Journal of Medical Virology 87:2018–2020 (2015)
Lack of Exposure of H10N8 Avian Influenza Virus Among Veterinarians in Guangdong Province, China Lingshuang Sun,1,2 Lifang Wang,1 Weidong Zhang,3 Yankuo Sun,1 Yongfeng Luo,1 Yao Sun,1 Ziguo Yuan,1,2 Heng Wang,1,2 Zhangyong Ning,1,2 Kun Jia,1,2 and Li-guo Yuan1,2* 1
College of Veterinary Medicine, South China Agricultural University, Guangdong Province 510642, People’s Republic of China 2 Guangdong Provincial Key Laboratory of Prevention and Control for Severe Clinical Animal Diseases, Guangdong Province 510642, People’s Republic of China 3 Hospital of South China Agricultural University, Guangzhou 510642, China
We conducted a retrospective seroepidemiological study for H10N8 avian influenza infection among 400 veterinarians sampled from February 2013 to August 2013 in Guangdong Province, China. None of the veterinarians had evidence of previous infection with the emergent H10N8 AIV. Although there is no evidence of H10N8-infected veterinarian before the first human index case of H10N8 infection in southern China, a more rigorous and long-term surveillance remained essential for early warning of novel reassortant viruses and interspecies transmission events. J. Med. Virol. 87:2018– 2020, 2015. © 2015 Wiley Periodicals, Inc. KEY WORDS:
avian influenza virus; seroepidemiological study; veterinarian
INTRODUCTION Human infections with novel influenza A (H7N9) virus were first identified in China in March 2013. As
of October 18, 2014, a total of 456 human infections of H7N9 in China have been reported to the World Health Organization [Gao et al., 2013]. At the end of 2013, another novel avian influenza A (H10N8) virus has also been reported to cause human death but no apparent outbreaks in poultry has emerged in Nanchang City, China. To our knowledge, it’s the first time that H10N8 virus has infected people and caused fatal case [Qi et al., 2014]. Particularly, the H10N8 virus emergence coincided with a second wave of human H7N9 AIV outbreak [Garcia-Sastre and Schmolke, 2014], and subsequent to the human index case more H10N8 AIV infections have been detected in both avian and mammal species [Jiao et al., 2012; Su et al., 2014a; To et al., 2014; Xu et al., 2015]. Veterinarians are high risk groups of people with zoonotic disease infection based on epidemiological and serological evidence [Koopmans et al., 2004; Myers et al., 2007] due to the nature of their work environment and practices. Thus, veterinarians working with pet birds, poultry farms, and live poultry markets may have more intense and frequent exposure to diseased poultry than poultry workers themselves. As H10N8 AIV was first identified in a duck from Guangdong Province in 2012
Abbreviations: HI, hemagglutination inhibition; MN, microneutralization; AIV, avian influenza virus Grant sponsor: the National Natural Science Foundation of China; Grant number: 31402259; Grant sponsor: the Promote Scientific and Technological Development Program of Guangdong Province; Grant number: 2013B040200032; Grant sponsor: Special Fund for Agro-scientific Research in the Public Interest; Grant number: 201303042; Grant sponsor: Science and Technology Planning Project of Guangdong Province; Grant number: 20140224; Grant sponsor: the Natural Science Foundation of Guangdong Province, China; Grant number: S2013020013858; Grant sponsor: Guangdong Provincial Key Laboratory of Prevention and Control for Severe Clincal Animal Diseases; Grant number: 2013A061401013 Conflict of interest: The authors declare that there is no conflict of interest regarding the publication of this article. Lingshuang Sun, Lifang Wang, and Weidong Zhang contributed equally to this work. Correspondence to: Li-guo Yuan, College of Veterinary Medicine, South China Agricultural University, Guangdong Province 510642, People’s Republic of China. E-mail: [email protected] Accepted 10 May 2015 DOI 10.1002/jmv.24268 Published online 2 June 2015 in Wiley Online Library (wileyonlinelibrary.com). C 2015 WILEY PERIODICALS, INC.
