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VOL 30 — NOVEMBER 2014 [email protected] | WWW.FAO.ORG/AG/EMPRES.HTML Avian A(H5N6): the latest addition to emerging zoonotic threatsats in East and Southeast

FAO Contributors: Guillaume Belot, Filip Claes, Sophie Von Dobschuetz, Akiko Kamata, Scott Newman, Chintana Chanthavisouk, Phouvong Phommachanh, Kachen Wongsathapornchai, Guo Fusheng, John Edwards, Wantanee Kalpravidh, Subhash Morzaria, Eran Raizman, Juan Lubroth.

Hong Kong Special Administrative Region Since early 2013 several new avian Contents (SAR), including six fatalities [WHO]. influenza strains have been reported in A program of massive culling of in the East and Southeast Asia, threatening both Context of new emerging autonomous region was necessary to put an poultry-dependant livelihoods and human subtypes of Avian Influenza end to the epidemic [De Jong et al, 1998]. A health. In March 2013, avian influenza in eastern Asia 1 few years later the H5N1 HPAI re-emerged A(H7N9) emerged in causing a total in Asia on a much larger scale. Two human of 456 human cases, and claiming 172 lives Emergence of H5N6 1 cases were first reported in SAR as of 05 November 2014. The virus is of low in February 2003 [Peiris et al, 2004], before pathogenicity in poultry (no clinical signs are H5N6 in 2 the Republic of Korea reported several poultry observed in infected ) but can cause outbreaks in December 2003. Between late lethal pulmonary infection in mammals without Genetic characteristics 2003 and early 2004 H5N1 HPAI expanded prior trans-species adaptation [Can et al, of H5N6 viruses 2 rapidly throughout East and Southeast Asia, 2014]. Subsequently, H10N8 was reported in with more than 1,300 outbreaks in , December 2013, causing three human cases Phylogenetic analysis China, Lao People’s Democratic Republic, in China, including two fatalities, while H5N8 of H5N6, H5N8 and H5N1 the Republic of Korea, and Viet Nam emerged the month after and was the cause viruses 3 reported in January 2004 alone [EMPRES-i]. of at least 40 poultry outbreaks, mainly in the By mid-2006, the virus had spread to , Republic of Korea but also in and China Perspectives and and , affecting over 60 [OIE; EMPRES-i]. This was followed by the recommendations 4 countries and territories. Most countries first reports from China and Lao People’s succeeded in eliminating the from Democratic Republic in early May 2014, Acknowledgements 4 the poultry sector with few endemic hot spots describing outbreaks in poultry caused by a remaining in the Indo-Gangetic Plain and the highly pathogenic H5N6. More recently, the References 5 Greater Mekong subregions, China, , finding of a H5N3 subtype was reported for and [EMPRES-i]. The nature of the the first time on 24 October 2014 from a live poultry production systems including poor market in Changsha, Hunan, China [OIE]. biosecurity and inadequate veterinary services Concerns grow as the rate of emergence Context of new confounded efforts to control the disease of new sub-types increases, creating new effectively, and it is unlikely that the disease potential threats and a need for continuous emerging subtypes of will be eliminated in these countries in the vigilance and monitoring (Table 1 and Figure 1). Avian Influenza viruses foreseeable future without major changes in in eastern Asia production and marketing practices to improve hygiene, inspection and compliance. Emergence of H5N6 he first reported appearance of a A diverse viral pool now exists in global zoonotic influenza of avian eastern Asia due to co-circulation of many Low pathogenic viruses belonging to the T origin dates from 1996, when an different avian influenza (AI) viruses. Following H5N6 subtype have already occurred in outbreak of H5N1 highly pathogenic avian genetic events between the past. Found mainly in but also in influenza (HPAI) occurred on a viruses or of viral , novel virus environmental samples, H5N6 viruses had in Province, China [Guan et strains continue to emerge in the region with already been detected in various areas of Smith, 2013]. One year later, the H5N1 unpredictable consequences for animal and the world, including Wisconsin, the United HPAI virus was recognised as a zoonotic human health. Recently, the detection of such States of America in 1975 [GenBank acc. agent with 18 human cases identified in new reassortants has become more frequent. U79451], in 1984 [GenBank], VOL 30 — NOVEMBER 2014 | empres watch

Table 1: New avian influenza virus types and sub-types detected in East and Southeast Asia since early 2013 (as of 05 November 2014).

