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Antigua, K.J. Evolution of H5Nx Subtypes. Encyclopedia. Available online: https://encyclopedia.pub/entry/18849 (accessed on 22 December 2025).
Antigua KJ. Evolution of H5Nx Subtypes. Encyclopedia. Available at: https://encyclopedia.pub/entry/18849. Accessed December 22, 2025.
Antigua, Khristine Joy. "Evolution of H5Nx Subtypes" Encyclopedia, https://encyclopedia.pub/entry/18849 (accessed December 22, 2025).
Antigua, K.J. (2022, January 26). Evolution of H5Nx Subtypes. In Encyclopedia. https://encyclopedia.pub/entry/18849
Antigua, Khristine Joy. "Evolution of H5Nx Subtypes." Encyclopedia. Web. 26 January, 2022.
Evolution of H5Nx Subtypes
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms7060156

With the extensive divergence of the H5 hemagglutinin (HA) sequences of documented viruses, the WHO/FAO/OIE H5 Evolutionary Working Group clustered these viruses into a systematic and unified nomenclature of clade 2.3.4.4 currently known as “H5Nx” viruses. The rapid emergence and circulation of these viruses, namely, H5N2, H5N3, H5N5, H5N6, H5N8, and the regenerated H5N1, are of great concern based on their pandemic potential. 

evolution epidemiology avian H5Nx Influenza

1. H5N5

Domestic ducks, among poultry, are highly regarded as the reassortant vessel for most avian influenza viruses [1][2]. Furthermore, the extensive prevalence of live poultry markets in China enhances the reassortment activities of influenza subtypes [3][4][5]. The combination of these two factors has contributed significantly to the formation of the first H5Nx virus [6][1][7][2]. It was in the latter part of 2008 when the first H5N5 virus was isolated in China (Figure 1) [1][2].
Microorganisms 07 00156 g001 550
Figure 1. H5Nx timeline of evolution and continuous emergence (2008–2018).
Specifically, the first reassortant subtype was isolated from apparently healthy mallard ducks (Anas platyrhynchos) in a live poultry market surveillance program [6][1][7][2][8][9]. Two isolates, A/duck/eastern/China/008/2008 and A/duck/eastern/China/031/2009 were detected in live poultry markets in eastern China [6]. Furthermore, three more H5N5 isolates were isolated from ducks during the same period of live poultry market surveillance in Guangdong during the same year [6][1]. In 2010, another case was isolated from ducks in Central China [7].
H5N5 are multiple reassortants of possible parent viruses: H5N1 A/duck/Eastern-China/108/2008, H5N1 A/duck/Eastern-China/909/2009, and H6N5 A/duck/Yangzhou/013/2008. Gu et al. (2011) further speculated that H5N5 viruses are contemporary reassortants of Eurasian subtype H5N1, some unidentified subtype, and/or the H6N5 avian influenza virus [2]. Conversely, Zou et al. (2012) theorized that H5N5 is a result of multiple reassortments of the H10N5 and H5N1 viruses, which have been circulating in China since 1983 and 1997, respectively, and with another circulating AIV in China [7].
Although the H5N5 subtype was the first H5Nx reported, there are only a few documented records of H5N5 viruses of the 2.3.4.4 clade. Furthermore, no records of human infection nor massive poultry outbreak have been reported [6]. Moreover, this subtype, from the time of its detection, was rarely isolated [7]. According to the Animal and Plant Health Agency (APHA)-UK, during 2016–2017, H5N5 re-emerged because H5N8, which had been predominantly circulating worldwide, lost its N8 during its reassortment activities with LPAI viruses from circulating wild birds and this led to the incorporation of the N5 gene [10][11]. Based on the records of the Food and Agriculture Organization (FAO)’s Empress-I, aside from its detection in China, H5N5 has only 18 other noted occurrences in 11 European countries, namely, France, Italy, Montenegro, Croatia, Poland, Czech Republic, Greece, Germany, Serbia, Slovenia, and the Netherlands, between 2016 and 2017 [12].