Lack of exposure of H10N8 Avian Influenza Virus
2019
[Jiao et al., 2012], it seems important to understand whether subclinical human infection with the H10N8 virus occurred before November 30, 2013. Therefore, we conducted a retrospective seroepidemiological study for H10N8 infection among veterinarians in Guangdong Province.
However, no statistical significant difference was found between parameter of HI and gender, age, or occupation age. Additionally, none of the three samples were positive tested by the MN assay.
MATERIALS AND METHODS
According to the serological evidence, veterinarians are at high risk of AIV infection [Koopmans et al., 2004; Myers et al., 2007], which may be due to their more intense and frequent exposure to diseased poultry. An epizootic of H7N7 AIV in the Netherlands resulted in the death of a veterinarian [Koopmans et al., 2004]. Detection of antibodies against subtypes H5, H6, and H7 have been reported in a sero survey of veterinarians in the United States [Myers et al., 2007]. Therefore, veterinarians may serve as a more sensitive sentinel for investigating emerging zoonosis of influenza A virus, such as the novel H10N8 virus. In this seralogic survey of veterinarian with H10N8 infections during first half year of 2013 in Guangdong Province, no seral positive was observed using two methods with HI titers 1:20 and MN titers 1:80. Our study has a number of limitations. Three samples low titer antibody to H10N8 measured by HI may indicate antibody generated after H10N8 infection, or crossreactive antibody after a different influenza virus infection.We have also lack investigated seroprevalence of antibody to H5N1 and H7N9 in these samples. Although it remains possible that true infections with H10N8 among veterinarians could have been missed, it is essential to confirm the positive is guaranteed precision by the two tests since HI test is not 100% specific and MN method also is not 100% sensitive. No sera positive against H10N8 virus indicated that no evidence for human infection with the novel avian-origin influenza A (H10N8) virus in China during February 2013 to August 2013. It may prove to be important in considering the origins of the H10N8 AIV, since first human infection case with H10N8 was reported at the end of 2013. More importantly, these seroepidemiological findings are corroborated by our previous epidemiologic study which suggested that H10N8 was recently circulating among poultry in Guangdong Province in 2012 [Jiao et al., 2012]. This also suggests that poultry workers may be unable to obtain specific immunity to H10N8
Veterinarians from Guangzhou, Shenzhen, Huizhou, and Zhuhai in Guangdong Province were recruited for the study. A total of 400 serum samples from veterinarians who were in close contact with poultry populations in the last year were collected during the period February 2013 to August 2013 (Table I). The sera were tested by a horse RBC hemagglutination inhibition (HI) assays against H10N8 influenza virus, according to the World Health Organization guidelines [Marschall et al., 2008; Su et al., 2014b]. It is important to note that horse RBCs show a high proportion of sialic acid a2,3-Gal binding, which is preferential for AIV. It is observed that use of horse RBCs significantly increased the sensitivity of detection of HI antibodies in the sera of confirmed H7N9 cases compared with the use of turkey RBCs, thus the World Health Organization recommends that horse RBCs should be used to detect HI antibodies for H7N9 virus infection . So we used the 1.0% horse RBC HI assay to look for evidence of previous H10N8 virus infection. The A/Jiangxi-Donghu/346-1/2013 (H10N8) was used in the assay (rescued virus generated by Dr. Gang Lu via reverse genetic). Sera with HI titers 1:20 were further studied with microneutralization (MN) assays against the same virus. The MN assay was performed according to the World Health Organization guidelines [Marschall et al., 2008; Su et al., 2014b]. Only the sera with both HI 1:20 and MN titers 1:80 were regarded as having evidence of previous infection with influenza A (H10N8) virus. RESULTS Three of 400 sera had HI titers 1:20 against the H10N8 antigen (Table II). Two positive sera were from poultry farm veterinarians in Guangzhou, with HI titer of 1:40 and 1:20. One from the veterinarian official in Huizhou had HI titer of 1:20 (Table II). All the positive sera were from male veterinarians.
