Table 1.
Forty-two documented pandemics, epidemics, or limited outbreaks of HPAI since discovery of AI viruses as cause of fowl plague in 1955
| No. | Year | Country | Host species | Prototype AI virus | Subtype | Accession No. (NCBI GenBank or GISAID Epiflu database) | HA cleavage site | Number affected with high mortality or depopulateda |
|---|---|---|---|---|---|---|---|---|
| 1 | 1959 | Scotland | Domestic poultry | A/chicken/Scotland/1959 | H5N1 | GU052518 | PQRKKR/GLF | Aberdeen: 1 premise, unknown number of chickens (Gallus gallus domesticus) affected (Pereira et al. 1965; Alexander et al. 2008) |
| 2 | 1961 | South Africa | Wild bird | A/tern/South Africa/1961 | H5N3 | GU052822 | PQRETRRQKR/GLF | Western and Eastern Cape provinces (coastline from Port Elizabeth to Lambert's Bay): 1300 common terns (Sterna hirundo) (Rowan 1962; Becker 1966; Alexander et al. 2008) |
| 3 | 1963 | England | Domestic poultry | A/turkey/England/1963 | H7N3 | AF202238 | PETPKRRRR/GLF | Norfolk County: 2 farms; 29,000 breeder turkeys (Meleagridis gallopavo) in outdoor and indoor pens (Wells 1963; Alexander et al. 2008) |
| 4 | 1966 | Canada | Domestic poultry | A/turkey/Ontario/7732/1966 | H5N9 | CY107859 | PQRRRKKR/GLF | Ontario province: 2 indoor farms; 8,100 breeder turkeys (Lang et al. 1968; Swayne 2008b) |
| 5 | 1976 | Australia | Domestic poultry | A/chicken/Victoria/1976 | H7N7 | CY024786 | PEIPKKREKR/GLF | Victoria province: 2 farms; 25,000 indoor laying chickens, 17,000 indoor broilers, and 16,000 indoor and outdoor ducks (Anas platyrhyncos) (Anonymous 1976; Turner 1976; Bashiruddin et al. 1992; Sims and Turner 2008b) |
| 6 | 1979 | Germany | Domestic poultry | A/chicken/Germany/01/1979 A/goose/Leipzig/187_7/1979 A/goose/Leipzig/137/8/1979 A/chicken/Leipzig/79 A/goose/Leipzig/192/7/1979 |
H7N7 |
CY107844 L43914 L43913 U20459 L43915 |
PEIPKKKKKKR/GLF PETPKKKKKKR/GLF PEIPKRKKR/GLF PEIPKKKKR/GLF PEIPKKRKKR/GLF |
Saxony: 2 farms: 600,000 chickens, 80 geese (Röhm et al. 1996; Harder and Werner 2006; Alexander et al. 2008) |
| 7 | 1979 | England | Domestic poultry | A/turkey/England/199/1979 | H7N7 | N/A | PEIPKKRKR/GLF, PEIP KRRRR/GLF, PEIP KKREKR/GLF | Norfolk county: 3 commercial farms, 9262 turkeys (Alexander et al. 2008) |
| 8 | 1983–84 | USA | Domestic poultry | A/chicken/Pennsylvania/1/1983 (LP) A/chicken/Pennsylvania/1370/1983 (HP) | H5N2 |
J04325 GU052771 |
PQKKKR/GLF (LP) PQKKKR/GLF (HP) – lost a glycosylation site on amino acid 13 |
Pennsylvania, Maryland, and Virginia: 452 flocks, 17 million birds; mostly chickens or turkeys, a few chukar partridges (Alectoris chukar) and guinea fowl (Numida meleagris) (Kawaoka and Webster 1985; USAHA 1985; Eckroade and Silverman-Bachin 1986; Easterday et al. 1997) |
| 9 | 1983 | Ireland | Domestic poultry | A/turkey/Ireland/1378/1983 | H5N8 | M18451 | PQRKRKKR/GLF | Monaghan County: 4 farms; 8,120 turkeys, 28,020 chickens, and 270,000 ducks (McNulty et al. 1985; Alexander et al. 2008) |
