Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): West Nile fever

Abstract

West Nile fever (WNF) has been assessed according to the criteria of the Animal Health Law (AHL), in particular criteria of Article 7 on disease profile and impacts, Article 5 on the eligibility of WNF to be listed, Article 9 for the categorisation of WNF according to disease prevention and control rules as in Annex IV and Article 8 on the list of animal species related to WNF. The assessment has been performed following a methodology composed of information collection and compilation, expert judgement on each criterion at individual and, if no consensus was reached before, also at collective level. The output is composed of the categorical answer, and for the questions where no consensus was reached, the different supporting views are reported. Details on the methodology used for this assessment are explained in a separate opinion. According to the assessment performed, WNF can be considered eligible to be listed for Union intervention as laid down in Article 5(3) of the AHL. The disease would comply with the criteria as in Sections 2 and 5 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in points (b) and (e) of Article 9(1). The animal species to be listed for WNF according to Article 8(3) criteria are several orders of birds and mammals as susceptible species and several families of birds as reservoir. Different mosquito species can serve as vectors.

1. Introduction

1.1. Background and Terms of Reference as provided by the requestor

The background and Terms of Reference (ToR) as provided by the European Commission for the present document are reported in Section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the Animal Health Law (AHL) framework (EFSA AHAW Panel, 2017a).

1.2. Interpretation of the Terms of Reference

The interpretation of the ToR is as in Section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the AHL framework (EFSA AHAW Panel, 2017a).

The present document reports the results of assessment on West Nile fever (WNF) according to the criteria of the AHL articles as follows:

• Article 7: West Nile fever profile and impacts

• Article 5: eligibility of West Nile fever to be listed

• Article 9: categorisation of West Nile fever according to disease prevention and control rules as in Annex IV

• Article 8: list of animal species related to West Nile fever.

2. Data and methodologies

The methodology applied in this opinion is described in detail in a dedicated document about the ad hoc method developed for assessing any animal disease for the listing and categorisation of diseases within the AHL framework (EFSA AHAW Panel, 2017a).

3. Assessment

3.1. Assessment according to Article 7 criteria

This section presents the assessment of WNF according to the Article 7 criteria of the AHL and related parameters (see Table 2 of the opinion on methodology (EFSA AHAW Panel, 2017a)), based on the information contained in the fact sheet as drafted by the selected disease scientist (see Section 2.1 of the scientific opinion on the ad hoc methodology) and amended by the AHAW Panel.

Table 2.

Duration of infection period in experimentally infected birds

Species	Viraemia duration	Cloacal and oropharyngeal WNV shedding	Inoculum (WNV isolate, dose and inoculation route)	Challenge dose	Reference
Rock pigeons (Columbia livia)	2 days (viraemia)	15 dpi	3 WNV Italian isolates (L1*) (IT/2009‐IT/2011‐IT/2012) 1 mL subcutaneously	106 TCID50/mL	Spedicato et al. (2016)
Red‐legged partridge (Alectoris rufa)	4 days (viraemia)	7 dpi	1 WNV Morocco isolate (Mo/03) (L1) 1 WNV Spanish isolate (SP/07)(L1) 0.1 mL subcutaneously	104 PFU/bird	Sotelo et al. (2011b)
House sparrows (Passer domesticus)	3 days (viraemia)	12 dpi	2 WNV Italian isolates (IT/2008 and IT/2009)(L1) 1 WNV Spanish isolate (SP/07)(L1) 1 WNV US isolate (NY99)(L1) 0.1 mL subcutaneously	104 PFU/bird	Del Amo et al. (2014)
Gyrfalcons (Falco rusticolus)	4–6 days (viraemia)	21 dpi	1 WNV US isolate (NY99)(L1) 1WNV Austrian isolate (Aus/09)(L2*) 1 mL subcutaneously	Low dose: 500 TCID50/mL Medium dose: 104 TCID50/mL High dose: 106 TCID50/mL	Ziegler et al. (2013)

WNV: West Nile virus; TCID₅₀: tissue culture infective dose, median; PFU: plaque‐forming unit.