2. H5N8

With the massive avian influenza surveillance and sample collection among domestic live poultry markets and farms in China, the novel subtype H5N8 (A/duck/Jiangsu/k1203/2010), along with the three H5N5 subtypes, was first detected in eastern China in 2010 (Figure 1) [1].
Zhou et al. (2013) have also revealed that the five H5N8 internal genes (PB1, PB2, PA, M, and NS) share high sequence homologies with H5N1 isolated in eastern China from 2005 to 2006 [1]. Nonetheless, as for the NP gene, it was observed to have high sequence similarities with H6N2 viruses isolated from Guangdong Province during 2001–2003. Thus, it suggests that H5 HPAI bearing the N8 gene may have originated in China [13].
Furthermore, Ma et al. (2018) reported that the maximum clade credibility (MCC) trees generated for HA and NA genes of the first H5N8 isolate revealed that the reassortment likely happened in August 2009 [14]. Their study further inferred that reassortment happened between domestic poultry “HPAI H5Ny and HxN8” and circulating wild aquatic birds [14][13]. Known as one of the most prevalently circulating HPAI in China in 2009, H3N8 viruses were mainly identified as the subtype with the highest probability of being the neuraminidase donor [14][1]. Thus, it was theorized that this reassortment which occurred between domestic poultry and wild aquatic birds likely paved the way for the formation of the novel H5N8 [14].
When H5N8 was first detected and isolated, it was from apparently healthy ducks (Annas platyrhynchos) in the province of Jiangsu [15][14][1]. No H5N8 outbreaks were recorded in China during that time, and it was first isolated and reported in 2013. However, an outbreak caused by H5N8 in poultry and wild birds was reported in the Republic of Korea from January 2014 to July 2015. The detected H5N8 in Korea is highly homologous with the same virus isolated during the live poultry market surveillance program in China [14]. Japan also had the same outbreak in April 2014 [10]. Moreover, with the aid of the migratory pathways, in late 2014, H5N8 began spreading explosively in Russia and six other European countries (i.e., Germany, Hungary, Italy, the Netherlands, Sweden, and the United Kingdom) [16][10][17] in early 2015. The spread of HPAIV (H5N1) from Asia to Europe may have been brought about by several factors, such as transport, production, or wild bird migration [18]. Some scientific papers have separated the sublineages of H5N8 and referred to each group as either as 2.3.4.4 “Buan-like” or “Gochang-like” [10][19].
H5N8 Buan-like sublineages, or Group A, are the viruses detected which were established and first detected in Europe and some Asian countries in 2014. Buan-like H5N8 precursor viruses were believed to have been initially detected in eastern China before their intercontinental spread [10][1][19][20]. Although outbreaks did not persist for a long period, this was the first incursion of clade 2.3.4.4 of Gs/GD lineage into Europe [10][21]).
In 2016, the second wave of H5N8 was detected. This group of H5N8 was then called “Gochang-like” viruses [10]. This novel H5N8 reassortant was detected in a wild bird in Qinghai, China in May 2016, before it persisted in intercontinental spread [16][17][22]. Furthermore, Lee et al. reported that this H5N8 HPAI virus group, which had also been detected in the Tyva Republic, Russia, is different from the H5N8 group, which persisted in Europe in 2014 [19]. Moreover, in their study, they showed that this reassortant has three out of eight genes as in the case of the Gochang-like viruses. The reassortant is a product of Eurasian lineage LPAI and HPAI H5N8, containing five Eurasian LPAI segments (PB2, PB1, PA, NP, and M) [16].
Since the re-emergence of the novel reassortant H5N8 in 2016, a wide range of avian species have been reported to be affected by H5N8 HPAI viruses in 49 countries [10][12][23]. Studies revealed that this new novel reassortant was then disseminated to Siberia during migratory fowl migration [24][10][25]. In 2016, H5N8 viruses continued to spread across Europe, Asia, and Africa [17][23]. With the contingencies made in animal health regulations, poultry trade, and country quarantine procedures, the number of outbreaks has gradually declined. However, even with the combined strategies in Asia, H5N8 still persists, especially in China [24][26][27][15][14][28][1][13][5][22][29][30].
Based on data collated from the Empress-I database run by the FAO, there were already almost 3,400 reports globally of HPAI H5N8 infection, alone and/or combined with other HPAI viruses from 2013 to 2018 [12]. Although this subtype has not been reported to cause human infection, the continuous spread of this virus is alarming and should be regarded with precautionary measures. The circulation of this novel subtype from domestic poultry to wild birds has generated novel reassortants which have spread globally [15][14][28][5]. Moreover, Ma et al. (2018) reported that in the process of adaptation, H5N8 amino acids changed gradually during its transmission from one host to another [14]. Recently, the rapid adaptation of the virus in mammalian hosts was observed; the mouse-adapted virus significantly increased virulence in mice, further highlighting potential concerns for public health [31].