| 10 | 1985 | Australia | Domestic poultry | A/chicken/Victoria/1/1985 | H7N7 | M17735 | PEIPKKREKR/GLF | Victoria province: 1 farm; 24,000 broiler breeders, 27,000 laying chickens, and 61,000 broilers (Barr et al. 1986; Cross 1987; Senne et al. 1996a; Sims and Turner 2008b) |
| 11 | 1991 | England | Domestic poultry | A/turkey/England/50-92/1991 | H5N1 | GU052510 | PQRKRKTR/GLF | Norfolk County: 1 farm; 8000 turkeys (Alexander et al. 1993; Alexander and Wood 1993; Wood et al. 1993; Senne et al. 1996) |
| 12 | 1992 | Australia | Domestic poultry | A/chicken/Victoria/1/1992 | H7N3 | AF202227 | PEIPKKKKR/GLF | Victoria province: 2 farms, 1 backyard flock and 1 hatchery; 17,000 broiler breeders, 5,700 ducks, 105,000 day-old chicks, 540,000 hatching eggs (Selleck et al. 1997; Westbury 1998; Sims and Turner 2008b) |
| 13 | 1994–95 | Australia | Domestic poultry | A/chicken/Queensland/1994 A/chicken/Queensland/667/1995 |
H7N3 |
CY022685 AF202231 |
PEIPRKRKR/GLF | Queensland province: 1 farm; 22,000 laying chickens (Westbury 1998; Perdue et al. 1999) |
| 14 | 1994–95 | Mexico | Domestic poultry | A/chicken/Mexico/31381-7/1994 (LP) A/chicken/Puebla/8623-607/1994 (HP) |
H5N2 |
GU186573 AB558473 |
PQRETR/GLF (LP) PQRKRKTR/GLF (HP) |
Puebla and Queretaro: Chickens—concurrent circulation of LP (1993–) and HPAI virus (late 1994 to mid-1995) strains. 360 commercial chicken flocks “depopulated” (1995) via vaccination and controlled marketing. Unknown number of HP-infected birds (García et al. 1996; Easterday et al. 1997; Perdue et al. 1997; Villareal and Flores 1998; Smith 2006) |
| A/chicken/Queretaro/14588_19/1995 A/chicken/Queretaro/7653_20/1995 |
H5N2 |
AB558474 U85390 |
PQRKRKTR/GLF PQRKRKRKTR/GLF |
|||||
| 15 | 1994–95, 2004 | Pakistan | Domestic poultry | A/chicken/Pakistan/447/1995 A/chicken/Pakistan/CR2/95 A/chicken/Karachi/NARC-23/2003 |
H7N3 |
AF202226 AF202230 HM346493 |
PETPKRKRKR/GLF PETPKRRKR/GLF |
Two incursions: (1) 3.2 million broilers and broiler breeder chickens (northern part of country, 1994–1995), and (2) 2.52 million layers (Karachi, 2004). Vaccination and controlled marketing (Naeem and Hussain 1995; Easterday et al. 1997; Naeem 1998; Banks et al. 2000) |
| 16 | 1996– cont. | 84 countries in Asia, Africa, Europe and North America | Domestic poultry and wild bird | A/goose/Guangdong/1/1996 (Gs/GD) | H5Nx |
NC_007362 | PQRERRRKKR/GLF (majority), Variations: 1) Clade 1, PQREGRRKKR/GLF; 2) Clade 2.1, PQRESRRKK/GLF; 3) Clade 2.2, QGERRRKKR/GLF; 4) Clade 2.3, PQRERRRKR/GLF, PLRERRRKR/GLF; 5) Clade 7, PQIEGRRRKR/GLF |
Unknown number of commercial and noncommercial flocks (principally village poultry); more than 400 million birds dead or culled from 2003 to early 2012, mostly chickens, but also ducks, geese, Japanese quail, and some wild birds (Sims et al. 2003a; Sims et al. 2003b; FAO 2006; Sims and Brown 2008a; Sims and Brown 2017). Largest HPAI outbreak since 1959 with more birds and countries affected than the other 41 outbreaks since 1959. |
| 17 | 1997 | Australia | Domestic poultry | A/chicken/NSW/1/1997 A/chicken/New_South_Wales/327/1997 |
