- Email: [email protected]
Human infections with avian influenza viruses in mainland China: A particular risk for southeastern China
Accepted Manuscript Human infections with Avian Influenza Viruses in mainland China: a big risk in southeastern China Bin Xiang, Wenxian Zhu, Renrong You, Libin Chen, Yaling Li, Jianpeng Liang, Qiuyan Lin, Ming Liao, Chencheng Xiao, Tao Ren PII:
S0163-4453(17)30136-6
DOI:
10.1016/j.jinf.2017.05.002
Reference:
YJINF 3921
To appear in:
Journal of Infection
Received Date: 3 May 2017 Accepted Date: 4 May 2017
Please cite this article as: Xiang B, Zhu W, You R, Chen L, Li Y, Liang J, Lin Q, Liao M, Xiao C, Ren T, Human infections with Avian Influenza Viruses in mainland China: a big risk in southeastern China, Journal of Infection (2017), doi: 10.1016/j.jinf.2017.05.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1
Human infections with Avian Influenza Viruses in mainland China: a big risk in
2
southeastern China
3
Bin Xiang1,2,3,4, Wenxian Zhu1,2,3,4, Renrong You1,2,3,4, Libin Chen1,2,3,4, Yaling Li5,
5
Jianpeng Liang1,2,3,4, Qiuyan Lin1,2,3,4, Ming Liao1,2,3,4, Chencheng Xiao5,*, Tao
6
Ren1,2,3,4, *
RI PT
4
SC
7 8 1
College of Veterinary Medicine, South China Agricultural University, China
10
2
National and Regional Joint Engineering Laboratory for Medicament of Zoonosis
11
Prevention and Control, China
12
3
Key Laboratory of Animal Vaccine Development, Ministry of Agriculture, China
13
4
Key Laboratory of Zoonosis Prevention and Control of Guangdong
14
Province, China
15
5
TE D
M AN U
9
EP
College of Animal Science and Technology, Shihezi University, Shihezi, China
16
Address for Correspondence:
18
Chencheng Xiao, College of Animal Science and Technology, Shihezi University,
19
Shihezi, China, 832000; Telephone:
20
Email: [email protected]
21
Tao Ren, College of Veterinary Medicine, South China Agricultural University,
22
Guangzhou
23
86-20-85280234, E-mail: [email protected]
AC C
17
510642,
China.
86-188-99591678, Fax:
Telephone:
1
86-0993-2058775,
86-20-85283054
(office),
Fax:
ACCEPTED MANUSCRIPT 24
Dear editor: As reported recently, human infections with different subtypes of avian influenza
26
viruses (AIVs) including H5N1, H5N6, H7N9, H10N8 and H9N2 have been
27
identified in mainland China from 2005 to 2017.1-4 Since the first H5N1 human case
28
was confirmed in Hunan province in December 2005, a total of 46 human cases were
29
reported in mainland China, of which 29 cases were fatal; while human infections
30
with H5N6 virus was firstly documented in Sichuan province on March 3, 2014, 11 of
31
16 patients have been fatal (Table S1). In March 2013, human infections with the
32
novel H7N9 virus were confirmed in Shanghai and Anhui province, 1394 infections
33
and 539 deaths were reported by April 27, 2017. In addition, three H10N8 (two deaths)
34
human cases in Jiangxi province from 2013 to 2014, and two H9N2 human cases
35
without fatality (one in Hunan province in 2014 and one in Guangdong province in
36
2016) were confirmed. Epidemiology analysis displayed that the case fatality rate
37
(CFR) is much higher for high pathogenicity avian influenza (HPAI)—64.52% (40/62)
38
than low pathogenicity avian influenza (LPAI)—38.53% (539/1399), and men are
39
more susceptible to LPAIVs—68.76% (962/1399). Moreover, the age median of
40
H5N1 and H5N6 human case were 27.0- and 29.0-year-old, respectively, while these
41
were 57.9- and 67.7-year-old for H7N9 and H10N8 cases, respectively (Table S1).