3. H5N6

After the emergence of H5N5 viruses in clade 2.3.4.4, their HA gene was observed to be closely associated with the emergence of NA subtypes, with N2, N5, N6, and N8 variants in poultry and wild birds [32]. The revolution of H5Nx viruses began in July 2008 when an H5N5 virus of Guangdong Province (A/duck/Guangdong/wy19/2008) spread and caused an outbreak in the northeastern province of Jiangsu [33][4]. In 2010, it was recognized that Jiangsu Province became a central pool of avian influenza viruses transmitting towards the northern and southern parts of China [33]. The interplay and movement of migratory fowls across China has resulted in the development of the highly pathogenic avian influenza virus H5N6 [3][34][4][32][35].
The Chinese government enforced active surveillance and sample collection activities to secure public health. Hence, during the surveillance, it was found that H5N6 viruses have dominated and spread throughout the country [3]. From the time it was first isolated and detected, this virus has continuously persisted in China and caused fatal human infection [3][34][4][32][35]. To date, HPAI H5N6 is one of the few AIV subtypes reported to cause human infection [36]. Understanding the origins and genesis of each virus subtype can help determine their relationship with other subtypes in the same clade.
Previous studies have revealed that H5N6 emerged from a common H5 progenitor strain of the 2.3.4.4. clade reassorted with the neuraminidase of the Eurasian lineage originating from the H6N6 A/duck/Guangxi/2281/2007 [3][33][36][32] However, Yang et al. (2017) revealed that this novel reassortant emerged from two evolutionary pathways [34]. From 2010 to mid-2012, the HA H5N2 of clade 2.3.4.4 reassorted with the NA of H6N6 (A/duck/Guangxi/2281/2007) and further reassorted with the six internal genes of a chicken host H5N1 of clade 2.3.2.1c [34]. The H5N6 reassortant (“Reassortant A”) resulting from this pathway has been circulating in Xinjiang, Jilin, and northern China [3][33][37]. Moreover, in 2013, H5 viruses of the 2.3.4.4 clade have then spread widely to western parts of China, causing outbreaks in Sichuan Province and neighboring countries such as Vietnam and Laos [24][36].
Beyond 2013, H6N6 viruses bearing deletions at the 59–69 position in the stalk regions of its NA have reassorted with the HA of H5N8 of clade 2.3.4.4 and further reassorted with the H5N1 of 2.3.2.1c (“Reassortant B”) [34]. Likewise, Reassortant B viruses have also been detected in China, Vietnam, and Laos. Two years later, these Reassortant B H5N6 viruses then further reassorted with H9N2, generating the H5N6 “Reassortant C”. Moreover, these newly reassorted H5N6 viruses were reported in Yunnan and Guangdong Provinces [37][34].
Apparently, no matter the evolutionary pathway from which these sequential multiple-step reassortant viruses emerged, all were reported to cause human infection [3][33][34]. Based on the data within the FAO’s Empress-I database, there were 19 confirmed cases of human infections due to HPAI H5N6. Notably, all 19 reports were confirmed positive and distributed only in China [12]. Most of the human cases are attributed to Reassortants A or B. However, the first case of H5N6 human infection in 2014 was due to H5N6 Reassortant A [34][35]. Reassortant C viruses were noted to have lower virulence compared with Reassortants A and B [34].
To date, based on the Empress-I database managed by the FAO, H5N6 cases are confined to Asia and Europe. H5N6 spread across Laos and Vietnam in 2014, causing economic losses due to increased poultry mortalities [12]. By 2016, H5N6 was responsible for a series of outbreaks in Asia, including a poultry outbreak in Japan, Myanmar, and the Republic of Korea. Moreover, the highest number of human cases due to H5N6 was recorded in December 2015 (including 9 out of 16 human fatal cases to date) [33][12]. By 2017, H5N6 had already spread through China’s neighboring countries such as Taiwan and the Philippines. Furthermore, it began spreading to some European countries such as Greece, Germany, the Netherlands, and Switzerland. Primarily, migratory birds have been the key player for the expansion and genetic reassortment of HPAIVs, particularly for H5N6 from Asia to Europe [3][33][34][4][32].