Type and Sub-type Location Human cases Clinical signs in poultry Poultry outbreaks First report

H7N9 China 455 No * March 2013

H10N8 China 3 ? ? December 2013

H5N8 China, Korea, Japan 0 Yes 42 January 2014

H5N6 China, Lao PDR, Viet Nam 1 Yes 34 May 2014

H5N3 China 0 Yes 1 October 2014 *In the absence of clinical signs in poultry the term outbreak cannot be used. However the virus has been found in 132 out of over 600,000 samples collected by the Chinese Ministry of Agriculture from poultry or the environment and 63 environmental samples collected during trace-back surveillance of human cases in China between April 2013 and September 2014. Remarkably, peer-reviewed publications reported 326 positive virological samples out of 22,197 [1, 2, 3, 4, 5, 6, 7, 8].

This suggests that H5N6 is already fairly Figure 1. Overview of avian influenza virus strains circulating in East and widespread in eastern Asia (Figure 1). Southeast Asia that emerged since 2013 Data: EMPRES-i* According to official information, for each outbreak, contingency measures such as stamping out, movement control, and disinfection of infected premises were implemented [OIE, 2014].

H5N6 in Humans

Only one human H5N6 infection has been detected to date. This case, a 49-year-old male farmer from Sichuan Province, China, associated to the first poultry outbreak, was reported on 6 May 2014 and died from severe a few days after hospitalization. Close contacts of the patient were placed under medical observation without additional human cases detected [HFPC Sichuan, 2014]. Given the current evidence, and the fact that despite the virus being detected in poultry across a fairly widespread geographical area in eastern Asia, only one human case was reported, WHO considers that H5N6 is not likely to be easily * Data in EMPRES-i is derived from numerous sources: FAO representatives or country missions, FAO reports, World Organisation for Animal Health (OIE), official government sources, the European Commission (EC), transmissible from birds to humans. peer-reviewed publications, FAO reference centres, laboratories and FAO collaborators. Genetic characteristics

Sweden in 2002 [GenBank acc. AY995892], present in China several months prior to of H5N6 viruses and California, the United States of America notification, though no outbreak was officially Analysis of the eight genome segments in 2013 [GenBank acc. CY177425]. These reported [OIE]; the virus had been isolated of H5N6 viruses from Viet Nam and Lao outbreaks however had little to no impact on from an environmental sample collected on People’s Democratic Republic indicated the poultry industry and no implications for 20 December 2013 in a live poultry market in that these viruses are genetically similar. public health. Zhenjiang, Jiangsu Province [Qi et al, 2014] The hemagglutinin (HA) gene belongs to Unlike its predecessors, the recently and from a duck in Guangdong Province in a specific H5 clade 2.3.4.4 group1. The emerged Asian H5N6 is a highly March 2014 [GenBank acc. KJ754145]. recently isolated H5N1 HPAI viruses from pathogenic AI virus, which causes severe Shortly after, Lao People’s Democratic live bird markets in Viet Nam and the H5N8 clinical signs in poultry and associated Republic and Viet Nam both reported two and viruses detected in Republic of Korea and mortality. The first poultry outbreak caused seven H5N6 poultry outbreaks, respectively, Japan also belong to this genetic group2. The by H5N6 was reported in Nanchong City, with initial outbreak observation in March neuraminidase (NA) gene is closely related to Sichuan Province, China, on 4 May 2014 2014 in Lao People’s Democratic Republic 1 While the HA genes from viruses in this emerging [OIE], after confirmation by both reverse and in April 2014 in Viet Nam (Table 2). virus group meet the criteria for novel clade designation, transcription polymerase chain reaction On 24 October 2014, China notified OIE a formal nomenclature has not yet been adopted. (RT-PCR) and virus isolation at the Harbin of another 24 positive findings in poultry or 2.3.4.4 is used as a provisional nomenclature only. 2 Veterinary Research Institute (OIE/FAO the environment, reported in 12 different It will be interesting to ascertain if the H5 from the H5N3 that was recently detected in a Chinese live bird Reference Centre). Genetic sequences provinces from Heilongjiang in the northeast market also belongs to the same clade. At the time of demonstrate that the virus was already of China down to Tibet in the southwest. writing its genetic information was not available. 2 empres watch | VOL 30 — NOVENBER 2014

Table 2. Reports of poultry outbreaks caused by H5N6 HPAI in East and Southeast Asia, sorted by sample collection date as reported to the OIE (as of 05 November 2014) [OIE, 2014].