3.1.1. Article 7(a) Disease Profile

West Nile virus (WNV) belongs to the Flaviviridae family, genus Flavivirus, and is included in the serocomplex of Japanese Encephalitis virus together with Murray Valley encephalitis (MVE), St. Louis encephalitis (SLE), Kunjin (KUN), Usutu (USU), Koutango (KOU), Cacipacore (CPC), Alfuy (ALF) and Yaounde (YAO) viruses. Apart from Usutu virus, the other viruses in the serocomplex are not present in Europe. The virus was isolated for the first time in 1937 in Uganda, from the blood of a woman with febrile symptoms who came from the West Nile district (hence the name West Nile fever).

Different genetic lineages have been identified worldwide but the strains responsible for serious epidemics are attributable to Lineage 1 and, more recently, also to Lineage 2. Phylogenetic analyses revealed that all European WNV lineage 1 and 2 strains are derived from a limited number of independent introductions, most likely from Africa, followed by local spread and evolution. Other lineages have been identified but not associated so far with human or animal diseases.

WNV is transmitted by different genera and species of mosquitoes. The main vectors are some of the species of ornithophilic mosquitoes belonging to the genus Culex, which is always closely associated with the transmission of WNV during outbreaks. The mosquitoes cease their activity during the colder months, but it has been demonstrated that the virus is able to survive during this period in the infected mosquitoes, which overwinter indoors.

3.1.1.1. Article 7(a)(i) Animal species concerned by the disease

Susceptible animal species

Parameter 1 – Naturally susceptible wildlife species (or family/orders)

Several orders of birds can be naturally susceptible to WNV infections, i.e. Anseriformes, Apodiformes, Caprimulgiformes, Casuariiformes, Charadriiformes, Ciconiformes, Columbiformes, Coraciiformes, Cuculiformes, Falconiformes, Galliformes, Gaviformes, Gruiformes, Musophagiformes, Passeriformes, Pelecaniformes, Piciformes, Podicipediformes, Psittaciformes, Spheniscformes, Strigiformes and Struthioniformes.

Also several orders of mammals can be naturally susceptible to WNV infections, i.e. Artiodactyla, Carnivora, Chiroptera, Perissodactyla, Primates, Proboscidea and Rodentia.

Two orders of reptiles can be naturally susceptible to WNV infections: Crocodylia and Squamata.

Details concerning the susceptible families and species of the above mentioned orders are listed in Table A.1 in Appendix A.

Table A.1.

Naturally susceptible wildlife species (or family/orders)