4. H5N2

During the live bird market surveillance of AIVs, the regenerated H5N2 virus was isolated in apparently healthy domestic poultry in eastern China in 2011 [38]. More isolates were found in ducks and geese which were transported from Shandong and Jiangsu Provinces to eastern China for trade. Upon checking, the first isolate H5N2 gene origin was rooted in the HA gene of H5N1 (A/goose/Guangdong/1/1996), whereas its N2 shared the highest homology with the NA gene of the duck H3N2 (A/duck/Eastern China/142/2006) [38][39]. Nonetheless, in 2011, H5N2 outbreaks in Shandong and six more provinces in China including Tibet were reported [40][38].
H5N2 has also been reported in Taiwan. Since December 2014, a series of HPAI H5N2 outbreaks, coupled with H5N8 and H5N3, were reported by the Taiwan government. In January 2015, the occurrence of H5N2 of Eurasian lineage had spread widely in various provinces of Taiwan with numerous accounts of mortalities among poultry and wild birds [24][41]. With the destruction of more than 2 million poultry from more than 950 poultry farms, Taiwan declared this event as the “largest epidemic” of avian influenza in their country’s history [40].
The panzootic spread of H5Nx exhibited its intercontinental transmissibility in 2014 [42][43][44]. H5Nx viruses were introduced to the North American continent through migratory fowls [45][46][25][14][47]. HPAI H5N8 viruses have reassorted with North American LPAI viruses in wild birds resulting in the generation of H5N1 and H5N2 [12]. The generated reassortant HPAI H5N2 contains five segments of the H5N8 and three from the North American LPAIV [45][46][25]. On 28 November 2014, mortalities in an 11,000-head turkey farm in Canada were reported; sequencing confirmed that H5N2 was the causative agent of this outbreak [48]. This was the first time that a Eurasian lineage of HPAI crossed into North America, specifically through Canada [45][48]. Since then, additional cases have been detected on poultry farms and in wild birds. Furthermore, an estimated 50 million birds have been culled and stamped out in numerous areas [49]. Notably, the majority of these outbreaks were deemed to be caused by the H5N2 subtype [45].

