Skip to main content
Top
Published in: Archives of Virology 3/2018

01-03-2018 | Original Article

Serological evidence of H5-subtype influenza A virus infection in indigenous avian and mammalian species in Korea

Authors: Hye Kwon Kim, Hee-Jong Kim, Ji Yeong Noh, Le Van Phan, Ji Hyung Kim, Daesub Song, Woonsung Na, Aram Kang, Thi Lan Nguyen, Jeong-Hwa Shin, Dae Gwin Jeong, Sun-Woo Yoon

Published in: Archives of Virology | Issue 3/2018

Login to get access

Abstract

In Korea, H5-subtype highly pathogenic avian influenza (HPAI) has caused huge economic losses in poultry farms through outbreaks of H5N1 since 2003, H5N8 since 2013 and H5N6 since 2016. Although it was reported that long-distance migratory birds may play a major role in the global spread of avian influenza viruses (AIVs), transmission from such birds to poultry has not been confirmed. Intermediate hosts in the wild also may be a potential factor in viral transmission. Therefore, a total of 367 serum samples from wild animals were collected near major migratory bird habitats from 2011 to 2016 and tested by AIV-specific blocking ELISA and hemagglutination inhibition (HI) test. Two mammalian and eight avian species were seropositive according to the ELISA test. Among these, two mammalian (Hydropotes inermis and Prionailurus bengalensis) and three avian (Aegypius monachus, Cygnus cygnus, and Bubo bubo) species showed high HI titres (> 1,280) against one or two H5-subtype AIVs. As H. inermis (water deer), P. bengalensis (leopard cat), and B. bubo (Eurasian eagle owl) are indigenous animals in Korea, evidence of H5-subtype AIV in these animals implies that continuous monitoring of indigenous animals should be followed to understand interspecies transmission ecology of H5-subtype influenza viruses.
Literature
1.
go back to reference Sonnberg S, Webby RJ, Webster RG (2013) Natural history of highly pathogenic avian influenza H5N1. Virus Res 178(1):63–77CrossRefPubMed Sonnberg S, Webby RJ, Webster RG (2013) Natural history of highly pathogenic avian influenza H5N1. Virus Res 178(1):63–77CrossRefPubMed
2.
go back to reference World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5N1 Evolution Working Group (2014) Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respi Viruses 8(3):384–388CrossRef World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5N1 Evolution Working Group (2014) Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respi Viruses 8(3):384–388CrossRef
3.
go back to reference de Vries E, Guo H, Dai M, Rottier PJM, van Kuppeveld FJM, de Haan CAM (2015) Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg Infect Dis 21(5):842–846CrossRefPubMedPubMedCentral de Vries E, Guo H, Dai M, Rottier PJM, van Kuppeveld FJM, de Haan CAM (2015) Rapid emergence of highly pathogenic avian influenza subtypes from a subtype H5N1 hemagglutinin variant. Emerg Infect Dis 21(5):842–846CrossRefPubMedPubMedCentral
4.
go back to reference Si Y-J, Choi WS, Kim Y-I, Lee I-W, Kwon H-I, Park S-J, Kim E-H, Sm Kim, Kwon J-J, Song M-S, Kim C-J, Choi Y-K (2016) Genetic characteristics of highly pathogenic H5N8 avian influenza viruses isolated from migratory wild birds in South Korea during 2014–2015. Arch Virol 161:2749–2764CrossRefPubMed Si Y-J, Choi WS, Kim Y-I, Lee I-W, Kwon H-I, Park S-J, Kim E-H, Sm Kim, Kwon J-J, Song M-S, Kim C-J, Choi Y-K (2016) Genetic characteristics of highly pathogenic H5N8 avian influenza viruses isolated from migratory wild birds in South Korea during 2014–2015. Arch Virol 161:2749–2764CrossRefPubMed
5.