Class	Order	Family	Species
Aves	Anseriformes	Anatidae	Wood duck‐Aix sponsa, Eurasian wigeon‐Anas penelope (c), bronze‐winged duck (spectacled duck)‐Anas specularis (c), canvasback‐Aythya valisineria, Canada goose‐Branta Canadensis, barnacle goose‐Branta leucopsis (c)(a), emperor goose‐Chen canagica (c), greater Magellan goose (Andean goose)‐Chloephagapicta leucoptera (c)(a), Abyssinian blue‐winged goose‐Cyanochen cyanopterus (c)(a), tundra swan‐Cygnus columbianus (c), trumpeter swan‐Cygnus Cygnus buccinator (c)(a), mute swan‐Cygnus olor, Rosy‐billed pichard‐Netta peposaca (c)(a), ruddy duck‐Oxyura jamaicensis
	Apodiformes	Apodidae	Chimney swift‐Chaetura pelagica
		Trochilidae	Ruby‐throated hummingbird‐Archilochus colubris
	Caprimulgiformes	Caprimulgidae	Common nighthawk‐Chordeiles minor
	Casuariiformes	Dromaiidae	Emu‐Dromaius novaehollandiae (c)
	Charadriiformes	Haradriidae	Ruddy turnstone‐Arenaria interpres, killdeer‐Charadrius vociferous, piping plover‐Charadrius melodus
		Laridae	European herring gull‐Larus argentatus, laughing gull‐Larus atricilla, ring‐billed gull‐Larus delawarensis, great black‐backed gull‐Larus marinus, black skimmer‐Rhynchops niger, grey gull‐Larus modestus (c)(a), Inca tern‐Larosterna inca (c)(a)
	Ciconiformes	Ardeidae	Yellow‐crowned night‐heron‐Nyctanassa violacea (c), black‐crowned night‐heron‐Nycticorax nycticorax (c), great blue heron‐Ardea Herodias, green heron‐Butorides virescens, least bittern‐Ixobrychus exilis
		Cathartidae	Turkey vulture‐Cathartes aura, black vulture‐Coragyps atratus, king vulture‐Sarcoramphus papa (c)(a)
		Ciconiidae	Saddle‐billed stork‐Ephippiorhynchos senegalensis (c)(a), marabou stork‐Leptopilos crumeniferus (c)(a), lesser adjutant‐Leptoptilos javanicus (c)(a)
		Phoenicopteridae	Chilean flamingo‐Phoenicopterus chilensis (c), greater flamingo‐Phoenicopterus ruber ruber (c)
		Threskiornithidae	Scarlet ibis‐Eudocimus ruber (c), northern bald ibis‐Geronticus eremita (c)(a)
	Columbiformes	Columbidae	White‐crowned pigeon‐Columba leucocephala, rock dove‐Columba livia, Mauritius pink pigeon‐Columba mayeri (c)(a), common ground‐dove‐Columbina passerine, Eurasian collared‐dove‐Streptopelia decaocto, white‐winged dove‐Zenaida asiatica, mourning dove‐Zenaida macroura, Luzon bleeding‐heart‐Gallicolumba luzonica (c)(a), Inca dove‐Columbina inca
	Coraciiformes	Alcedinidae	Belted kingfisher‐Ceryle alcyon
	Cuculiformes	Cuculidae	Yellow‐billed cuckoo‐Coccyzus americanus
	Falconiformes	Accipitridae	Cooper's hawk‐Accipiter cooperii, Northern goshawk‐Accipiter gentilis, sharp‐shinned hawk‐Accipiter striatus, golden eagle‐Aquila chrysaetos, red‐tailed hawk‐Buteo jamaicensis, rough‐legged hawk‐Buteo lagopus (c), red‐shouldered hawk‐Buteo lineatus, broad‐winged hawk‐Buteo platypterus, Swainson's hawk‐Buteo swainsoni, Northern harrier‐Circus cyaneus, swallow‐tailed kite‐Elanoides forficatus, bald eagle‐Haliaeetus leucocephalus, Mississippi kite‐Ictinia mississippiensis, Osprey‐Pandion haliaetus, Harris's hawk‐Parabuteo unicinctus (c)
		Falconidae	Merlin‐Falco columbarius, prairie falcon‐Falco mexicanus, peregrine falcon‐Falco peregrinus, American kestrel‐Falco sparverius
	Galliformes	Numididae	Crested guineafowl‐Guttera pucherani (c)(a)
		Odontophoridae	Northern bobwhite‐Colinus virginianus
		Phasianidae	Chukar‐Alectoris chukar (c)(a), ruffed grouse‐Bonasa umbellus, green junglefowl‐Gallus varius (c)(a), Himalayan monal‐Lophophorus impeyanus (c), Bulwer's pheasant‐Lophura bulweri (c)(a), ring‐necked pheasant‐Phasianus colchicus, mountain peacock‐pheasant‐Polypectron inopinatum (c)(a), crested partridge‐Rollulus roulroul (c)(a), Blyth's tragopan‐Tragopan blythii (c), argus pheasant (unspecified)‐various (c)(a), greater sage grouse‐Centrocerus urophasianus
