Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Applied and Environmental Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Evolutionary and Genomic Microbiology

High Genetic Diversity of Newcastle Disease Virus in Wild and Domestic Birds in Northeastern China from 2013 to 2015 Reveals Potential Epidemic Trends

Pingze Zhang, Guangyao Xie, Xinxin Liu, Lili Ai, Yanyu Chen, Xin Meng, Yuhai Bi, Jianjun Chen, Yuzhang Sun, Tobias Stoeger, Zhuang Ding, Renfu Yin
D. W. Schaffner, Editor
Pingze Zhang
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Guangyao Xie
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Xinxin Liu
bCollege of Food Science and Engineering, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Lili Ai
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yanyu Chen
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Xin Meng
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yuhai Bi
cCAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jianjun Chen
dCAS Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Hubei, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yuzhang Sun
eChina Animal Health and Epidemiology Center, Qingdao, Shandong, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tobias Stoeger
fComprehensive Pneumology Center, Institute of Lung Biology and Disease, Helmholtz Zentrum Muenchen, Neuherberg/Munich, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Zhuang Ding
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Renfu Yin
aDepartment of Veterinary Preventive Medicine, College of Veterinary Medicine, Jilin University, Changchun, Jilin, China
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
D. W. Schaffner
Rutgers, The State University of New Jersey
Roles: Editor
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AEM.03402-15
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Newcastle disease (ND), caused by the virulent Newcastle disease virus (NDV), is one of the most important viral diseases of birds globally, but little is currently known regarding enzootic trends of NDV in northeastern China, especially for class I viruses. Thus, we performed a surveillance study for NDV in northeastern China from 2013 to 2015. A total 755 samples from wild and domestic birds in wetlands and live bird markets (LBMs) were collected, and 10 isolates of NDV were identified. Genetic and phylogenetic analyses showed that five isolates from LBMs belong to class I subgenotype 1b, two (one from wild birds and one from LBMs) belong to the vaccine-like class II genotype II, and three (all from wild birds) belong to class II subgenotype Ib. Interestingly, the five class I isolates had epidemiological connections with viruses from southern, eastern, and southeastern China. Our findings, together with recent prevalence trends of class I and virulent class II NDV in China, suggest possible virus transmission between wild and domestic birds and the potential for an NDV epidemic in the future.

INTRODUCTION

Newcastle disease virus (NDV) is synonymous with avian paramyxovirus type 1 and is a member of the genus Avulavirus within the family Paramyxoviridae (1). The virulent NDVs are the causative agents of Newcastle disease (ND), which is one of the most devastating diseases to the poultry industry worldwide (1). NDV is an enveloped virus containing a nonsegmented, single-stranded, negative-sense RNA genome 15.2 kb in size. The genome contains six genes, which encode the nucleocapsid protein (N), phosphoprotein (P), matrix protein (M), fusion protein (F), hemagglutinin-neuraminidase protein (HN), RNA-dependent RNA polymerase (L), and two additional nonstructural proteins (V and W, produced by a frameshift within the coding region of P) (1).

NDV is considered to be enzootic in both domestic and wild bird species (1). Based on the genomic length and phylogenetic analysis of the F gene, NDVs have been historically classified into two major groups, class I and class II, within a single serotype (2). Class I NDV is distributed globally, usually thought to be avirulent, and frequently isolated from wild birds and live bird markets (LBMs) (3). Class II NDV is widely distributed in multiple bird species. Some class II strains are avirulent or are vaccine viruses, but virulent strains of NDV also mainly group into class II and infections can cause significant economic losses to the poultry industry (2). Class I viruses were previously classified into nine genotypes (1 to 9), based on phylogenetic analysis using parts of the F gene (3, 4), but are now classified into a single phylogenetic group (genotype 1) based on the new classification criteria using the complete F gene sequence (5). Due to their high genetic diversity, class II viruses are classified into 18 genotypes (I to XVIII) (5, 6).

The scale and magnitude of ND outbreaks in China have been decreasing yearly since 2005 (Fig. 1). Interestingly, an increasing number of class I NDVs have been isolated from domestic poultry in southern, eastern, and southeastern China, as well as worldwide, in recent years (4, 7–10). However, no class I NDV was isolated in China before 2002, since they may escape detection by many conventional assays (2, 4). Furthermore, surveillance studies have demonstrated that the ecology of avirulent NDV in wild birds appears to be similar to that of low-pathogenicity avian influenza virus in that both viruses seem to enhance their pathogenicity in birds by accumulated mutations at the fusion protein cleavage site (3, 11–14).