go back to reference Mo IP, Bae YJ, Lee SB, Mo JS, Oh KH, Shin JH, Kang HM, Lee YJ (2016) Review of avian influenza outbreaks in South Korea from 1996 to 2014. Avian Dis 60:172–177CrossRefPubMed Mo IP, Bae YJ, Lee SB, Mo JS, Oh KH, Shin JH, Kang HM, Lee YJ (2016) Review of avian influenza outbreaks in South Korea from 1996 to 2014. Avian Dis 60:172–177CrossRefPubMed
6.
go back to reference Kwon JH, Lee DH, Swayne DE, Noh JY, Yuk SS, Erdene-Ochir TO, Hong WT, Jeong JH, Jeong S, Gwon GB, Song CS (2016) Highly pathogenic avian influenza A(H5N8) viruses reintroduced into South Korea by Migratory Waterfowl, 2014–2015. Emerg Infect Dis 22(3):507–510CrossRefPubMedPubMedCentral Kwon JH, Lee DH, Swayne DE, Noh JY, Yuk SS, Erdene-Ochir TO, Hong WT, Jeong JH, Jeong S, Gwon GB, Song CS (2016) Highly pathogenic avian influenza A(H5N8) viruses reintroduced into South Korea by Migratory Waterfowl, 2014–2015. Emerg Infect Dis 22(3):507–510CrossRefPubMedPubMedCentral
7.
go back to reference The Global Consortium for H5N8 and Related Influenza Viruses (2016) Role for migratory wild birds in the global spread of avian influenza H5N8. Science 354:213–217CrossRef The Global Consortium for H5N8 and Related Influenza Viruses (2016) Role for migratory wild birds in the global spread of avian influenza H5N8. Science 354:213–217CrossRef
8.
go back to reference Bi Y, Mei K, Shi W, Liu D, Yu X, Gao Z, Zhao L, Gao GF, Chen J, Chen Q (2015) Two novel reassortants of avian influenza A (H5N6) virus in China. J GenVirol 96:975–981 Bi Y, Mei K, Shi W, Liu D, Yu X, Gao Z, Zhao L, Gao GF, Chen J, Chen Q (2015) Two novel reassortants of avian influenza A (H5N6) virus in China. J GenVirol 96:975–981
9.
go back to reference Liu H, Zhou X, Zhao Y, Zheng D, Wang J, Wang X, Castellan D, Huang B, Wang Z, Soares Magalhães RJ (2015) Factors associated with the emergence of highly pathogenic avian influenza A (H5N1) poultry outbreaks in China: evidence from an epidemiological investigation in Ningxia, 2012. Transbound Emerg Dis 64:746–753CrossRefPubMed Liu H, Zhou X, Zhao Y, Zheng D, Wang J, Wang X, Castellan D, Huang B, Wang Z, Soares Magalhães RJ (2015) Factors associated with the emergence of highly pathogenic avian influenza A (H5N1) poultry outbreaks in China: evidence from an epidemiological investigation in Ningxia, 2012. Transbound Emerg Dis 64:746–753CrossRefPubMed
10.
go back to reference Wang Y, Li P, Wu Y, Sun X, Yu K, Yu C, Qin A (2014) The risk factors for avian influenza on poultry farms: a meta-analysis. Prev Vet Med 117:1–6CrossRefPubMed Wang Y, Li P, Wu Y, Sun X, Yu K, Yu C, Qin A (2014) The risk factors for avian influenza on poultry farms: a meta-analysis. Prev Vet Med 117:1–6CrossRefPubMed
11.
go back to reference Woo J-T, Park BK (2008) Seroprevalence of low pathogenic avian influenza (H9N2) and associated risk factors in the Gyeonggi-do of Korea during 2005–2006. J Vet Sci 9:161–168CrossRefPubMedPubMedCentral Woo J-T, Park BK (2008) Seroprevalence of low pathogenic avian influenza (H9N2) and associated risk factors in the Gyeonggi-do of Korea during 2005–2006. J Vet Sci 9:161–168CrossRefPubMedPubMedCentral
12.
go back to reference Short KR, Richard M, Verhagen JH, van Riel D, Schrauwen EJA, van den Brand JMA, Mänz B, Bodewes R, Herfst S (2015) One health, multiple challenges: the inter-species transmission of influenza A virus. One Health 1:1–13CrossRefPubMedPubMedCentral Short KR, Richard M, Verhagen JH, van Riel D, Schrauwen EJA, van den Brand JMA, Mänz B, Bodewes R, Herfst S (2015) One health, multiple challenges: the inter-species transmission of influenza A virus. One Health 1:1–13CrossRefPubMedPubMedCentral