H7N4 |
AY943924 CY022701 |
PEIPRKRKR/GLF PEIPRRRKR/GLF |
New South Wales province: 3 farms; 160,000 indoor broiler breeders and 261 outdoor emu (Dromaius novaehollandiae) (Perdue et al. 1999; Sims and Turner 2008b) |
| 18 | 1997 | Italy | Domestic poultry | A/poultry/Italy/330/1997 | H5N2 | CY017403 | PQRRRKKR/GLF | Veneto and Fruili–Venezia–Giulia Regions: 8 flocks (hobby/backyard only); 2116 chickens, 1501 turkeys, 731 guinea fowl, 2322 ducks, 204 quail (species unknown), 45 pigeons (Columbia livia), 45 geese (species unknown), 1 pheasant (species unknown) (Capua et al. 1999; Alexander et al. 2008) |
| 19 | 1999–2000 | Italy | Domestic poultry | A/turkey/Italy/977/1999 (LP) A/turkey/Italy/4580/1999 (HP) | H7N1 |
GU052999 CY021405 |
PEIPKGR/GLF (LP) PEIPKGSRVRR/GLF (HP, majority), PEIPKGSRMRR/GLF (HP, minor), PEIPKRSRVRR/GLF (HP, minor) |
Veneto and Lombardia Regions: 413 farms, 8.1 million laying chickens; 2.7 million meat and breeder turkeys; 2.4 million broiler breeders and broilers; 247,000 guinea fowl; 260,000 quail, ducks, and pheasants; 1,737 backyard poultry and 387 ostriches (Banks et al. 2001; Capua et al. 2003; Alexander et al. 2008) |
| 20 | 2002 | Chile | Domestic poultry | A/chicken/Chile/176822/2002 (LP) A/chicken/Chile/4322/2002 (HP) A/chicken/Chile/4957/2002 (HP) |
H7N3 |
AY303630 AY303631 AY303632 |
PEKPKTR/GLF (LP) PEKPKTCSPLSRCRETR/GLF (HP) PEKPKTCSPLSRCRKTR/GLF (HP) |
Valparaíso region: Two farms of one company, multiple houses; 617,800 broiler breeders, 18,500 turkey breeders (2 houses) (Rojas et al. 2002; Suarez et al. 2004; Max et al. 2007; Swayne 2008b) |
| 21 | 2003 | Netherlands Belgium Germany |
Domestic poultry | A/chicken/Netherlands/1/03 | H7N7 | AY338458 | PEIPKRRRR/GLF | (1) Netherlands, Gelderse Vallei and Limburg region: 255 infected flocks, and 1381 commercial and 16,521 backyard/smallholder flocks depopulated—30 million affected, mostly chickens. (2) Belgium (Limburg and Antwerp provinces), 8 farms, 2.3 million chickens. (3) Germany (Nordrhein–Westfalen State), 1 farm, 419,000 chickens (Elbers et al. 2004; Harder and Werner 2006; Alexander et al. 2008) |
| 22 | 2004 | Canada | Domestic poultry | A/chicken/Canada/AVFV1/2004 (LP) A/chicken/Canada/AVFV2/2004 (HP) |
H7N3 |
AY650270 AY648287 |
LP: PENPKTR/GLF HP: PENPKQAYRKRMTR/GLF PENPKQAYQKRMTR/GLF, PENPKQAYKKRMTR/GLF, PENPKQAYHKRMTR/GLF, PENPKQAHQKRMTR/GLF, PENPRQAYRKRMTR/GLF, PENPKQACQKRMTR/GLF |
British Columbia province: 42 commercial and 11 backyard flocks infected (1.2 million poultry)—approximately 16 million commercial poultry depopulated, most were chickens (Hirst et al. 2004; Pasick et al. 2005) |
| 23 | 2004 | USA | Domestic poultry | A/chicken/Texas/298313/2004 | H5N2 | AY849793 | PQRKKR/GLF | Texas state: 1 noncommercial farm (6608 chickens), 2 LPM affected; 3 dangerous LPM contacts culled (Lee et al. 2005) |