42
Notably, the number of H7N9 infections far exceeds human infections caused by
43
other AIVs. Zhao and colleagues have demonstrated that more specific mutations in
44
H7N9 virus (S138A, G186V, T221P, Q226L in HA protein, and Q591K, E627K,
45
D701N in PB2 protein) were observed, associated with its infectivity and
AC C
EP
TE D
M AN U
SC
RI PT
25
2
ACCEPTED MANUSCRIPT transmissibility in mammals or human, when compared to H5N1, H5N6, H9N2 and
47
H10N8.5 On the other hand, LPAIV H7N9 could trigger no illness in poultries, which
48
might increase possibility of close contact with virus contaminated poultries.6 Thus,
49
human is more susceptible to LPAIVs with a lower mortality, when compared to the
50
HPAIVs.
RI PT
46
As shown in Figure 1 A, most of AIV human cases were concentrated in
52
southeastern China. Southeastern China hosts high poultry density and population
53
density with a subtropical monsoon climate (Figure 1 B). Previous study have
54
revealed that exposure to live poultry was a main risk for human infection with AIV.7
55
The largest poultry industry of southeastern China, especially domestic waterfowl
56
industry (three out of five of the world’s population of domestic ducks are raised in
57
these regions), and high population density that associated with a huge consumption
58
of poultry products, increased the chance for human exposure to live poultry.
59
Moreover, previous research has also showed that high humidity and an atmospheric
60
temperature around 15
61
(H7N9), generally consistent with the characteristics of subtropical monsoon climate.8
62
However, human infections with H5N1 virus are most closely linked to the coverage
63
of forest and water body.9 We could observe abundant forest and water resource in
64
southeastern China due to geographical and climatic conditions. Thus, southeastern
65
China has a high risk for human infections with AIV.
TE D
M AN U
SC
51
AC C
EP
were important factors for the risk of avian influenza A
66
To control the current H7N9 epidemic, many effective measures have been
67
implemented, such as temporarily closing live poultry markets and encouraging 3
ACCEPTED MANUSCRIPT 68
chilled instead of live poultry for sale.
69
rural areas should be strengthened and the development of vaccine targeted prevalent
70
LPAIVs should be promoted. Furthermore, to decrease future HPAI and LPAI
71
mortality in human, promoting the development of early and rapid detection and
72
antiviral drug is necessary.
However, surveillance and biosecurity in
RI PT
10
73
SC
74
Reference
76
1.
77
triple-subtype reassortants of fatal human H5N6 avian influenza virus in Yunnan,
78
China. The Journal of infection. 2016 Jun;72(6):753-6. PubMed PMID: 26994688.
79
2.
80
of human disease due to avian influenza A(H10N8)--cause for concern? The Journal
81
of infection. 2014 Mar;68(3):205-15. PubMed PMID: 24406432. Epub 2014/01/11.
82
eng.
83
3.
84
avian influenza A/H9N2 virus in Guangdong in 2016. The Journal of infection. 2017
85
Apr;74(4):422-5. PubMed PMID: 28109675.
86
4.
87
recently-emerging highly pathogenic H7N9 avian influenza virus in China. The
88
Journal of infection. 2017 Apr 06. PubMed PMID: 28390707.
89
5.
M AN U
75
Feng Y, Guan W, Yuan B, Wang Y, Li Z, Song Y, et al. Emergence of
EP
TE D
To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen KY. Emergence in China
AC C
Yuan R, Liang L, Wu J, Kang Y, Song Y, Zou L, et al. Human infection with an
Zhang F, Bi Y, Wang J, Wong G, Shi W, Hu F, et al. Human infections with
Zhao F, Tian J, Lin T, Shao J, Zhang Y, Chen Y, et al. Features of human-infecting 4
ACCEPTED MANUSCRIPT 90
avian influenza viruses and mammalian adaptations. Journal of Infection.
91
2016;73(1):95-7.
92
6.
93
quail, and pigeons to an H7N9 human influenza virus and subsequent egg-passaged
94
strains.
95
WOS:000392383900011. English.
96
7.
97
live poultry markets on poultry-to-person transmission of avian influenza A H7N9
98
virus: an ecological study. Lancet (London, England). 2014 Feb 08;383(9916):541-8.
99
PubMed PMID: 24183056. Pubmed Central PMCID: 3946250.
Archives
of
virology.
2017
RI PT
Uchida Y, Kanehira K, Takemae N, Hikono H, Saito T. Susceptibility of chickens,
Jan;162(1):103-16.
PubMed
PMID:
M AN U
SC
Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, et al. Effect of closure of
100
8.