FIG 1
  • Open in new tab
  • Download powerpoint
FIG 1

ND outbreak events in China between 2005 and 2015. The asterisk indicates data cutoff on June 2015. All data were collected from the OIE official website (http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/statusdetail).

In this study, NDVs from wild birds and domestic poultries in LBMs were sequenced and analyzed in order to understand the current epidemiology and gene evolution of NDV in northeastern China. We then analyzed the epidemic trends of class I NDV in China and elucidated the potential ecological relationships between class I and class II NDVs, and the results are presented here.

MATERIALS AND METHODS

Sample collection, virus isolations, and identification.During the surveillance of NDV from April 2013 to June 2015, a total of 755 tracheal or cloacal swab samples were collected from clinically healthy birds in 16 LBMs and three wetlands in Jilin Province of northeastern China. Of these, 340 were from wild birds, and 415 were from domestic poultries. Details of collection for the NDV isolates are given in Fig. 2 and Table 1.

FIG 2
  • Open in new tab
  • Download powerpoint
FIG 2

Sample collection sites in Jilin Province. Sampled cities or areas are indicated by color. The number of samples and positive rates of NDV are annotated.

View this table:
  • View inline
  • View popup
TABLE 1

Samples and isolates obtained from birds in different ecological groups in Jilin Province from 2013 to 2015a

All samples were inoculated into the allantoic cavities of 9- to 11-day-old specific-pathogen-free (SPF) chicken embryos (Beijing Merial Vital Laboratory Animal Technology Co., Ltd., Beijing, China) and incubated 96 h at 37°C. Allantoic fluids from inoculated eggs were harvested either when the embryos were killed or after the two passages; the presence of NDV was confirmed by hemagglutination, as well as hemagglutination inhibition (HI) assay, using La Sota-specific polyclonal sera (Harbin Weike Biotechnology Development Company, Harbin, China) according to the standardized OIE protocols for NDV (15).

Nucleic acid extraction, PCR, and sequencing.For genetic characterization of NDV, total RNA was extracted from infectious allantoic fluid using TriPure RNA isolation reagent (Hoffmann-La Roche, Ltd., Basel, Switzerland) according to the manufacturer's instructions. The extracted RNA was used for reverse transcription with random hexamer primers and Moloney murine leukemia virus reverse transcriptase (Promega Corporation, Madison, WI) according to the manufacturer's instructions.

The amplification for partial F genes of class I and II strains are performed as described in previous studies (16, 17). Conditions for PCR of complete F genes was as follows: 95°C for 3 min, followed by 35 cycles at 95°C for 1 min, 51°C for 45 s, and 72°C for 2 min 30 s, with a final extension step at 72°C for 10 min. The primer pair sequences used are listed in Table 2. Sequencing of PCR amplicons was conducted by Majorbio (Shanghai, China).

View this table:
  • View inline
  • View popup
TABLE 2

Primers used in this study

Phylogenetic analysis.In this study, the sequences of class I NDV reference strains of 1a, 1b, and 1c subgenotypes were obtained from GenBank (http://www.ncbi.nlm.nih.gov/GenBank). The accession numbers of the reference NDVs are shown in the phylogenetic trees. Alignment and comparison of the nucleotide and amino acid sequences were performed using the MegAlign program in the Lasergene package (DNASTAR, Inc., Madison, WI). A maximum-likelihood tree was generated using MEGA 6.06 (18).

Pathogenicity tests.The intracerebral pathogenicity index (ICPI) in 1-day-old SPF chickens and mean time to death (MDT) in 9- to 11-day-old SPF embryonated chicken eggs (Beijing Merial Vital Laboratory Animal Technology Co., Ltd., Beijing, China) were determined according to standard OIE procedures (15).

RESULTS AND DISCUSSION

A total of 755 samples were obtained from 16 LBMs and three wetlands from April 2013 to June 2015. Ten NDVs (six from LBMs and four from wild birds) were isolated; five isolates from LBMs were found to cluster with class I subgenotype 1b, two isolates (one from wild bird and one from LBMs) grouped with the vaccine-like class II genotype II, and three (all from wild birds) belonged to class II subgenotype Ib, based on complete F gene sequences (Fig. 3). No virulent NDV strain was isolated. Isolation rates for class I and II NDV were 0.66% (5/755), indicating that both viruses were equally prevalent in the sampled bird population.