| 24 | 2004 | South Africa | Domestic poultry | A/ostrich/South Africa/N227/2004 | H5N2 | FJ519983 | PQREKRRKKR/GLF | East Cape province: 2004–2008 farms, culled. 23,625 ostriches, 3,550 other poultry (chickens, turkeys, geese, ducks, and pigeons), 1594 ostrich eggs and 1707 other farmed bird eggs (Abolnik 2007; Alexander et al. 2008; Abolnik et al. 2009) |
| 25 | 2006 | South Africa | Domestic poultry | A/ostrich/South_Africa/AI1160/2006 (LP) A/ostrich/South Africa/AI1091/2006 (HP) |
H5N2 |
EF591757 EF591749 |
PQRRKKR/GLF | Western Cape province: 24 farms, 7334 ostriches culled (Abolnik 2007; Alexander et al. 2008; Brown et al. 2017) |
| 26 | 2005 | North Korea | Domestic poultry | A/chicken/North Korea/1/2005 | H7N7 | N/A | PEIPKGRHRRPKR/GLF | 3 farms, 218,882 layer chickens culled; number dead unknown (Alexander et al. 2008) |
| 27 | 2007 | Canada | Domestic poultry | A/chicken/Saskatchewan/HR-00011/2007 | H7N3 | EU500860 | PENPKTTKPRPRR/GLF | Saskatchewan province: 1 farm, 10 barns, 49,500 broiler breeder hens and roosters (Swayne 2008b; Berhane et al. 2009) |
| 28 | 2008 | England | Domestic poultry | A/chicken/England/1158-114061/2008 | H7N7 | FJ476173 | PEIPKRKKR/GLF | Oxfordshire county: 1 farm, 25,000 free-range layer chickens (Brown et al. 2017) |
| 29 | 2009 | Spain | Domestic poultry | A/chicken/Spain/6279-2/2009 | H7N7 | GU121458 | PELPKGTKPRPRR/GLF | Guadalajara province: 1 farm, 5 barns; 308,640 layer chickens (Iglesias et al. 2010; Brown et al. 2017) |
| 30 | 2011–2013 | South Africa | Domestic poultry | A/ostrich/SA/AI2114/2011 A/ostrich/SA/AI2512/2011 |
H5N2 |
JX069081 JX069097 |
PQRRKKR/GLF PQRRRKR/GLF |
Western Cape province: 45,343 ostriches on 50 premises (Brown et al. 2017) |
| 31 | 2012–2013 | Taiwan | Domestic poultry | A/chicken/Taiwan/A1997/2012 A/chicken/Taiwan/1680/2013 |
H5N2 |
KF193394 KJ162620 |
PQRRKR/GLF PQRKKR/GLF |
Chang-Hua, Pingtung, Yunlin, and Penghu counties: 6 premises (4 native chickens, 1 broiler breeder, 1 layer chicken); 47,151 chickens (Lee et al. 2014; Brown et al. 2017) |
| 32 | 2012- present | Mexico | Domestic poultry | A/chicken/Jalisco/12283/2012 | H7N3 | JX908509 | PENPKDRKSRHRRTR/GLF | Jalisco, Aguascalientes, Guanajuato, Tlaxcala, and Puebla states: 110 premises, 18,906,702 poultry. Two waves of disease: (1) 6/13/2012–9/29/2012, and (2) 1/3/2013–ongoing (Maurer-Stroh et al. 2013; Brown et al. 2017) |
| 33 | 2012 | Australia | Domestic poultry | A/chicken/New South Wales/12-3121-1/2012 | H7N7 | N/A | PEIPRKRKR/GLF | New South Wales province: 1 premise, free-range layers, 50,000 chickens (Brown et al. 2017) |
| 34 | 2013 | Italy | Domestic poultry | A/chicken/Italy/13VIR4527-11/2013 | H7N7 | KF569186 | PETPKRRERR/GLF | Emilia-Romagna Region: 6 premises, layers, 952,658 chickens (Brown et al. 2017) |
| 35 | 2013 | Australia | Domestic poultry | A/chicken/New South Wales/13-02811-1/2013 | H7N2 | N/A | PEIPRKRKR/GLF | New South Wales province: 2 premises, free-range and caged layers, 490,000 chickens (Brown et al. 2017) |
| 36 | 2015 | England | Domestic poultry | A/chicken/England/26352/2015 (H7N7) | H7N7 | EPI623939 | PEIPRHRKGR/GLF | Lancashire county: 1 premise, colony and free-range laying chickens, 179,865 affected (Brown et al. 2017) |