101
of avian influenza A (H7N9) in China. Scientific reports. 2013 Sep 26;3:2722.
102
PubMed PMID: 24072008. Pubmed Central PMCID: 3784030.
103
9.
104
Human Infections with Avian Influenza H7N9 and H5N1 virus in China. Scientific
105
reports. 2015 Dec 22;5:18610. PubMed PMID: 26691585. Pubmed Central PMCID:
106
4686887.
107
10. Yuan J, Lau EHY, Li KB, Leung YHC, Yang ZC, Xie CJ, et al. Effect of Live
108
Poultry Market Closure on Avian Influenza A(H7N9) Virus Activity in Guangzhou,
109
China, 2014. Emerging infectious diseases. 2015 Oct;21(10):1784-93. PubMed PMID:
110
WOS:000362158000012. English.
TE D
Fang LQ, Li XL, Liu K, Li YJ, Yao HW, Liang S, et al. Mapping spread and risk
AC C
EP
Li XL, Yang Y, Sun Y, Chen WJ, Sun RX, Liu K, et al. Risk Distribution of
111 5
ACCEPTED MANUSCRIPT Figure and table legends
113
Figure 1. (A) Geographic distribution of human infection with avian influenza A virus
114
in mainland China. These data collected from National Health and Family Planning
115
Commission of the People’s Republic of China (http://www.nhfpc.gov.cn/) and World
116
Health Organization (http://www.who.int/influenza/en/)(accessed on April 27, 2017).
117
(B) Density of poultry and population and the climate characteristics in mainland
118
China. These data come from National Bureau of Statistics of the People’s Republic
119
of China (http://www.stats.gov.cn/), the Ministry of Agriculture of China
120
(http://english.agri.gov.cn/)
121
(http://www.cma.gov.cn/).
122
China
Meteorological
Administration
TE D
123
and
M AN U
SC
RI PT
112
Supplementary Table S1. Comparison of high and Low Pathogenicity Avian Influenza
125
Viruses Case-Patients in mainland China from 2005 to 2017a
126
EP
124
127
a
128
People’s Republic of China (http://www.nhfpc.gov.cn/) and World Health
129
Organization (http://www.who.int/influenza/en/)(accessed on April 27, 2017).
AC C
130
These data come from National Health and Family Planning Commission of the
131
6
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
S0163-4453(17)30136-6
DOI:
10.1016/j.jinf.2017.05.002
Reference:
YJINF 3921
To appear in:
Journal of Infection
Received Date: 3 May 2017 Accepted Date: 4 May 2017
Please cite this article as: Xiang B, Zhu W, You R, Chen L, Li Y, Liang J, Lin Q, Liao M, Xiao C, Ren T, Human infections with Avian Influenza Viruses in mainland China: a big risk in southeastern China, Journal of Infection (2017), doi: 10.1016/j.jinf.2017.05.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1
Human infections with Avian Influenza Viruses in mainland China: a big risk in
2
southeastern China
3
Bin Xiang1,2,3,4, Wenxian Zhu1,2,3,4, Renrong You1,2,3,4, Libin Chen1,2,3,4, Yaling Li5,
5
Jianpeng Liang1,2,3,4, Qiuyan Lin1,2,3,4, Ming Liao1,2,3,4, Chencheng Xiao5,*, Tao
6
Ren1,2,3,4, *
RI PT
4
SC
7 8 1
College of Veterinary Medicine, South China Agricultural University, China
10
2
National and Regional Joint Engineering Laboratory for Medicament of Zoonosis
11
Prevention and Control, China
12
3
Key Laboratory of Animal Vaccine Development, Ministry of Agriculture, China
13
4
Key Laboratory of Zoonosis Prevention and Control of Guangdong
14
Province, China
15
5
TE D
M AN U
9
EP
College of Animal Science and Technology, Shihezi University, Shihezi, China
16
Address for Correspondence:
18
Chencheng Xiao, College of Animal Science and Technology, Shihezi University,
19
Shihezi, China, 832000; Telephone:
20
Email: [email protected]
21
Tao Ren, College of Veterinary Medicine, South China Agricultural University,
22
Guangzhou
23
86-20-85280234, E-mail: [email protected]
AC C
17
510642,
China.