FIG 3
  • Open in new tab
  • Download powerpoint
FIG 3

Phylogenetic analysis of complete F gene sequences (1,662 nucleotides). Class I and II sequences are indicated as gray and white circles, respectively. Only bootstrap values of ≥50% are shown. The evolutionary history was inferred by using the maximum-likelihood method based on the general-time-reversible model. The tree with the highest log likelihood (−11262.9423) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained by applying the neighbor-joining method to a matrix of pairwise distances estimated using the maximum-composite-likelihood approach. A discrete gamma distribution was used to model evolutionary rate differences among sites (four categories [+G, parameter = 0.6973]). The rate variation model allowed for some sites to be evolutionarily invariable ([+I], 0.0000% sites). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 58 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 1,662 positions in the final data set. Evolutionary analyses were conducted using MEGA 6.06.

All five class II isolates showed the typical lentogenic sequence motifs 112GRQGR*L117 and 112GKQGR*L117 (the asterisk indicates the cleavage site of the F0 precursor protein into its F1 and F2 subunits) (Table 3). The genotype II strain Swan goose/China/Jilin/CC01/2015, which was isolated from a swan goose in the wetlands of Changchun, Jilin Province, in 2015, has a high similarity of complete F gene sequence compared to the duck-origin NDV strain Duck/China/Jilin/SY01/2014 (nucleotide sequence homologies of 100%), which was isolated from LBMs in Songyuan, Jilin Province, in 2014. Both strains share a 99.9% nucleotide similarity in complete F gene sequence to two commonly used live vaccine strains in China, La Sota and clone 30, suggesting that the swan goose and duck strains may be reisolation of a vaccine strain. The remaining three class II NDVs (Swan goose/China/Jilin/CC02/2013, Hooded crane/China/Jilin/BC01/2015, and Hooded crane/China/Jilin/BC02/2015), isolated from wild birds in Baicheng and Changchun of Jilin Province, were clustered into subgenotype Ib, which phylogenetically closed to both wild waterfowl isolates in the Far East (Russia, South Korea, and Japan) and recent isolates from domestic ducks in Asia (Eastern China, Japan, and South Korea) (8, 9, 19–21). Highly similar genotype II NDVs isolated from distinct species in different cities of Jilin Province suggested that the virus may be transmitted between wild birds and domestic poultries in the region and that the NDV isolates from wild birds detected in this study will likely be detected from domestic birds in the future.

View this table:
  • View inline
  • View popup
TABLE 3

Detailed information of NDVs isolated from northeastern China from 2013 to 2015

The complete F gene of four class I NDVs (Chicken/China/Jilin/CC02/2015, Chicken/China/Jilin/CC03/2014, Duck/China/Jilin/CC04/2015, and Chicken/China/Jilin/CC05/2015) isolated from LBMs shared high genetic identities (nucleotide sequence homologies of 99.7 to 100%) and formed a cluster within subgenotype 1b, suggesting that these isolates had a similar ancestor (Fig. 3). The remaining F gene sequence characterized in this study (Chicken/China/Jilin/SY02/2015) was also nested within subgenotype 1b. Chicken/China/Jilin/SY02/2015 had a typical cleavage site of avirulent class I subgenotype 1b strains, 112ERQER*L117, while Chicken/China/Jilin/CC02/2015, Chicken/China/Jilin/CC03/2014, Duck/China/Jilin/CC04/2015, and Chicken/China/Jilin/CC05/2015 displayed a motif of 112ARQER*L117 due to a nonsynonymous adenine-to-cytosine substitution at nucleotide position 335. All class I strains belonged to the subgenotype 1b cluster found mainly in domestic ducks and chickens in eastern, southern, and southeastern China (7, 8). Interestingly, similar subgenotype 1b strains were not detected in poultries in northeastern China, even during more intensive sampling periods during 2013 to 2014, suggesting these strains may have been introduced into northeast China from eastern, southern, or southeastern China via the poultry trade. To our knowledge, wild birds are the natural reservoirs of NDV (1). Hence, NDV transmitted between migratory birds and domestic poultries also cannot be excluded (22), even though class I NDV was not isolated in Japan and South Korea after 2006 (20). These countries, including China, are all in the East Asian-Australasian flyway, which provides the opportunity for NDV transmission from wild birds to domestic waterfowl via the stopover wetland sites and vice versa (20, 23).