DISCUSSIONS AND CONCLUSIONS
TABLE I. Characteristics of Participants in the Serological Survey in Guangdong Province, China
Total No. Demographic description Occupation
Median of age (range) No. of female (%) Median of occupation age pet birds veterinarian veterinary official Poultry farm veterinarian
Guangzhou
Shenzhen
Huizhou
Zhuhai
100 32 (24-53) 12 (12) 11.21 13 24 63
100 33 (29-61) 5 (5) 14.22 17 31 52
100 39 (27-63) 16 (16) 18.56 9 18 73
100 28 (21-50) 2 (2) 8.68 11 18 71
Occupation age: from the start engaged in veterinary occupational to the time when we collected samples.
J. Med. Virol. DOI 10.1002/jmv
2020
Sun et al. TABLE II. Serological Survey of Veterinarian Infection With H10n8 in Guangdong Province, China
Sample No. 116 180 225
Age
Occupation
Occupation age
Location
HI titer
MN titer
43 31 37
Poultry farm veterinarians Poultry farm veterinarians Veterinarian official
9 5 7
Guangzhou Guangzhou Huizhou
1:40 1:20 1:20
0 0 0
Occupation age: from the start engaged in veterinary occupational to the time when we collected samples.
through subclinical A (H10N8) infection. Thus, may explain why human lack population immunity against A (H10N8) viruses. Similar to the case avian influenza A H5N1 virus infection in Hong Kong in 1997, as suggested by Chen, more human cases of H10N8 infection might occur in the future [Chen et al., 2014]. As novel viruses may rapidly change, it seems prudent to continue surveillance for the H10N8 virus among veterinarians in China. In summary, there is no evidence of H10N8infected veterinarian before the first human index case of H10N8 infection in southern China and it is reassuring that our veterinary samples were not found to be seropositive. Thus, a more rigorous and long-term surveillance remained essential for early warning of novel reassortant viruses and interspecies transmission events[Su et al., 2014b], it seems prudent to continue surveillance for the H10N8 virus among high-risk groups such as poultry workers, veterinarians, healthcare, and non-healthcare workers. ACKNOWLEDGEMENTS The use of the rescued H10N8 virus by Dr. Gang Lu is gratefully acknowledged. The review and approval of the protocol by the Institutional Review Board at the Guangdong Center for Disease Control and Prevention is also appreciated. ETHICAL APPROVAL This study protocol was reviewed and approved by the Institutional Review Board at the South China Agricultural University Hospital. REFERENCES Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Zhang Y, Li H, Gong T, Shi Y, Ni X, Li J, Zhou J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y. 2014. Clinical and epidemiological characteristics
J. Med. Virol. DOI 10.1002/jmv
of a fatal case of avian influenza A H10N8 virus infection: A descriptive study. Lancet 383:714–721. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N Eng J Med 368:1888– 1897. Garcia-Sastre A, Schmolke M. 2014. Avian influenza A H10N8-a virus on the verge? Lancet 383:676–677. Jiao P, Cao L, Yuan R, Wei L, Song Y, Shen D, Gong L, Luo K, Ren T, Liao M. 2012. Complete genome sequence of an H10N8 avian influenza virus isolated from a live bird market in Southern China. J Virol 86:7716. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, Meijer A, van Steenbergen J, Fouchier R, Osterhaus A, Bosman A. 2004. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587–593. Marschall J, Schulz B, Harder Priv-Doz TC, Vahlenkamp Priv-Doz TW, Huebner J, Huisinga E, Hartmann K. 2008. Prevalence of influenza A H5N1 virus in cats from areas with occurrence of highly pathogenic avian influenza in birds. J Feline Med Surg 10:355–358. Myers KP, Setterquist SF, Capuano AW, Gray GC. 2007. Infection due to 3 Avian influenza subtypes in United States veterinarians. Clin Infect Dis 45:4–9. Qi W, Zhou X, Shi W, Huang L, Xia W, Liu D, Li H, Chen S, Lei F, Cao L, Wu J, He F, Song W, Li Q, Li H, Liao M, Liu M. 2014. Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry, China. Euro Surveill 19. Report of Health and Family Planning Commission of Jiangxi Province. 2014. The third human case of H10N8 bird flu was confirmed. 2014 China. (Site):http://www.jxwst.gov.cn/gzdt/ 201402/t20140213_20308109.htm. Su S, Qi WB, Zhou P, Xiao CC, Yan ZS, Cui J, Jia K, Zhang GH, Gray GC, Liao M, Li SJ. 2014a. First evidence of H10N8 avian influenza virus infections among feral dogs in live poultry markets in Guangdong Province, China. Clin Infect Dis 59. Su S, Zhou P, Fu X, Wang L, Hong M, Lu G, Sun L, Qi W, Ning Z, Jia K, Yuan Z, Wang H, Ke C, Wu J, Zhang G, Gray GC, Li S. 2014b. Virological and epidemiological evidence of avian influenza virus infections among feral dogs in live poultry markets, china: A threat to human health? Clin Infect Dis 58:1644–1646. To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen K-Y. 2014. Emergence in China of human disease due to avian influenza A (H10N8)-Cause for concern? J Infect 68:205–215. Xu Y, Cao H, Liu H, Sun H, Martin B, Zhao Y, Wang Q, Deng G, Xue J, Zong Y, Zhu J, Wen F, Long LP, Wong SS, Zhao N, Fu X, Liao M, Hu G, Webby R, Gao GF, Wan XF. 2015. Identification of the source of A (H10N8) virus causing human infection. Infect Genet Evol 30:159–163.
Lack of Exposure of H10N8 Avian Influenza Virus Among Veterinarians in Guangdong Province, China Lingshuang Sun,1,2 Lifang Wang,1 Weidong Zhang,3 Yankuo Sun,1 Yongfeng Luo,1 Yao Sun,1 Ziguo Yuan,1,2 Heng Wang,1,2 Zhangyong Ning,1,2 Kun Jia,1,2 and Li-guo Yuan1,2* 1
College of Veterinary Medicine, South China Agricultural University, Guangdong Province 510642, People’s Republic of China 2 Guangdong Provincial Key Laboratory of Prevention and Control for Severe Clinical Animal Diseases, Guangdong Province 510642, People’s Republic of China 3 Hospital of South China Agricultural University, Guangzhou 510642, China
We conducted a retrospective seroepidemiological study for H10N8 avian influenza infection among 400 veterinarians sampled from February 2013 to August 2013 in Guangdong Province, China. None of the veterinarians had evidence of previous infection with the emergent H10N8 AIV. Although there is no evidence of H10N8-infected veterinarian before the first human index case of H10N8 infection in southern China, a more rigorous and long-term surveillance remained essential for early warning of novel reassortant viruses and interspecies transmission events. J. Med. Virol. 87:2018– 2020, 2015. © 2015 Wiley Periodicals, Inc. KEY WORDS:
avian influenza virus; seroepidemiological study; veterinarian
INTRODUCTION Human infections with novel influenza A (H7N9) virus were first identified in China in March 2013. As
of October 18, 2014, a total of 456 human infections of H7N9 in China have been reported to the World Health Organization [Gao et al., 2013]. At the end of 2013, another novel avian influenza A (H10N8) virus has also been reported to cause human death but no apparent outbreaks in poultry has emerged in Nanchang City, China. To our knowledge, it’s the first time that H10N8 virus has infected people and caused fatal case [Qi et al., 2014]. Particularly, the H10N8 virus emergence coincided with a second wave of human H7N9 AIV outbreak [Garcia-Sastre and Schmolke, 2014], and subsequent to the human index case more H10N8 AIV infections have been detected in both avian and mammal species [Jiao et al., 2012; Su et al., 2014a; To et al., 2014; Xu et al., 2015]. Veterinarians are high risk groups of people with zoonotic disease infection based on epidemiological and serological evidence [Koopmans et al., 2004; Myers et al., 2007] due to the nature of their work environment and practices. Thus, veterinarians working with pet birds, poultry farms, and live poultry markets may have more intense and frequent exposure to diseased poultry than poultry workers themselves. As H10N8 AIV was first identified in a duck from Guangdong Province in 2012