86-188-99591678, Fax:
Telephone:
1
86-0993-2058775,
86-20-85283054
(office),
Fax:
ACCEPTED MANUSCRIPT 24
Dear editor: As reported recently, human infections with different subtypes of avian influenza
26
viruses (AIVs) including H5N1, H5N6, H7N9, H10N8 and H9N2 have been
27
identified in mainland China from 2005 to 2017.1-4 Since the first H5N1 human case
28
was confirmed in Hunan province in December 2005, a total of 46 human cases were
29
reported in mainland China, of which 29 cases were fatal; while human infections
30
with H5N6 virus was firstly documented in Sichuan province on March 3, 2014, 11 of
31
16 patients have been fatal (Table S1). In March 2013, human infections with the
32
novel H7N9 virus were confirmed in Shanghai and Anhui province, 1394 infections
33
and 539 deaths were reported by April 27, 2017. In addition, three H10N8 (two deaths)
34
human cases in Jiangxi province from 2013 to 2014, and two H9N2 human cases
35
without fatality (one in Hunan province in 2014 and one in Guangdong province in
36
2016) were confirmed. Epidemiology analysis displayed that the case fatality rate
37
(CFR) is much higher for high pathogenicity avian influenza (HPAI)—64.52% (40/62)
38
than low pathogenicity avian influenza (LPAI)—38.53% (539/1399), and men are
39
more susceptible to LPAIVs—68.76% (962/1399). Moreover, the age median of
40
H5N1 and H5N6 human case were 27.0- and 29.0-year-old, respectively, while these
41
were 57.9- and 67.7-year-old for H7N9 and H10N8 cases, respectively (Table S1).
42
Notably, the number of H7N9 infections far exceeds human infections caused by
43
other AIVs. Zhao and colleagues have demonstrated that more specific mutations in
44
H7N9 virus (S138A, G186V, T221P, Q226L in HA protein, and Q591K, E627K,
45
D701N in PB2 protein) were observed, associated with its infectivity and
AC C
EP
TE D
M AN U
SC
RI PT
25
2
ACCEPTED MANUSCRIPT transmissibility in mammals or human, when compared to H5N1, H5N6, H9N2 and
47
H10N8.5 On the other hand, LPAIV H7N9 could trigger no illness in poultries, which
48
might increase possibility of close contact with virus contaminated poultries.6 Thus,
49
human is more susceptible to LPAIVs with a lower mortality, when compared to the
50
HPAIVs.
RI PT
46
As shown in Figure 1 A, most of AIV human cases were concentrated in
52
southeastern China. Southeastern China hosts high poultry density and population
53
density with a subtropical monsoon climate (Figure 1 B). Previous study have
54
revealed that exposure to live poultry was a main risk for human infection with AIV.7
55
The largest poultry industry of southeastern China, especially domestic waterfowl
56
industry (three out of five of the world’s population of domestic ducks are raised in
57
these regions), and high population density that associated with a huge consumption
58
of poultry products, increased the chance for human exposure to live poultry.
59
Moreover, previous research has also showed that high humidity and an atmospheric
60
temperature around 15
61
(H7N9), generally consistent with the characteristics of subtropical monsoon climate.8
62
However, human infections with H5N1 virus are most closely linked to the coverage
63
of forest and water body.9 We could observe abundant forest and water resource in
64
southeastern China due to geographical and climatic conditions. Thus, southeastern
65
China has a high risk for human infections with AIV.
TE D
M AN U
SC
51
AC C
EP
were important factors for the risk of avian influenza A
66
To control the current H7N9 epidemic, many effective measures have been
67
implemented, such as temporarily closing live poultry markets and encouraging 3
ACCEPTED MANUSCRIPT 68
chilled instead of live poultry for sale.
69
rural areas should be strengthened and the development of vaccine targeted prevalent
70
LPAIVs should be promoted. Furthermore, to decrease future HPAI and LPAI
71
mortality in human, promoting the development of early and rapid detection and
72
antiviral drug is necessary.
However, surveillance and biosecurity in
RI PT
10
73
SC
74
Reference
76
1.
77
triple-subtype reassortants of fatal human H5N6 avian influenza virus in Yunnan,
78
China. The Journal of infection. 2016 Jun;72(6):753-6. PubMed PMID: 26994688.
79
2.
80
of human disease due to avian influenza A(H10N8)--cause for concern? The Journal
81
of infection. 2014 Mar;68(3):205-15. PubMed PMID: 24406432. Epub 2014/01/11.