Class I NDV was first isolated in Fujian and Zhejiang Province in 2002 (9) and since then has been spread into most regions of China, including the south, east, and southeast regions, as well as Hong Kong (Fig. 4) (4, 7–9). Class I NDVs are always considered avirulent for chickens; however, a waterfowl-source avirulent virus, goose/Alaska415/91, became virulent after serial passaging in SPF chicken eggs (24, 25). Therefore, class I NDV has the potential risk to virulent by the viral amino acid substitutions and may need to be monitored in the future (24, 25). In addition, previous study indicated that vaccination with avirulent class II NDV vaccine strains, such as La Sota and V4, may fail to prevent virus shedding of ducks infected with class I virus due to considerable differences in their antigenicity (8). Thus, a killed vaccine based on class I NDV may be necessary to protect the domestic poultry industry from potentially virulent strains of class I NDV.

FIG 4
  • Open in new tab
  • Download powerpoint
FIG 4

Isolation sites and years (A) and percentages (B) of class I NDV clusters in China. Sampled provinces in this study are indicated by a star in panel A. The asterisk in panel B indicates the data cutoff on 20 November 2015. All data were obtained from GenBank (http://www.ncbi.nlm.nih.gov/GenBank/).

Based on hemagglutination inhibition (HI) and virus neutralization (VN) tests, class I NDV showed a broader cross-antigenicity to other genotype NDV strains (8, 26) and displayed higher HI and VN titers against both class I and class II virulent NDV strains than the current class II vaccine strain La Sota (26). Therefore, to some extent, the wide distribution of class I NDV may protect infected poultry against disease caused by virulent class II NDVs and may be one of the reasons for the decreased incidence of ND outbreaks in China from 2005 to 2015.

NDV recombination has also been reported in some reports during recent years (27–32), though even these events are quite controversial (30, 33). A high rate of NDV coinfection will increase the chance for recombination; therefore, the growing prevalence of class I NDV in wild waterfowl and domestic poultries may recombine with other class I and II circulating viruses to generate new strains with unpredictable phenotypes. More research is needed to elucidate the frequency and impact of NDV recombination among wild and domestic birds.

In conclusion, both class I and II NDVs were prevalent in northeastern China from 2013 to 2015. Some class II viruses of wild bird origin were closely related to the NDV from domestic poultry, suggesting interspecies transmission and the potential for virus recombination into more virulent strains, necessitating the demand for constant surveillance.

ACKNOWLEDGMENTS

This study was partly supported by two grants from National Science Foundation of China (31402195 to R.Y. and 31472195 to Z.D.), two grants from Jilin Provincial Science Technology Department (20140520171JH and 20160414029GH to R.Y.) and one grant from Chinese Special Fund for Agri-scientific Research in the public interest (201303033 to Z.D.), three grants from Jilin University (4305050102TS and 450060501486 to R.Y. and 4305050102S4 to X.L.). None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.

FOOTNOTES

    • Received 19 October 2015.
    • Accepted 16 December 2015.
    • Accepted manuscript posted online 28 December 2015.
  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.