Abbreviations: HI, hemagglutination inhibition; MN, microneutralization; AIV, avian influenza virus Grant sponsor: the National Natural Science Foundation of China; Grant number: 31402259; Grant sponsor: the Promote Scientific and Technological Development Program of Guangdong Province; Grant number: 2013B040200032; Grant sponsor: Special Fund for Agro-scientific Research in the Public Interest; Grant number: 201303042; Grant sponsor: Science and Technology Planning Project of Guangdong Province; Grant number: 20140224; Grant sponsor: the Natural Science Foundation of Guangdong Province, China; Grant number: S2013020013858; Grant sponsor: Guangdong Provincial Key Laboratory of Prevention and Control for Severe Clincal Animal Diseases; Grant number: 2013A061401013 Conflict of interest: The authors declare that there is no conflict of interest regarding the publication of this article. Lingshuang Sun, Lifang Wang, and Weidong Zhang contributed equally to this work. Correspondence to: Li-guo Yuan, College of Veterinary Medicine, South China Agricultural University, Guangdong Province 510642, People’s Republic of China. E-mail: [email protected] Accepted 10 May 2015 DOI 10.1002/jmv.24268 Published online 2 June 2015 in Wiley Online Library (wileyonlinelibrary.com). C 2015 WILEY PERIODICALS, INC.
Lack of exposure of H10N8 Avian Influenza Virus
2019
[Jiao et al., 2012], it seems important to understand whether subclinical human infection with the H10N8 virus occurred before November 30, 2013. Therefore, we conducted a retrospective seroepidemiological study for H10N8 infection among veterinarians in Guangdong Province.
However, no statistical significant difference was found between parameter of HI and gender, age, or occupation age. Additionally, none of the three samples were positive tested by the MN assay.
MATERIALS AND METHODS
According to the serological evidence, veterinarians are at high risk of AIV infection [Koopmans et al., 2004; Myers et al., 2007], which may be due to their more intense and frequent exposure to diseased poultry. An epizootic of H7N7 AIV in the Netherlands resulted in the death of a veterinarian [Koopmans et al., 2004]. Detection of antibodies against subtypes H5, H6, and H7 have been reported in a sero survey of veterinarians in the United States [Myers et al., 2007]. Therefore, veterinarians may serve as a more sensitive sentinel for investigating emerging zoonosis of influenza A virus, such as the novel H10N8 virus. In this seralogic survey of veterinarian with H10N8 infections during first half year of 2013 in Guangdong Province, no seral positive was observed using two methods with HI titers 1:20 and MN titers 1:80. Our study has a number of limitations. Three samples low titer antibody to H10N8 measured by HI may indicate antibody generated after H10N8 infection, or crossreactive antibody after a different influenza virus infection.We have also lack investigated seroprevalence of antibody to H5N1 and H7N9 in these samples. Although it remains possible that true infections with H10N8 among veterinarians could have been missed, it is essential to confirm the