82
eng.
83
3.
84
avian influenza A/H9N2 virus in Guangdong in 2016. The Journal of infection. 2017
85
Apr;74(4):422-5. PubMed PMID: 28109675.
86
4.
87
recently-emerging highly pathogenic H7N9 avian influenza virus in China. The
88
Journal of infection. 2017 Apr 06. PubMed PMID: 28390707.
89
5.
M AN U
75
Feng Y, Guan W, Yuan B, Wang Y, Li Z, Song Y, et al. Emergence of
EP
TE D
To KK, Tsang AK, Chan JF, Cheng VC, Chen H, Yuen KY. Emergence in China
AC C
Yuan R, Liang L, Wu J, Kang Y, Song Y, Zou L, et al. Human infection with an
Zhang F, Bi Y, Wang J, Wong G, Shi W, Hu F, et al. Human infections with
Zhao F, Tian J, Lin T, Shao J, Zhang Y, Chen Y, et al. Features of human-infecting 4
ACCEPTED MANUSCRIPT 90
avian influenza viruses and mammalian adaptations. Journal of Infection.
91
2016;73(1):95-7.
92
6.
93
quail, and pigeons to an H7N9 human influenza virus and subsequent egg-passaged
94
strains.
95
WOS:000392383900011. English.
96
7.
97
live poultry markets on poultry-to-person transmission of avian influenza A H7N9
98
virus: an ecological study. Lancet (London, England). 2014 Feb 08;383(9916):541-8.
99
PubMed PMID: 24183056. Pubmed Central PMCID: 3946250.
Archives
of
virology.
2017
RI PT
Uchida Y, Kanehira K, Takemae N, Hikono H, Saito T. Susceptibility of chickens,
Jan;162(1):103-16.
PubMed
PMID:
M AN U
SC
Yu H, Wu JT, Cowling BJ, Liao Q, Fang VJ, Zhou S, et al. Effect of closure of
100
8.
101
of avian influenza A (H7N9) in China. Scientific reports. 2013 Sep 26;3:2722.
102
PubMed PMID: 24072008. Pubmed Central PMCID: 3784030.
103
9.
104
Human Infections with Avian Influenza H7N9 and H5N1 virus in China. Scientific
105
reports. 2015 Dec 22;5:18610. PubMed PMID: 26691585. Pubmed Central PMCID:
106
4686887.
107
10. Yuan J, Lau EHY, Li KB, Leung YHC, Yang ZC, Xie CJ, et al. Effect of Live
108
Poultry Market Closure on Avian Influenza A(H7N9) Virus Activity in Guangzhou,
109
China, 2014. Emerging infectious diseases. 2015 Oct;21(10):1784-93. PubMed PMID:
110
WOS:000362158000012. English.
TE D
Fang LQ, Li XL, Liu K, Li YJ, Yao HW, Liang S, et al. Mapping spread and risk
AC C
EP
Li XL, Yang Y, Sun Y, Chen WJ, Sun RX, Liu K, et al. Risk Distribution of
111 5
ACCEPTED MANUSCRIPT Figure and table legends
113
Figure 1. (A) Geographic distribution of human infection with avian influenza A virus
114
in mainland China. These data collected from National Health and Family Planning
115
Commission of the People’s Republic of China (http://www.nhfpc.gov.cn/) and World
116
Health Organization (http://www.who.int/influenza/en/)(accessed on April 27, 2017).
117
(B) Density of poultry and population and the climate characteristics in mainland
118
China. These data come from National Bureau of Statistics of the People’s Republic
119
of China (http://www.stats.gov.cn/), the Ministry of Agriculture of China
120
(http://english.agri.gov.cn/)
121
(http://www.cma.gov.cn/).
122
China
Meteorological
Administration
TE D
123
and
M AN U
SC
RI PT
112
Supplementary Table S1. Comparison of high and Low Pathogenicity Avian Influenza
125
Viruses Case-Patients in mainland China from 2005 to 2017a
126
EP
124
127
a
128
People’s Republic of China (http://www.nhfpc.gov.cn/) and World Health
129
Organization (http://www.who.int/influenza/en/)(accessed on April 27, 2017).
AC C
130
These data come from National Health and Family Planning Commission of the
131
6
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT