have been reported frequently [7, 25]. In this study, 860 cloacal swabs were collected, and 16 AAvV-1 isolates were collected from four water bird species (Eurasian coot, cormorant, pelican, and common merganser) and five terrestrial species (pigeon, garden warbler, common long-legged buzzard, common myna, and pheasant) and studied. The amino acid sequence at the cleavage site of the fusion protein plays a decisive role in the pathogenic properties of the virus and directly affects the efficiency of virus penetration into target cells [22]. Sequencing and genetic analysis of the fusion protein genes of the identified viruses showed

Table 2 Characteristics of AAvV-1 isolated from wild birds in Kazakhstan #

Name of the isolated ND virus

Sampling place

Sampling date Bird species

F gene cleavage site

1

Phasianus colchicus/KZ/ Zhambyl/5/2011 Columbalivia /KZ/Zhambyl/27/2014 (KT965732) Columbalivia /KZ/Zhambyl/30/2014

Zhambyl region, Tasotkel Lake

Nov. 2011

Pheasant

112

Zhambyl region, Shakpak ornithological station Zhambyl region, Shakpak ornithological station Zhambyl, Shakpak ornithological station Zhambyl, Shakpak ornithological station Zhambyl region, Shakpak ornithological station Zhambyl, Shakpak ornithological station Zhambyl, Shakpak ornithological station Almaty region, Teskenterek River

Oct. 2014

Pigeon

112

Oct. 2014

Pigeon

112

Oct. 2014

Pigeon

112

Oct. 2014

Long-legged buzzard

112

Oct. 2014

Common myna

112

Dec. 2014

Common myna

112

Dec. 2014

Pigeon

112

May. 2014

Garden warbler

112

Almaty region, Alakol Lake

Jul. 2014

Cormorant

112

Almaty region, Alakol Lake Almaty region, Alakol Lake

Jul. 2014 Jul. 2014

Pelican Cormorant

112

East-Kazakhstan region, Borodulikha district, Tuzdykol Lake East-Kazakhstan region, Borodulikha village Pavlodar region Ak-Tyobe region, Martuk district, Bulak Lake

Oct. 2014

Northern pintail

112

Oct. 2014

Pigeon

112

Oct. 2014 Apr. 2014

Common merganser Eurasian coot

112

2 3 4

7

Columbalivia /KZ/Zhambyl/32/2014 (KT965728) Buteo rufinius/KZ/Zhambyl/41/2014 (KT965731) Acridotheres/KZ/Zhambyl/17/2014 (KT965729) Acridotheres /KZ/Zhambyl/6/2014

8

Columbalivia /KZ/Zhambyl/26/2014

9

Acrocephalus dumetorum/KZ/ Almaty/59/2014 (MG976930) Phalacrocorax carbo/KZ/ Almaty/167/2014 (MG976931) Pelicanus crispus/KZ/Almaty/94/2014 Phalacrocorax carbo/KZ/ Almaty/186/2014 Anas acuta/KZ/EKO/1/2014 (KT965730) Columbalivia/KZ/EKO/15/2014 (KT965727) Mergus/KZ/Pavlodar/8/2014 Fulica atra/KZ/WKO/4/2014

5 6

10 11 12 13 14 15 16

13

KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117 RRQKRF117 RRQKRF117 RRQKRF117 KRQKRF117