REFERENCES

  1. 1.↵
    1. Swayne DE
    . 2013. Diseases of poultry, 13th ed. John Wiley & Sons, Ames, IA.
  2. 2.↵
    1. Czeglédi A,
    2. Ujvári D,
    3. Somogyi E,
    4. Wehmann E,
    5. Werner O,
    6. Lomniczi B
    . 2006. Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications. Virus Res 120:36–48. doi:10.1016/j.virusres.2005.11.009.
    OpenUrlCrossRefPubMedWeb of Science
  3. 3.↵
    1. Miller PJ,
    2. Decanini EL,
    3. Afonso CL
    . 2010. Newcastle disease: evolution of genotypes and the related diagnostic challenges. Infect Genet Evol 10:26–35. doi:10.1016/j.meegid.2009.09.012.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    1. Kim LM,
    2. King DJ,
    3. Suarez DL,
    4. Wong CW,
    5. Afonso CL
    . 2007. Characterization of class I Newcastle disease virus isolates from Hong Kong live bird markets and detection using real-time reverse transcription-PCR. J Clin Microbiol 45:1310–1314. doi:10.1128/JCM.02594-06.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Diel DG,
    2. da Silva LH,
    3. Liu H,
    4. Wang Z,
    5. Miller PJ,
    6. Afonso CL
    . 2012. Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12:1770–1779. doi:10.1016/j.meegid.2012.07.012.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Snoeck CJ,
    2. Owoade AA,
    3. Couacy-Hymann E,
    4. Alkali BR,
    5. Okwen MP,
    6. Adeyanju AT,
    7. Komoyo GF,
    8. Nakoune E,
    9. Le Faou A,
    10. Muller CP
    . 2013. High genetic diversity of Newcastle disease virus in poultry in West and Central Africa: cocirculation of genotype XIV and newly defined genotypes XVII and XVIII. J Clin Microbiol 51:2250–2260. doi:10.1128/JCM.00684-13.
    OpenUrlAbstract/FREE Full Text
  7. 7.↵
    1. Zhu J,
    2. Xu H,
    3. Liu J,
    4. Zhao Z,
    5. Hu S,
    6. Wang X,
    7. Liu X
    . 2014. Surveillance of avirulent Newcastle disease viruses at live bird markets in Eastern China during 2008-2012 reveals a new sub-genotype of class I virus. Virol J 11:211. doi:10.1186/s12985-014-0211-2.
    OpenUrlCrossRefPubMed
  8. 8.↵
    1. Wu W,
    2. Liu H,
    3. Zhang T,
    4. Han Z,
    5. Jiang Y,
    6. Xu Q,
    7. Shao Y,
    8. Li H,
    9. Kong X,
    10. Chen H,
    11. Liu S
    . 2015. Molecular and antigenic characteristics of Newcastle disease virus isolates from domestic ducks in China. Infect Genet Evol 32:34–43. doi:10.1016/j.meegid.2015.02.016.
    OpenUrlCrossRefPubMed
  9. 9.↵
    1. Liu X,
    2. Wang X,
    3. Wu S,
    4. Hu S,
    5. Peng Y,
    6. Xue F,
    7. Liu X
    . 2009. Surveillance for avirulent Newcastle disease viruses in domestic ducks (Anas platyrhynchos and Cairina moschata) at live bird markets in Eastern China and characterization of the viruses isolated. Avian Pathol 38:377–391. doi:10.1080/03079450903183637.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Kim LM,
    2. King DJ,
    3. Curry PE,
    4. Suarez DL,
    5. Swayne DE,
    6. Stallknecht DE,
    7. Slemons RD,
    8. Pedersen JC,
    9. Senne DA,
    10. Winker K,
    11. Afonso CL
    . 2007. Phylogenetic diversity among low-virulence Newcastle disease viruses from waterfowl and shorebirds and comparison of genotype distributions to those of poultry-origin isolates. J Virol 81:12641–12653. doi:10.1128/JVI.00843-07.
    OpenUrlAbstract/FREE Full Text
  11. 11.↵
    1. Webster RG,
    2. Bean WJ,
    3. Gorman OT,
    4. Chambers TM,
    5. Kawaoka Y
    . 1992. Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179.
    OpenUrlAbstract/FREE Full Text
  12. 12.↵
    1. Senne DA,
    2. Panigrahy B,
    3. Kawaoka Y,
    4. Pearson JE,
    5. Suss J,
    6. Lipkind M,
    7. Kida H,
    8. Webster RG
    . 1996. Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 40:425–437. doi:10.2307/1592241.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    1. Gould AR,
    2. Kattenbelt JA,
    3. Selleck P,
    4. Hansson E,
    5. Della-Porta A,
    6. Westbury HA