5. H5N3

The detection of the first H5N3 virus of Eurasian lineage was observed during Taiwan’s largest avian influenza epidemic in 2014 [40][41]. During avian influenza surveillance conducted by Taiwanese authorities, two novel HPAI H5N3 viruses from a chicken (a/chicken/Taiwan/a174/2015) and a duck (A/duck/Taiwan/a180/2015) on a farm located in Pingtung Province were detected [40]. Chang et al. (2016) revealed that the nucleotide identities of the representative isolates—three (HA, PA, and NS) likely of H5N3 genes of 99.82–100%—are highly associated with the wild bird H5N8 (A/crane/Kagoshima/KU13/2014) [40]. On the other hand, the N3 gene originated from H10N3 (A/duck/Jiangxi/33629/2013). The PB2 shares 97% similarity with that of the H6N2 isolated from a coot in Georgia (A/common coot/Republic of Georgia/1/2010) [40]. However, along with the H5N8 and H5N2 subtypes, this novel reassortant contributed to the massive outbreak of AIV in Taiwan (Figure 1) [41].
There were very few documentations of this subtype, and its occurrence has also been limited. To date, there have been reports of H5N3 causing outbreaks in China, Germany, and the Netherlands. The cases reported were limited and occurred sporadically.

6. H5N1

HPAI H5N1 of the Gs/GD lineage has been known for its impact and novel reassortants. It has been widely disseminated around the globe and reported in various hosts. Thus, this subtype has a long history of causing massive outbreaks affecting the poultry industry and poses a continuous threat to public health. According to Ducatez et al. (2017), H5N1 has three large expansions in clades 2.2, 2.3.2.1, and 2.3.4.4 [50]. Having been widely established in various hosts and environments, it was hardly surprising that a reassortant of H5N1 appeared under clade 2.3.4.4 recently.
Between December 2013 and 2014, a wave of HPAI outbreaks occurred in three counties of Yunnan, China. The reported outbreaks in Tonghai, Anning, and Dali killed 20,000 heads of layer poultry [51]. Upon sequence verification, the virus detected and isolated was found to belong to clade 2.3.4.4, sharing the highest identity of its HA gene with the isolates from H5N6 Laos (A/chicken/Laos/LPQ001/2014) and H5N6 China (A/duck/Guangdong/GD01/2014) [51]. Moreover, it was also identified that the NA gene of this emerging H5N1 was closely related to the N1 of isolates of clade 2.3.2, which are A/chicken/Vietnam/NCVD-KA423/2013, A/duck/Hunnan/S4220/2011, and A/duck/Zhejiang/213/2011. Nonetheless, all the other six genes of this novel emergent are shared with H5N2 A/duck/Jiangxi/JXA132023/2013 [51].

7. H5Nx Provisional Grouping

With the continuous emergence and observed diversity patterns of H5 viruses, Lee et al. proposed a provisional grouping for viruses belonging to clade 2.3.4.4. The H5Nx viruses were grouped into four (A-D) based on the phylogenetic relationships and the temporal evolutionary history of viruses when investigated using molecular clock analysis [52]. Moreover, Lee et al. also demonstrated that the genetic relatedness of viruses in each group are well supported by the observed high bootstrap values (>70%) and long HA branches [16][52]. Group A or 2.3.4.4A is composed of viruses such as the following: a) H5N8, identified from China in early 2014 and from South Korea, Japan, Taiwan, Canada, European countries and North America; b) H5N1 and H5N2 from North America; and c) H5N2 and H5N3 from Taiwan. On the other hand, group B or 2.3.4.4B is primarily composed of H5N8 viruses identified in China in 2013 and South Korea in 2014 [16][52]. Moreover, recent studies have suggested that H5N6 from South Korea in 2017–2018 as well as H5N5 and H5N8 from Germany in 2016–2017 also belong to this group by phylogenetic relatedness [53][54]. Group C of 2.3.4.4 clade is composed of H5N6 from China and Laos in 2013–2014 and H5N1 identified from Vietnam and China in 2014 [16][52]. Kim et al. also reported that H5N6 identified in Korea in 2016–2017 shares the phylogenetic relatedness in this group of 2.3.4.4 [55]. Remarkedly, 2013–2014 H5N6 identified in China and Vietnam were grouped in 2.3.4.4D [16][52]. Although this provisional grouping remained unofficial, few studies have adapted the groupings to elucidate the diversity patterns of clade 2.3.4.4 viruses or H5Nx based on molecular clock analysis.

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