112

KRQKRF117 KRQKRF117 KRQKRF117 KRQKRF117

112

Avian avulavirus 1 in wild birds in Kazakhstan

that they all had a cleavage site characteristic of pathogenic AAvV-1. In addition, the presence of a phenylalanine (F) residue at position 117 is a potential indicator of higher pathogenicity compared to low-pathogenic (lentogenic) isolates that contain leucine (L) instead of F. An in-depth study of the genetic relationships between viruses isolated from different bird species in different geographical areas provides important information about the molecular epidemiology of AAvV-1. The genotypes to which the strains isolated from wild birds in Kazakhstan belong are of special interest. Phylogenetic analysis of the isolated viruses indicated that 13 viruses belonged to the VIg genotype and three belonged to the VIIb genotype. Viruses of the VIg genotype are closely related to strains from Kazakhstan (JN806236), Russia (JF827026), Nigeria (JQ039385) and Italy (JN638236). Isolated strains of the VIIb genotype were genetically most closely related to AAvV-1 strains of Chinese origin, such as APMV-1/China/ZJ-17-08-Ch/2008 (GQ245819) and to the viruses that have been isolated from dead domestic birds in Kazakhstan: APMV-1/chicken/ KZ/Almaty/07/2013 (KT719399), APMV-1/chicken/KZ/ Korday/05/2013 (KT719398), and APMV-1/chicken/KZ/ SKO/12/2012 (KT719397). Molecular genetic studies in many countries have shown heterogeneity of circulating AAvV-1. Viruses of various phylogenetic lineages from different global geographical regions circulate simultaneously and undergo evolutionary changes, and this fact significantly impedes disease diagnosis and control [9]. Viruses of genotype VI have been isolated from different continents and from various bird species [6, 20, 26, 27]. In the current study, 13 AAvV-1 of the VIg genotype were isolated from pigeons, mynas, a long-legged buzzard, a pheasant, a pintail, a coot, a merganser and cormorants from different geographical areas in Kazakhstan (Table 2). The geo-phylogenetic data (Fig. 1) indicated that some AAvV-1 genotypes, such as VIIb, may circulate in distant geographical regions of Kazakhstan. AAvV-1 has been isolated from pigeons on different continents [21, 26, 27]. In Kazakhstan, AAvV-1 of genotype VI was only isolated from pigeons [6], and these viruses have never been isolated or identified in other species of wild birds in the country. Pheasants are susceptible to nearly all strains of AAvV-1 circulating in domestic and wild birds. Nevertheless, the clinical signs and mortality rates of infected birds differ significantly [1]. In the current study, infected pheasants were identified on the shores of Tasotkol Lake (Zhambyl region). These birds do not migrate and are permanent residents in this area; therefore, most probably they acquired infection via migrating waterfowl. Isolation of the virus from apparently healthy wild terrestrial and water birds indicates that these birds may act as asymptomatic carriers of the AAvV-1 and spread it to the various geographical areas during seasonal migrations.

The viruses of genotype VII are particularly important, as they cause most epizootic outbreaks in domestic birds in Asia, Europe and Africa [7, 17, 21, 25]. In addition, viruses of this genotype have been isolated from wild birds [26]. It has been postulated that availability of short migration routes between northern European countries and Ukraine may have resulted in local dissemination of AAvV-1 of genotype VIIa to Ukraine, and additionally, massive migration from Southeast Asia through Russia, Kazakhstan and Kyrgyzstan to the Caspian Sea and further wetlands may have facilitated spread of viruses of genotypes VIIb and VIId [17]. The results of the current study may strengthen this assumption, as three AAvV-1 isolates of genotype VIIb were obtained from a cormorant, a pelican and a garden warbler in the Almaty region, and analysis of the genetic data showed that these viruses are 100% identical to AAvV-1 isolated in 2012-2013 from unvaccinated poultry in private households of Almaty, Zhambyl and the northeastern regions of Kazakhstan [25]. These results suggest that wild birds act as reservoirs of AAvV-1 of the VIIb genotype, and outbreaks of disease among poultry in various regions of Kazakhstan are possibly associated with migrations of wild birds. Alternatively, the wild birds may catch the virus from infected/diseased domestic poultry. In summary, the results of our study provide important information about the epidemiology of AAvV-1 in wild birds in Kazakhstan. Monitoring of wild birds for avian paramyxoviruses in their natural habitats will increase our knowledge of the epidemiology, ecology and genetic relationships of these viruses and help us to evaluate the risk of transmission between domestic poultry and wild birds. This knowledge will facilitate risk assessments concerning poultry and wild bird populations and provide information on currently circulating viruses. Therefore, we strongly recommend continued surveillance of wild bird populations in Central Asia. Acknowledgements The authors are grateful to the specialists of the Zoology Institute, MES RK, for their assistance in identification of the bird species in the process of their capture; and to PK Walzer for editorial advice during the preparation of the manuscript. Funding This study was funded by the Committee of Science of the Ministry of Education and Science of the Republic of Kazakhstan (Grant number 0920/GF 4).

Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest. Ethical approval All applicable international, national, and institutional guidelines for the care and use of animals were followed. All ethics, field and laboratory studies were reviewed and approved by the appropriate committees of the Research Institute for Biological Safety Problems (RIBSP), Ministry of Education & Science in Gvardeiskiy,

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Zhambylskaya oblast, Republic of Kazakhstan. The committee’s reference number was No. 19-17.

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