    . 2001. Virulent Newcastle disease in Australia: Molecular epidemiological analysis of viruses isolated prior to and during the outbreaks of 1998-2000. Virus Res 77:51–60. doi:10.1016/S0168-1702(01)00265-9.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.↵
    1. Alexander DJ,
    2. Campbell G,
    3. Manvell RJ,
    4. Collins MS,
    5. Parsons G,
    6. McNulty MS
    . 1992. Characterisation of an antigenically unusual virus responsible for two outbreaks of Newcastle disease in the Republic of Ireland in 1990. Vet Rec 130:65–68. doi:10.1136/vr.130.4.65.
    OpenUrlAbstract
  15. 15.↵
    OIE. 2008. Manual of diagnostic tests and vaccines for terrestrial animals: mammals, birds, and bees, 6th ed, p 1092–1106. International Office of Epizootics, World Organization for Animal Health, Paris, France.
  16. 16.↵
    1. Yang CY,
    2. Shieh HK,
    3. Lin YL,
    4. Chang PC
    . 1999. Newcastle disease virus isolated from recent outbreaks in Taiwan phylogenetically related to viruses (genotype VII) from recent outbreaks in western Europe. Avian Dis 43:125–130. doi:10.2307/1592771.
    OpenUrlCrossRefPubMed
  17. 17.↵
    1. Wu S,
    2. Wang W,
    3. Yao C,
    4. Wang X,
    5. Hu S,
    6. Cao J,
    7. Wu Y,
    8. Liu W,
    9. Liu X
    . 2011. Genetic diversity of Newcastle disease viruses isolated from domestic poultry species in Eastern China during 2005-2008. Arch Virol 156:253–261. doi:10.1007/s00705-010-0851-5.
    OpenUrlCrossRef
  18. 18.↵
    1. Tamura K,
    2. Stecher G,
    3. Peterson D,
    4. Filipski A,
    5. Kumar S
    . 2013. MEGA6: molecular evolutionary genetics analysis, version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    1. Sakai K,
    2. Sakabe G,
    3. Tani O,
    4. Watanabe Y,
    5. Jahangir A,
    6. Nakamura M,
    7. Takehara K
    . 2007. Characterization of Newcastle disease virus isolated from northern pintail (Anas acuta) in Japan. J Vet Med Sci 69:1307–1311. doi:10.1292/jvms.69.1307.
    OpenUrlCrossRefPubMed
  20. 20.↵
    1. Lee EK,
    2. Jeon WJ,
    3. Kwon JH,
    4. Yang CB,
    5. Choi KS
    . 2009. Molecular epidemiological investigation of Newcastle disease virus from domestic ducks in Korea. Vet Microbiol 134:241–248. doi:10.1016/j.vetmic.2008.08.020.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    1. Kim BY,
    2. Lee DH,
    3. Kim MS,
    4. Jang JH,
    5. Lee YN,
    6. Park JK,
    7. Yuk SS,
    8. Lee JB,
    9. Park SY,
    10. Choi IS,
    11. Song CS
    . 2012. Exchange of Newcastle disease viruses in Korea: the relatedness of isolates between wild birds, live bird markets, poultry farms and neighboring countries. Infect Genet Evol 12:478–482. doi:10.1016/j.meegid.2011.12.004.
    OpenUrlCrossRefPubMed
  22. 22.↵
    1. Muzyka D,
    2. Pantin-Jackwood M,
    3. Stegniy B,
    4. Rula O,
    5. Bolotin V,
    6. Stegniy A,
    7. Gerilovych A,
    8. Shutchenko P,
    9. Stegniy M,
    10. Koshelev V,
    11. Maiorova K,
    12. Tkachenko S,
    13. Muzyka N,
    14. Usova L,
    15. Afonso CL
    . 2014. Wild bird surveillance for avian paramyxoviruses in the Azov-black sea region of Ukraine (2006 to 2011) reveals epidemiological connections with Europe and Africa. Appl Environ Microbiol 80:5427–5438. doi:10.1128/AEM.00733-14.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    1. Takakuwa H,
    2. Ito T,
    3. Takada A,
    4. Okazaki K,
    5. Kida H
    . 1998. Potentially virulent Newcastle disease viruses are maintained in migratory waterfowl populations. Jpn J Vet Res 45:207–215.
    OpenUrlPubMed
  24. 24.↵
    1. Shengqing Y,
    2. Kishida N,
    3. Ito H,
    4. Kida H,
    5. Otsuki K,
    6. Kawaoka Y,
    7. Ito T
    . 2002. Generation of velogenic Newcastle disease viruses from a nonpathogenic waterfowl isolate by passaging in chickens. Virology 301:206–211. doi:10.1006/viro.2002.1539.
    OpenUrlCrossRefPubMed
  25. 25.↵
    1. Tsunekuni R,