positive is guaranteed precision by the two tests since HI test is not 100% specific and MN method also is not 100% sensitive. No sera positive against H10N8 virus indicated that no evidence for human infection with the novel avian-origin influenza A (H10N8) virus in China during February 2013 to August 2013. It may prove to be important in considering the origins of the H10N8 AIV, since first human infection case with H10N8 was reported at the end of 2013. More importantly, these seroepidemiological findings are corroborated by our previous epidemiologic study which suggested that H10N8 was recently circulating among poultry in Guangdong Province in 2012 [Jiao et al., 2012]. This also suggests that poultry workers may be unable to obtain specific immunity to H10N8
Veterinarians from Guangzhou, Shenzhen, Huizhou, and Zhuhai in Guangdong Province were recruited for the study. A total of 400 serum samples from veterinarians who were in close contact with poultry populations in the last year were collected during the period February 2013 to August 2013 (Table I). The sera were tested by a horse RBC hemagglutination inhibition (HI) assays against H10N8 influenza virus, according to the World Health Organization guidelines [Marschall et al., 2008; Su et al., 2014b]. It is important to note that horse RBCs show a high proportion of sialic acid a2,3-Gal binding, which is preferential for AIV. It is observed that use of horse RBCs significantly increased the sensitivity of detection of HI antibodies in the sera of confirmed H7N9 cases compared with the use of turkey RBCs, thus the World Health Organization recommends that horse RBCs should be used to detect HI antibodies for H7N9 virus infection . So we used the 1.0% horse RBC HI assay to look for evidence of previous H10N8 virus infection. The A/Jiangxi-Donghu/346-1/2013 (H10N8) was used in the assay (rescued virus generated by Dr. Gang Lu via reverse genetic). Sera with HI titers 1:20 were further studied with microneutralization (MN) assays against the same virus. The MN assay was performed according to the World Health Organization guidelines [Marschall et al., 2008; Su et al., 2014b]. Only the sera with both HI 1:20 and MN titers 1:80 were regarded as having evidence of previous infection with influenza A (H10N8) virus. RESULTS Three of 400 sera had HI titers 1:20 against the H10N8 antigen (Table II). Two positive sera were from poultry farm veterinarians in Guangzhou, with HI titer of 1:40 and 1:20. One from the veterinarian official in Huizhou had HI titer of 1:20 (Table II). All the positive sera were from male veterinarians.
DISCUSSIONS AND CONCLUSIONS
TABLE I. Characteristics of Participants in the Serological Survey in Guangdong Province, China
Total No. Demographic description Occupation
Median of age (range) No. of female (%) Median of occupation age pet birds veterinarian veterinary official Poultry farm veterinarian
Guangzhou
Shenzhen
Huizhou
Zhuhai
100 32 (24-53) 12 (12) 11.21 13 24 63
100 33 (29-61) 5 (5) 14.22 17 31 52
100 39 (27-63) 16 (16) 18.56 9 18 73
100 28 (21-50) 2 (2) 8.68 11 18 71
Occupation age: from the start engaged in veterinary occupational to the time when we collected samples.
J. Med. Virol. DOI 10.1002/jmv
2020
Sun et al. TABLE II. Serological Survey of Veterinarian Infection With H10n8 in Guangdong Province, China
Sample No. 116 180 225
Age
Occupation
Occupation age
Location
HI titer
MN titer
43 31 37
Poultry farm veterinarians Poultry farm veterinarians Veterinarian official
9 5 7
Guangzhou Guangzhou Huizhou
1:40 1:20 1:20
0 0 0
Occupation age: from the start engaged in veterinary occupational to the time when we collected samples.