Collection Reporting Location Species Unit Susceptible Cases Deaths Date Date

13/03/14 05/05/14 Xayabury LAO PDR , Duck Village 5 142 457 457

22/04/14 12/08/14 Lang Son VIET NAM Chicken Village 80 40 15

23/04/14 04/05/14 Sichuan CHINA Chicken Farm 1 338 1 0

25/06/14 12/08/14 Ha Tinh VIET NAM Duck Village 1900 950 0

14/07/14 15/09/14 Luangprabang, LAO PDR Chicken, Duck Farm 200 2 2

11/08/14 22/08/14 Lao Cai VIET NAM Pheasant Village 558 498 498

15/08/14 04/09/14 Quang Tri VIET NAM Duck Village 1 550 350 350

23/08/14 01/09/14 Heilongjiang CHINA Goose Farm 86 674 20 550 17 790

23/08/14 04/09/14 Quang Ngai VIET NAM Duck Village 1100 200 200

12/09/14 24/10/14 24 outbreaks in 12 Duck, Chicken, provinces in China Environment

13/09/14 20/09/14 Quang Ngai VIET NAM Duck Backyard 1 000 1 000 300

14/09/14 20/09/14 Quang Nam VIET NAM Duck Backyard 2 000 2 000 600

that of a group of H6N6 viruses circulating in domestic in Southern China. Internal Figure 2. Hypothetical source of origin of the H5N6 triple reassortant based on closest relationship to known ancestral viruses in GenBank genes show a high similarity to those of the H5 virus clade 2.3.2.1.B H5N1 virus A/ A/goose/Eastern China/1112/2011 (H5N2) — like wild duck//1//2011. Thus H5N6 is A/duck/Fujian/3059/2007 likely to be a triple-reassortant virus (Figure PB2 (H6N6) — like PB1 A/wild duck/Fujian/1/2011 1). Genetic features of the novel A(H5N6) PA PB2 (H5N1) — like (2.3.2.1) HA PB1 viruses isolated thus far from the human case PB2 NP PA or poultry outbreaks can be summarized as PB1 NA HA PA follows: MA NP HA NS NA t High pathogenicity for poultry: Novel MA NP A(H5N6) viruses have the polybasic HA NS NA MA cleavage sequence, PLRERRRKR/GLF NS common to clade 2.3.4 HPAI viruses. This indicates that they are highly pathogenic PB2 avian influenza viruses, capable of causing PB1 PA high mortalities in poultry. HA H5N6 t Preference for avian-like receptor binding: NP Sichuan 2014 2014 The amino acid characteristics of the NA MA hemagluttinin of these novel H5N6 viruses NS show a predicted preference for avian- like Į2,3-linked sialic acid receptors. This means that H5N6 has currently more avian than mammalian-like receptor affinity, linked to mammalian host adaptation was (Figure 3). A first group consists of the contrary to the recently emerged H7N9 not present in the A(H5N6) viruses isolated emerging H5N8 viruses isolated in 2013- LPAI in China. However these viruses do so far. 2014 in China and the Republic of Korea contain a Thr156Ala substitution, which t Sensitivity to (Tamiflu®): No (pink squares). These viruses show a close disrupts N-glycosylation at position 154, known N1 and N2 genetic relationship to some older H5N1/ potentially leading to enhanced receptor- resistance markers present in known H5N2 HPAI viruses isolated in ducks and binding affinity to mammalian receptors A(H5N6) viruses, thus indicating that there wild birds in China in 2010-2011. A second [Herfst et al, 2012]. these viruses are sensitive to osteltamavir genetic cluster contains the newly isolated t Adaptation to terrestrial poultry: The NA [Boltz et al, 2010]. H5N1 HPAI from live bird markets in Viet Nam gene from H5N6 contains an 11-amino (black triangles), H5N8 viruses isolated in the acid deletion in the NA stalk region Republic of Korea and Japan, and the H5N6 (positions 59–69; N6 numbering) as Phylogenetic analysis viruses isolated in Lao People’s Democratic previously found in A(H6N6) viruses of H5N6, H5N8 and H5N1 Republic and in Guangdong Province, China isolated from domestic ducks in (green circles). The third group in this 2.3.4.4 Guangdong Province in China [Herfst et al, viruses clade is formed of Vietnamese and Chinese 2012]. When analyzing the HA gene of the emerging H5N6 viruses (red circles). It shows that all t No evidence of mammalian host clade 2.3.4.4 viruses (H5N1, H5N6, and five Vietnamese cases are closely related to adaptation: The PB2 E627K mutation H5N8), three distinct groups are found each other, and are also closely related to 3 VOL 30 — NOVEMBER 2014 | empres watch