	Gaviiformes	Gaviidae	Common loon‐Gavia immer
	Gruiformes	Gruidae	Demoiselle crane‐Anthropoides virgo (c)(a), West African crowned crane‐Balearica pavonina pavonina (a), wattled crane‐Bugeranus carunculatus (c)(a), whooping crane‐Grus americana (c)(a), Mississippi sandhill crane‐Grus canadensis pulla (c), red‐crowned crane‐Grus japonensis (c)(a), Siberian crane‐Grus leucogeranus (c)(a), hooded crane‐Grus monacha (c)(a), white‐naped crane‐Grus vipio (c)(a) black‐necked crane‐Grus nigricollis (c)(a)
		Rallidae	Virginia rail‐Rallus limicola
	Musophagiformes	Musophagidae	Lady Ross's turaco‐Musophaga rossae (c)(a)
	Passeriformes	Bombycillidae	Cedar waxwing‐Bombycilla cedrorum
		Cardinalidae	Northern cardinal‐Cardinalis cardinalis, blue grosbeak‐Guiraca caerulea (a), rose‐breasted grosbeak‐Pheucticus ludovicianus, dickcissel‐Spiza americana
		Corvidae	Western scrub‐jay‐Aphelocoma californica, American crow‐Corvus brachyrhynchos, common raven‐Corvus corax, fish crow‐Corvus ossifragus, blue jay‐Cyanocitta cristata, Steller's jay‐Cyanocitta stelleri, black‐billed magpie‐Pica hudsonia (c)
		Emberizidae	Song sparrow‐Melospiza melodia, savannah sparrow‐Passerculus sandwichensis, fox sparrow‐Passerella iliaca, Eastern towhee‐Pipilo erythrophthalmus, field sparrow‐Spizella pusilla
		Estrildidae	Zebra finch‐Taeniophygia guttata (c)
		Fringillidae	American goldfinch‐Carduelis tristis, house finch‐Carpodacus mexicanus, purple finch‐Carpodacus purpureus, evening grosbeak‐Coccothraustes vespertinus, European goldfinch‐Carduelis carduelis (c)
		Hirundinidae	Barn swallow‐Hirundo rustica, purple martin‐Progne subis, tree swallow‐Tachycineta bicolor
		Icteridae	Red‐winged blackbird‐Agelaius phoeniceus, rusty blackbird‐Euphagus carolinus, Brewer's blackbird‐Euphagus cyanocephalus, Baltimore oriole‐Icterus galbula, brown‐headed cowbird‐Molothrus ater, boat‐tailed grackle‐Quiscalus major, great‐tailed grackle‐Quiscalus mexicanus, common grackle‐Quiscalus quiscula
		Laniidae	Loggerhead shrike‐Lanius ludovicianus
		Mimidae	Gray catbird‐Dumetella carolinensis, Northern mockingbird‐Mimus polyglottos, brown thrasher‐Toxostoma rufum
		Paridae	Tufted titmouse‐Baeolophus bicolor, varied tit‐Parus varius (c), black‐capped chickadee‐Poecile atricapilla, Carolina chickadee‐Poecile carolinensis
		Parulidae	Black‐throated blue warbler‐Dendroica caerulescens, yellow‐rumped warbler‐Dendroica coronate, yellow warbler‐Dendroica petechial, blackpoll warbler‐Dendroica striata, common yellowthroat‐Geothlypis trichas, Kentucky warbler‐Oporornis formosus, Northern parula‐Parula Americana, ovenbird‐Seiurus aurocapillus, Northern waterthrush‐Seiurus noveboracensis, Nashville warbler‐Vermivora ruficapilla, Canada warbler‐Wilsonia Canadensis, hooded warbler‐Wilsonia citrina
		Passeridae	House sparrow‐Passer domesticus
		Sylviidae	White‐crested laughingthrush‐Garrulax leucolophus (c)(a)
		Sittadae	White‐breasted nuthatch‐Sitta carolinensis
		Sturnidae	European starling‐Sturnus vulgaris
		Thraupidae	Palm tanager‐Thraupis palmarum (c)
		Troglodytidae	Carolina wren‐Thryothaurus ludovicianus, winter wren‐Troglodytes troglodytes
		Turdidae	Veery‐Catharus fuscescens, hermit thrush‐Catharus guttatus, gray‐cheeked thrush‐Catharus minimus, Swainson's thrush‐Catharus ustulatus, wood thrush‐Hylocichla mustelina, Eastern bluebird‐Sialia sialis, American robin‐Turdus igratorius
		Tyrannidae	Traill's flycatcher‐Empidonax traillii/alnorum, Eastern phoebe‐Sayornis phoebe, scissor‐tailed flycatcher‐Tyrannus forficatus, Eastern kingbird‐Tyrannus tyrannus
		Vireonidae	Black‐whiskered vireo‐Vireo altiloquus, warbling vireo‐Vireo gilvus, red‐eyed vireo‐Vireo olivaceus