through subclinical A (H10N8) infection. Thus, may explain why human lack population immunity against A (H10N8) viruses. Similar to the case avian influenza A H5N1 virus infection in Hong Kong in 1997, as suggested by Chen, more human cases of H10N8 infection might occur in the future [Chen et al., 2014]. As novel viruses may rapidly change, it seems prudent to continue surveillance for the H10N8 virus among veterinarians in China. In summary, there is no evidence of H10N8infected veterinarian before the first human index case of H10N8 infection in southern China and it is reassuring that our veterinary samples were not found to be seropositive. Thus, a more rigorous and long-term surveillance remained essential for early warning of novel reassortant viruses and interspecies transmission events[Su et al., 2014b], it seems prudent to continue surveillance for the H10N8 virus among high-risk groups such as poultry workers, veterinarians, healthcare, and non-healthcare workers. ACKNOWLEDGEMENTS The use of the rescued H10N8 virus by Dr. Gang Lu is gratefully acknowledged. The review and approval of the protocol by the Institutional Review Board at the Guangdong Center for Disease Control and Prevention is also appreciated. ETHICAL APPROVAL This study protocol was reviewed and approved by the Institutional Review Board at the South China Agricultural University Hospital. REFERENCES Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, Fan G, Yang F, Li X, Zhou J, Zou S, Yang L, Chen T, Dong L, Bo H, Zhao X, Zhang Y, Lan Y, Bai T, Dong J, Li Q, Wang S, Zhang Y, Li H, Gong T, Shi Y, Ni X, Li J, Zhou J, Fan J, Wu J, Zhou X, Hu M, Wan J, Yang W, Li D, Wu G, Feng Z, Gao GF, Wang Y, Jin Q, Liu M, Shu Y. 2014. Clinical and epidemiological characteristics
J. Med. Virol. DOI 10.1002/jmv
of a fatal case of avian influenza A H10N8 virus infection: A descriptive study. Lancet 383:714–721. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, Dong L, Zhu Y, Bai T, Wang S, Hao P, Yang W, Zhang Y, Han J, Yu H, Li D, Gao GF, Wu G, Wang Y, Yuan Z, Shu Y. 2013. Human infection with a novel avian-origin influenza A (H7N9) virus. N Eng J Med 368:1888– 1897. Garcia-Sastre A, Schmolke M. 2014. Avian influenza A H10N8-a virus on the verge? Lancet 383:676–677. Jiao P, Cao L, Yuan R, Wei L, Song Y, Shen D, Gong L, Luo K, Ren T, Liao M. 2012. Complete genome sequence of an H10N8 avian influenza virus isolated from a live bird market in Southern China. J Virol 86:7716. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, Meijer A, van Steenbergen J, Fouchier R, Osterhaus A, Bosman A. 2004. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587–593. Marschall J, Schulz B, Harder Priv-Doz TC, Vahlenkamp Priv-Doz TW, Huebner J, Huisinga E, Hartmann K. 2008. Prevalence of influenza A H5N1 virus in cats from areas with occurrence of highly pathogenic avian influenza in birds. J Feline Med Surg 10:355–358. Myers KP, Setterquist SF, Capuano AW, Gray GC. 2007. Infection due to 3 Avian influenza subtypes in United States veterinarians. Clin Infect Dis 45:4–9. Qi W, Zhou X, Shi W, Huang L, Xia W, Liu D, Li H, Chen S, Lei F, Cao L, Wu J, He F, Song W, Li Q, Li H, Liao M, Liu M. 2014. Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry, China. Euro Surveill 19. Report of Health and Family Planning Commission of Jiangxi Province. 2014. The third human case of H10N8 bird flu was confirmed. 2014 China. (Site):http://www.jxwst.gov.cn/gzdt/ 201402/t20140213_20308109.htm. Su S, Qi WB, Zhou P, Xiao CC, Yan ZS, Cui J, Jia K, Zhang GH, Gray GC, Liao M, Li SJ. 2014a. First evidence of H10N8 avian influenza virus infections among feral dogs in live poultry markets in Guangdong Province, China. Clin Infect Dis 59. Su S, Zhou P, Fu X, Wang L, Hong M, Lu G, Sun L, Qi W, Ning Z, Jia K, Yuan Z, Wang H, Ke C, Wu J, Zhang G, Gray GC, Li S. 2014b. Virological and epidemiological evidence of avian influenza virus infections among feral dogs in live poultry markets, china: A threat to human health? Clin Infect Dis 58:1644–1646. To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen K-Y. 2014. Emergence in China of human disease due to avian influenza A (H10N8)-Cause for concern? J Infect 68:205–215. Xu Y, Cao H, Liu H, Sun H, Martin B, Zhao Y, Wang Q, Deng G, Xue J, Zong Y, Zhu J, Wen F, Long LP, Wong SS, Zhao N, Fu X, Liao M, Hu G, Webby R, Gao GF, Wan XF. 2015. Identification of the source of A (H10N8) virus causing human infection. Infect Genet Evol 30:159–163.