Figure 3. Genetic similarity of H5 clade 2.3.4.4 viruses in East and Southeast Asia

Emergence and spread of HPAI H5N6, H5N8 and H5N1 with HA gene clade 2.3.4.4 in Asia 2013-2014 2013-11-18 | A/mallard duck/Shanghai/SH-9/2013 H5N8 HPAI 2013-11-14 | A/duck/Zhejiang/W24/2013 H5N8 HPAI 2014-01-16 | A/breeder duck/Korea/Gochang1/2014 H5N8 HPAI 2013-12-14 | A/duck/Zhejiang/6D18/2013 H5N8 HPAI 2010-12-05 | A/duck/Jiangsu/k1203/2010 H5N8 HPAI 2011-01 | A/goose/Eastern China/1112/2011 H5N2 HPAI 2012-01-18 | A/duck/Jiangsu/m234/2012 H5N2 HPAI 2011 A/wild duck/Shandong/628/2011(H5N1) 2011-12-07 | A/duck/Hebei/3/2011 H5N2 HPAI 2011-12-01 | A/duck/Hebei/2/2011 H5N2 HPAI 2011-01 | A/duck/Eastern China/1111/2011 H5N2 HPAI 2012 A/chicken/China/AH/2012(H5N1) 2014-04-15 A/muscovy duck/Vietnam/LBM636/2014(H5N1) 2014-04-15 A/duck/Vietnam/LBM638/2014(H5N1) 2014-03 | A/duck/Guangdong/GD01/2014 H5N6 HPAI 2013-12-02 | A/environment/Shenzhen/25-24/2013 H5N6 HPAI LA14(03) A/chicken//NAHLLPQ001(14-01188-01)/2014 2014-01-10 | A/duck/Jiangxi/95/2014 H5N6 HPAI 2014-04-13 | A/Chicken/Kumamoto/1-7/2014 H5N8 HPAI 2.3.4 .4 (proposed) 2014 A/waterfowl/Korea/S005/2014(H5N8) 2014-01-17 | A/broiler duck/Korea/Buan2/2014 H5N8 HPAI 2014-01-17 | A/baikal teal/Korea/Donglim3/2014 H5N8 HPAI VN14(08/22) A/duck/VN/QuangTri(GioLinh)/R3(14A392)/2014 H5N6 HPAI VN14(08/14) A/pheasant/VN/LaoCai(BaoThang)/NCVD140771(14A367)/2014 H5N6 Sichuan - like VN14(08/23) A/duck/VN/QuangNgai(SonTinh)/R4(14A421)/2014 H5N6 2013 A/environment/Zhenjiang/C13/2013(H5N6) H5N6 Laos - like VN14(04) A/chicken/VN/LangSon(TrangDinh)/NCVD(14A324)/2014 H5N6 CN14(04) A/Sichuan/26221/2014 H5N6 Human case H5N6 Sequence not available yet VN14(06) A/duck/VN/HaTinh(KyAnh)/R3(14A338)/2014 H5N6 HPAI A/chicken/Sichuan/J1/2014(H5N6) HPAI H5N8 Korea /Gochang - like A/chicken/Ningxia/S6/2014(H5N6) HPAI H5N8 Japan/Kumamoto - like 2008-06-06 | A/duck/Guangdong/wy19/2008 H5N5 HPAI 2008 A/duck/Guangdong/wy11/2008(H5N5) H5N1 Vietnam (new 04/2014) 0.005