    2. Ito H,
    3. Otsuki K,
    4. Kida H,
    5. Ito T
    . 2010. Genetic comparisons between lentogenic Newcastle disease virus isolated from waterfowl and velogenic variants. Virus Genes 40:252–255. doi:10.1007/s11262-009-0427-1.
    OpenUrlCrossRefPubMed
  26. 26.↵
    1. Meng C,
    2. Qiu X,
    3. Jin S,
    4. Yu S,
    5. Chen H,
    6. Ding C
    . 2012. Whole genome sequencing and biological characterization of Duck/JS/10, a new lentogenic class I Newcastle disease virus. Arch Virol 157:869–880. doi:10.1007/s00705-012-1248-4.
    OpenUrlCrossRefPubMed
  27. 27.↵
    1. Han GZ,
    2. He CQ,
    3. Ding NZ,
    4. Ma LY
    . 2008. Identification of a natural multi-recombinant of Newcastle disease virus. Virology 371:54–60. doi:10.1016/j.virol.2007.09.038.
    OpenUrlCrossRefPubMed
  28. 28.↵
    1. Qin Z,
    2. Sun L,
    3. Ma B,
    4. Cui Z,
    5. Zhu Y,
    6. Kitamura Y,
    7. Liu W
    . 2008. F gene recombination between genotype II and VII Newcastle disease virus. Virus Res 131:299–303. doi:10.1016/j.virusres.2007.10.001.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.↵
    1. Miller PJ,
    2. Kim LM,
    3. Ip HS,
    4. Afonso CL
    . 2009. Evolutionary dynamics of Newcastle disease virus. Virology 391:64–72. doi:10.1016/j.virol.2009.05.033.
    OpenUrlCrossRefPubMed
  30. 30.↵
    1. Chong YL,
    2. Padhi A,
    3. Hudson PJ,
    4. Poss M
    . 2010. The effect of vaccination on the evolution and population dynamics of avian paramyxovirus-1. PLoS Pathog 6:e1000872. doi:10.1371/journal.ppat.1000872.
    OpenUrlCrossRefPubMed
  31. 31.↵
    1. Zhang R,
    2. Wang X,
    3. Su J,
    4. Zhao J,
    5. Zhang G
    . 2010. Isolation and analysis of two naturally occurring multi-recombination Newcastle disease viruses in China. Virus Res 151:45–53. doi:10.1016/j.virusres.2010.03.015.
    OpenUrlCrossRefPubMed
  32. 32.↵
    1. Han GZ,
    2. Worobey M
    . 2011. Homologous recombination in negative sense RNA viruses. Viruses 3:1358–1373. doi:10.3390/v3081358.
    OpenUrlCrossRefPubMed
  33. 33.↵
    1. Afonso CL
    . 2008. Not so fast on recombination analysis of Newcastle disease virus. J Virol 82:9303. doi:10.1128/JVI.01231-08.
    OpenUrlFREE Full Text
PreviousNext
Back to top
Download PDF
Citation Tools
High Genetic Diversity of Newcastle Disease Virus in Wild and Domestic Birds in Northeastern China from 2013 to 2015 Reveals Potential Epidemic Trends
Pingze Zhang, Guangyao Xie, Xinxin Liu, Lili Ai, Yanyu Chen, Xin Meng, Yuhai Bi, Jianjun Chen, Yuzhang Sun, Tobias Stoeger, Zhuang Ding, Renfu Yin
Applied and Environmental Microbiology Feb 2016, 82 (5) 1530-1536; DOI: 10.1128/AEM.03402-15

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Applied and Environmental Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
High Genetic Diversity of Newcastle Disease Virus in Wild and Domestic Birds in Northeastern China from 2013 to 2015 Reveals Potential Epidemic Trends
(Your Name) has forwarded a page to you from Applied and Environmental Microbiology
(Your Name) thought you would be interested in this article in Applied and Environmental Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
High Genetic Diversity of Newcastle Disease Virus in Wild and Domestic Birds in Northeastern China from 2013 to 2015 Reveals Potential Epidemic Trends
Pingze Zhang, Guangyao Xie, Xinxin Liu, Lili Ai, Yanyu Chen, Xin Meng, Yuhai Bi, Jianjun Chen, Yuzhang Sun, Tobias Stoeger, Zhuang Ding, Renfu Yin
Applied and Environmental Microbiology Feb 2016, 82 (5) 1530-1536; DOI: 10.1128/AEM.03402-15
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • INTRODUCTION
    • MATERIALS AND METHODS
    • RESULTS AND DISCUSSION
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

Cited By...

About

  • About AEM
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AppEnvMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

 

Print ISSN: 0099-2240; Online ISSN: 1098-5336