| 37 | 2015 | Germany | Domestic poultry | A/chicken/Germany/AR1385/2015 (H7N7) | H7N7 | EPI634885 | PEIPKRKRR/GLF | Lower Saxony state: 1 premise, laying chickens, 10,104 affected (Brown et al. 2017) |
| 38 | 2015–2016 | France | Domestic poultry | A/chicken/France/150169a/2015 A/duck/France/150233/2015 A/duck/France/150236/2015 |
H5N1 H5N2 H5N9 |
KU310447 KX014878 KX014886 |
HQRRKR/GLF | 8 southwest/southcentral Departments: 81 premises, 155,415 poultry affected; primarily affected fattening ducks, and some guinea fowl, geese, and layer and meat chickens in small farms and backyard operations. H5N1 virus reassorted with Eurasian LPAI viruses to produce H5N2 and H5N9 HPAI viruses (OIE 2016b; Briand et al. 2017) |
| 39 | 2016 | USA | Domestic poultry | A/turkey/Indiana/16-001403-1/2016 | H7N8 | KU558906 | PENPKKRKTR/GLF | Indiana state, Dubois county: 1 premise, 43,500 meat turkeys. 1 dangerous contact layer farm (156,158 layers), and 9 LP-affected turkey farms (195,937 birds) in control zone depopulated (ISBOAH 2016; Lee et al. 2017b; Swayne et al. 2017) |
| 40 | 2016 | Italy | Domestic poultry | A/chicken/Italy/16VIR-1873/2016 | H7N7 | EPI756028* | PELPKGRKRR/GLF | Emilia-Romagna region: 1 premise, 17,500 organic/free range layers (OIE 2016a; OIE 2016b) |
| 41 | 2016–2019 | China | Domestic poultry | A/chicken/Huizhou/HZ-3/2016 A/chicken/Huizhou/HZ04/2016 A/chicken/Heyuan/16876/2016 |
H7N9 | EPI917102 EPI918826 EPI919533 |
PEVPKRKRTAR/GLF; PEVPKGKRTAR/GLF |
Initially Guangdong province: Since 10 January 2017, HP H7N9 virus was reported in a total of 58 poultry or environmental samples (46 chickens, 2 duck, and 10 environmental samples); H7N9 virus isolates from 32 human cases were found to be HP virus (as of 07 August 2019). HP derived from LP virus circulating in live poultry market system since early 2013 (OIE 2017a; Qi et al. 2018) |
| 42 | 2017 | USA | Domestic poultry | A/chicken/Tennessee/17-007147-1/2017 | H7N9 | MF357740 | PENPKTDRKSRHRRIR/GLF | Tennessee, Lincoln county: 2 premise, 128,000 chicken broiler breeders with HPAI virus. LPAI precursor virus on 12 premises (6 backyard and 6 commercial, 125,000 birds) in Tennessee, Alabama, Kentucky and Georgia (Lee et al. 2017a; OIE 2017b; USDA 2017) |
Data modified from Alexander (2000), Swayne and Suarez (2000), Swayne (2017), OFFLU (2019), and Swayne et al. (2020).
(AI) Avian influenza, (GISAID) Global Initiative on Sharing All Influenza Data, (HA) hemagglutinin, (HP) high pathogenicity, (LP) low pathogenicity, (LPM) live poultry market, (N/A) not available, (NCBI) National Center for Biotechnology Information.
aMost outbreaks were controlled by “stamping-out” or depopulation policies for infected and/or exposed populations of poultry. Chickens, turkeys, and poultry in the order Galliformes had clinical signs and mortality patterns consistent with HPAI, whereas ducks, geese, and other aquatic poultry lacked or had low mortality rates or infrequent presence of clinical signs.