H5N6 virus (A/Sichuan/2622/2014) detected to other countries or continents. Migratory N1 negative samples are tested for N6 by in a human case in April 2014 in Sichuan birds, which have played a key role in the applying validated protocols or sending Province, China as well as from isolates introduction of H5N1 to Europe and Africa samples to international reference laboratories from from Sichuan and NingXia [Kilpatrick et al, 2006] and of H5N8 to the for further characterization. Provinces. The phylogenetic tree shows that Republic of Korea [Jeong et al, 2014], could To reduce the risk of spread and the Vietnamese/Chinese H5N6 virus group spread the viruses to other countries or transmission, FAO recommends authorities to is slightly different from H5N6 virus detected continents. Research is required to better increase hygiene and biosecurity in live bird in March 2014 in Lao People’s Democratic understand the role migratory birds play in markets, to enhance market surveillance and Republic and from a duck virus isolated in the epidemiology of these novel viruses and to strengthen traceability to allow efficient Guangdong Province, China, thus indicating related risks. and timely traceback of any positive infection an already existing genetic diversity within this FAO is coordinating the evaluation of AI to its farm of origin. Poultry batches from newly emerging virus clade. poultry vaccines currently in use in Viet Nam. affected areas should always be tested prior Preliminary results are encouraging as two to importation. The diverse viral gene pool out of the three vaccines tested showed in eastern Asia, established through co- Perspectives and a drastic reduction of disease in chickens circulation of many different avian influenza [FAO unpublished data]. One of FAO’s viruses, will continue to give rise to novel recommendations Reference Centres, the Australian Animal reassortant viruses, such as H5N6, with The epidemiological and genetic analysis Health Laboratory (AAHL) in Geelong, has unpredictable consequences for animal and described above show that the virus is still established that current avian influenza tests human health. Continuous vigilance and more adapted to avian-type than human-type can detect H5N6 effectively. In addition, new, monitoring therefore remain needed, along respiratory receptors. However, with winter more specific tests are under development. with increased preparedness, especially as season approaching in eastern Asia, the Diagnostic protocols, soon available on the the next influenza season is approaching. prevalence of the virus in poultry is expected OIE/FAO Network of Expertise on Animal to rise, increasing both chances for human Influenza website [OFFLU], are also under exposure and opportunities for mutation or review to enhance diagnostic preparedness in Acknowledgements reassortment, especially considering the the region. location of circulation of this virus: in endemic With its own funding and that of a grant The authors wish to express their gratitude to regions with H5N1, H9N2 and H7N9 for received from United States Agency for the Ministry of Agriculture and Forestry in Lao China. The latter could change the viruses’ International Development, FAO is also People’s Democratic Republic, the Ministry transmissibility to humans. H5N6 therefore assisting countries in implementing AI of Agriculture and Rural Development in Viet remains a public health threat, which requires surveillance to enable early detection of Nam, the Ministry of Health and the Ministry of close monitoring in the same way as for incursion or spread of H7N9, H5N6 and Agriculture in China, as well as to the Chinese H5N1 HPAI and H7N9. other avian influenza viruses. Countries with Center for Disease Control and Prevention The possibility exists that wild birds could ongoing H5N1 HPAI surveillance are strongly (CDC) and the Australian Animal Health become infected and spread these viruses recommended to ensure that all H5 positive, Laboratory. 4 empres watch | VOL 30 — NOVEMBER 2014 References

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5 CONTACT

The Emergency Prevention System (EMPRES) is an FAO programme, founded in 1994, with the goal of enhancing world food security, fighting transboundary animal and plant pests and and reducing the adverse impact of food safety threats. EMPRES-Animal Health is the component dealing with the prevention and control of transboundary animal diseases (TADs). Recommended citation To subscribe or to ask for information about EMPRES-Animal Health send an e-mail to: FAO. 2014 Avian influenza A(H5N6): the [email protected] or a fax to (+39) 06 57053023 latest addition to emerging zoonotic avian influenza threats in East and Southeast Asia. For more information visit us at http://www.fao.org/ag/empres.html EMPRES WATCH, Vol. 30, November 2014. Rome. EMPRES-Animal Health can assist countries in the shipment of samples for TAD diagnostic testing at a FAO reference laboratory and reference centre. Please contact Empres-Shipping-Service@fao. org for information prior to sampling or shipment. Please note that sending samples out of a country Photo cover: ©FAO/Eran Raizman requires an export permit from the Chief Veterinarian’s Office of the country and an import permit from Photo back cover: ©FAO/Ken Inui the receiving country.

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