13.
go back to reference Yoon S-W, Webby RJ, Webster RG (2014) Evolution and ecology of influenza a viruses. In: Compans RW, Oldstone MBA (eds) Influenza pathogenesis and control, vol I. Springer International Publishing, Cham, pp 359–375 Yoon S-W, Webby RJ, Webster RG (2014) Evolution and ecology of influenza a viruses. In: Compans RW, Oldstone MBA (eds) Influenza pathogenesis and control, vol I. Springer International Publishing, Cham, pp 359–375
14.
go back to reference Song DS, Lee YJ, Jeong OM, Kim YJ, Park CH, Yoo JE, Jeon WJ, Kwon JH, Ha GW, Kang BK, Lee CS, Kim HK, Jung BY, Kim JH, Oh JS (2009) Evaluation of a competitive ELISA for antibody detection against avian influenza virus. J Vet Sci 10:323–329CrossRefPubMedPubMedCentral Song DS, Lee YJ, Jeong OM, Kim YJ, Park CH, Yoo JE, Jeon WJ, Kwon JH, Ha GW, Kang BK, Lee CS, Kim HK, Jung BY, Kim JH, Oh JS (2009) Evaluation of a competitive ELISA for antibody detection against avian influenza virus. J Vet Sci 10:323–329CrossRefPubMedPubMedCentral
15.
go back to reference Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289CrossRefPubMed Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289CrossRefPubMed
16.
go back to reference Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefPubMedPubMedCentral Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefPubMedPubMedCentral
18.
go back to reference Shriner SA, Root JJ, Lutman MW, Kloft JM, VanDalen KK, Sullivan HJ, White TS, Milleson MP, Hairston JL, Chandler SC, Wolf PC, Turnage CT, McCluskey BJ, Vincent AL, Torchetti MK, Gidlewski T, DeLiberto TJ (2016) Surveillance for highly pathogenic H5 avian influenza virus in synanthropic wildlife associated with poultry farms during an acute outbreak. Sci Rep 6:36237CrossRefPubMedPubMedCentral Shriner SA, Root JJ, Lutman MW, Kloft JM, VanDalen KK, Sullivan HJ, White TS, Milleson MP, Hairston JL, Chandler SC, Wolf PC, Turnage CT, McCluskey BJ, Vincent AL, Torchetti MK, Gidlewski T, DeLiberto TJ (2016) Surveillance for highly pathogenic H5 avian influenza virus in synanthropic wildlife associated with poultry farms during an acute outbreak. Sci Rep 6:36237CrossRefPubMedPubMedCentral
19.
go back to reference Wei Y-R, Yang X-Y, Li Y-G, Wei J, Ma W-G, Ren Z-G, Guo H-L, Wang T-C, Mi X-Y, Adili G, Miao S-K, Shaha A, Gao Y-W, Huang J, Xia X-Z (2016) Serological survey of avian influenza virus infection in non-avian wildlife in Xinjiang, China. Arch Virol 161:867–872CrossRefPubMed Wei Y-R, Yang X-Y, Li Y-G, Wei J, Ma W-G, Ren Z-G, Guo H-L, Wang T-C, Mi X-Y, Adili G, Miao S-K, Shaha A, Gao Y-W, Huang J, Xia X-Z (2016) Serological survey of avian influenza virus infection in non-avian wildlife in Xinjiang, China. Arch Virol 161:867–872CrossRefPubMed
20.
go back to reference Horimoto T, Maeda K, Murakami S, Kiso M, Iwatsuki-Horimoto K, Sashika M, Ito T, Suzuki K, Yokoyama M, Kawaoka Y (2011) Highly pathogenic avian influenza virus infection in Feral Raccoons, Japan. Emerg Infect Dis 17:714–717CrossRefPubMedPubMedCentral Horimoto T, Maeda K, Murakami S, Kiso M, Iwatsuki-Horimoto K, Sashika M, Ito T, Suzuki K, Yokoyama M, Kawaoka Y (2011) Highly pathogenic avian influenza virus infection in Feral Raccoons, Japan. Emerg Infect Dis 17:714–717CrossRefPubMedPubMedCentral
22.
go back to reference Yu Z, Gao X, Wang T, Li Y, Li Y, Xu Y, Chu D, Sun H, Wu C, Li S, Wang H, Li Y, Xia Z, Lin W, Qian J, Chen H, Xia X, Gao Y (2015) Fatal H5N6 avian influenza virus infection in a domestic cat and wild birds in China. Sci Rep 5:10704CrossRefPubMedPubMedCentral Yu Z, Gao X, Wang T, Li Y, Li Y, Xu Y, Chu D, Sun H, Wu C, Li S, Wang H, Li Y, Xia Z, Lin W, Qian J, Chen H, Xia X, Gao Y (2015) Fatal H5N6 avian influenza virus infection in a domestic cat and wild birds in China. Sci Rep 5:10704CrossRefPubMedPubMedCentral
23.
go back to reference Li X, Fu Y, Yang J, Guo J, He J, Guo J, Weng S, Jia Y, Liu B, Li X, Zhu Q, Chen H (2015) Genetic and biological characterization of two novel reassortant H5N6 swine influenza viruses in mice and chickens. Infect Genet Evol 36:462–466CrossRefPubMed Li X, Fu Y, Yang J, Guo J, He J, Guo J, Weng S, Jia Y, Liu B, Li X, Zhu Q, Chen H (2015) Genetic and biological characterization of two novel reassortant H5N6 swine influenza viruses in mice and chickens. Infect Genet Evol 36:462–466CrossRefPubMed
24.
go back to reference Li X, Shi J, Guo J, Deng G, Zhang Q, Wang J, He X, Wang K, Chen J, Li Y, Fan J, Kong H, Gu C, Guan Y, Suzuki Y, Kawaoka Y, Liu L, Jiang Y, Tian G, Li Y, Bu Z, Chen H (2014) Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses. PLoS Pathog 10:e1004508CrossRefPubMedPubMedCentral Li X, Shi J, Guo J, Deng G, Zhang Q, Wang J, He X, Wang K, Chen J, Li Y, Fan J, Kong H, Gu C, Guan Y, Suzuki Y, Kawaoka Y, Liu L, Jiang Y, Tian G, Li Y, Bu Z, Chen H (2014) Genetics, receptor binding property, and transmissibility in mammals of naturally isolated H9N2 Avian Influenza viruses. PLoS Pathog 10:e1004508CrossRefPubMedPubMedCentral
25.
go back to reference Kanehira K, Uchida Y, Takemae N, Hikono H, Tsunekuni R, Saito T (2015) Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Arch Virol 160:1629–1643CrossRefPubMed Kanehira K, Uchida Y, Takemae N, Hikono H, Tsunekuni R, Saito T (2015) Characterization of an H5N8 influenza A virus isolated from chickens during an outbreak of severe avian influenza in Japan in April 2014. Arch Virol 160:1629–1643CrossRefPubMed
26.
27.
go back to reference Kaplan BS, Russier M, Jeevan T, Marathe B, Govorkova EA, Russell CJ, Kim-Torchetti M, Choi YK, Brown I, Saito T, Stallknecht DE, Krauss S, Webby RJ (2016) Novel highly pathogenic avian A(H5N2) and A(H5N8) influenza viruses of clade 2.3.4.4 from North America have limited capacity for replication and transmission in mammals. mSphere 1:3–16 Kaplan BS, Russier M, Jeevan T, Marathe B, Govorkova EA, Russell CJ, Kim-Torchetti M, Choi YK, Brown I, Saito T, Stallknecht DE, Krauss S, Webby RJ (2016) Novel highly pathogenic avian A(H5N2) and A(H5N8) influenza viruses of clade 2.3.4.4 from North America have limited capacity for replication and transmission in mammals. mSphere 1:3–16
28.
go back to reference Ducatez MF, Cai Z, Peiris M, Guan Y, Ye Z, Wan X-F, Webby RJ (2011) Extent of antigenic cross-reactivity among highly pathogenic H5N1 influenza viruses. J Clin Microbiol 49:3531–3536CrossRefPubMedPubMedCentral Ducatez MF, Cai Z, Peiris M, Guan Y, Ye Z, Wan X-F, Webby RJ (2011) Extent of antigenic cross-reactivity among highly pathogenic H5N1 influenza viruses. J Clin Microbiol 49:3531–3536CrossRefPubMedPubMedCentral
29.
go back to reference Newman SH, Iverson SA, Takekawa JY, Gilbert M, Prosser DJ, Batbayar N, Natsagdorj T, Douglas DC (2009) Migration of whooper swans and outbreaks of highly pathogenic avian influenza H5N1 virus in eastern Asia. PLoS One 4:e5729CrossRefPubMedPubMedCentral Newman SH, Iverson SA, Takekawa JY, Gilbert M, Prosser DJ, Batbayar N, Natsagdorj T, Douglas DC (2009) Migration of whooper swans and outbreaks of highly pathogenic avian influenza H5N1 virus in eastern Asia. PLoS One 4:e5729CrossRefPubMedPubMedCentral
30.
go back to reference Kim H-R, Lee Y-J, Park C-K, Oem J-K, Lee OS, Kang H-M, Choi J-G, Bae Y-C (2012) Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg Infect Dis 18:480–483CrossRefPubMedPubMedCentral Kim H-R, Lee Y-J, Park C-K, Oem J-K, Lee OS, Kang H-M, Choi J-G, Bae Y-C (2012) Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg Infect Dis 18:480–483CrossRefPubMedPubMedCentral
31.
go back to reference Lopez JW, Woods GT (1984) Influenza virus in ruminants: a review. Research communications in chemical pathology and pharmacology 45:445–462PubMed Lopez JW, Woods GT (1984) Influenza virus in ruminants: a review. Research communications in chemical pathology and pharmacology 45:445–462PubMed
32.
go back to reference Hause BM, Collin EA, Liu R, Huang B, Sheng Z, Lu W, Wang D, Nelson EA, Li F (2014) Characterization of a novel influenza virus in cattle and Swine: proposal for a new genus in the Orthomyxoviridae family. mBio 5:e00031–00041CrossRefPubMedPubMedCentral Hause BM, Collin EA, Liu R, Huang B, Sheng Z, Lu W, Wang D, Nelson EA, Li F (2014) Characterization of a novel influenza virus in cattle and Swine: proposal for a new genus in the Orthomyxoviridae family. mBio 5:e00031–00041CrossRefPubMedPubMedCentral
33.
go back to reference Quast M, Sreenivasan C, Sexton G, Nedland H, Singrey A, Fawcett L, Miller G, Lauer D, Voss S, Pollock S, Cunha CW, Christopher-Hennings J, Nelson E, Li F (2015) Serological evidence for the presence of influenza D virus in small ruminants. Vet Microbiol 180:281–285CrossRefPubMedPubMedCentral Quast M, Sreenivasan C, Sexton G, Nedland H, Singrey A, Fawcett L, Miller G, Lauer D, Voss S, Pollock S, Cunha CW, Christopher-Hennings J, Nelson E, Li F (2015) Serological evidence for the presence of influenza D virus in small ruminants. Vet Microbiol 180:281–285CrossRefPubMedPubMedCentral
34.
go back to reference Kim SH, Choi H, Yoon J, Woo C, Chung HM, Kim JT, Shin JH (2014) Pathogens in water deer (Hydropotes inermis) in South Korea, 2010–12. J Wildlife Dis 50:478–483CrossRef Kim SH, Choi H, Yoon J, Woo C, Chung HM, Kim JT, Shin JH (2014) Pathogens in water deer (Hydropotes inermis) in South Korea, 2010–12. J Wildlife Dis 50:478–483CrossRef
35.
go back to reference Kim SH, Lee JY, Park YS, Yoon JT (2014) Physiological difference of estrus and pregnant ovary in Korean Water Deer. J Emb Trans 29:43–50CrossRef Kim SH, Lee JY, Park YS, Yoon JT (2014) Physiological difference of estrus and pregnant ovary in Korean Water Deer. J Emb Trans 29:43–50CrossRef
36.
go back to reference Root J, Shriner SA, Ellis JW, VanDalen KK, Sullivan HJ, Franklin AB (2015) When fur and feather occur together: interclass transmission of avian influenza A virus from mammals to birds through common resources. Sci Rep 5:14354CrossRefPubMed Root J, Shriner SA, Ellis JW, VanDalen KK, Sullivan HJ, Franklin AB (2015) When fur and feather occur together: interclass transmission of avian influenza A virus from mammals to birds through common resources. Sci Rep 5:14354CrossRefPubMed
Metadata
Title
Serological evidence of H5-subtype influenza A virus infection in indigenous avian and mammalian species in Korea
Authors
Hye Kwon Kim
Hee-Jong Kim
Ji Yeong Noh
Le Van Phan
Ji Hyung Kim
Daesub Song
Woonsung Na
Aram Kang
Thi Lan Nguyen
Jeong-Hwa Shin
Dae Gwin Jeong
Sun-Woo Yoon
Publication date
01-03-2018
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 3/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3655-z

Other articles of this Issue 3/2018

Archives of Virology 3/2018 Go to the issue