	Pelecaniformes	Pelecanidae	American white pelican‐Pelecanus erythrorhynchos, brown pelican‐Pelicanus occidentalis (c)(a), double‐crested cormorant‐Phalacrocorax auritus, guanay cormorant‐Phalacrocorax bougainvillei (c)
	Piciformes	Picidae	Red‐headed woodpecker‐Melanerpes erythrocephalus, downy woodpecker‐Picoides pubescens, yellow‐bellied sapsucker‐Sphyrapicus varius
	Podicipediformes	Podicipedidae	Pied‐billed grebe‐Podilymbus podiceps
	Psittaciformes	Cacatuidae	Cockatoo (unspecified)‐Cacatua spp. (c), cockatiel‐Nymphicus hollandicus (c)
		Psittacidae	Red‐crowned parrot‐Amazona viridigenalis (c), macaw (unspecified)‐Ara spp. (c), budgerigar‐Melopsittacus undulatus (c), lorikeet spp.‐Tricheglossus spp. (c)
	Sphenisciformes	Spheniscidae	African penguin‐Spheniscus demersus (c), Magellan penguin‐Spheniscus humboldti (c)(a)
	Strigiformes	Strigidae	Northern saw‐whet owl‐Aegolius acadicus, boreal owl‐Aegolius funereous (c), short‐eared owl‐Asio flammeus, Verreaux's eagle owl (milky eagle owl)‐Bubo lacteus (c)(a), great horned owl‐Bubo virginianus, snowy owl‐Nyctea scandiaca (c), Eastern screech owl‐Otus asio, tawny owl‐Strix aluco (c), great grey owl‐Strix nebulosa (c), spotted owl‐Strix occidentalis (c), barred owl‐Strix varia, Northern hawk owl‐Surnia ulula (c)
		Tytonidae	Barn owl‐Tyto alba
	Struthioniformes	Struthionidae	Ostrich‐Struthio camelis (c)(a)
Mammalia	Artiodactyla	Bovidae	Mountain goat‐Oreamnos americanus (c)
		Camelidae	Llama‐Lama glama (c), alpaca‐Lama pacos (c)
		Cervidae	White‐tailed deer‐Odocoileus virgninianus, reindeer‐Rangifer tarnadus (c), mule deer‐Odocoileus hemionus
		Suidae	Babirusa‐Babyrousa babyrousa (c)(a)
	Carnivora	Canidae	Timber wolf‐Canis lupus (c)
		Mustelidae	Striped skunk‐Mephitis mephitis
		Phocidae	Harbor seal‐Phoca vitulina (c)
		Procyonidae	Red panda‐Ailurus fulgens fulgens (c)(a)
		Ursidae	Black bear‐Ursus americanus (a)
	Chiroptera	Vespertilionidae	Big brown bat‐Eptesicus fuscus, little brown bat‐Myotis lucifugus
	Perissodactyla	Rhinocerotidae	Great Indian rhinoceros‐Rhinoceros unicornis (c)(a)
	Primates	Cercopithecidae	Barbary macaque‐Macaca sylvanus (c)
		Lemuridae	Ring‐tailed lemur‐Lemur catta (c)
	Proboscidea	Elephantidae	Indian (Asian) elephant‐Elephas maximus indicus (c)(a)
	Rodentia	Sciuridae	Gray squirrel‐Sciurus carolinensis, fox squirrel‐Sciurus niger, Eastern chipmunk‐Tamias striatus
Reptilia	Crocodylia	Alligatoridae	American alligator‐Alligator mississippiensis (c)
	Squamata	Varanidae	Crocodile monitor‐Varanus salvadorii (c)(a)

(c) Denotes either a captive or farmed animal(s). Virus or viral RNA was detected in animal tissue unless followed by an (a), which denotes detectable antibodies only have been reported (Source: USGS, National Wildlife Health Center (USGS, online)).

Parameter 2 – Naturally susceptible domestic species (or family/orders)

Several families of domestic animals can be naturally susceptible to WNV infections, i.e. Phasianidae, Anatidae, Bovidae, Canidae, Felidae, Leporidae and Equidae.

Details concerning the susceptible species of the above mentioned families are listed in Table A.2 in Appendix A.

Table A.2.

Naturally susceptible domestic species (or family/orders)

Class	Order	Family	Species
Aves	Galliformes	Phasianidae	Domestic chicken (Red junglefowl)‐Gallus gallus Turkey (domestic and wild)‐Meleagris gallopavo
	Anseriformes	Anatidae	Mallard‐Anas platyrhynchos Domestic goose‐Anser chinensis (c)(a)
Mammalia	Artiodactyla	Bovidae	Domestic cattle‐Bos taurus Domestic (suffolk) sheep‐Ovis aries
	Carnivora	Canidae	Domestic dog‐Canis familiaris
		Felidae	Domestic cat (feral)‐Felis catus
	Lagomorpha	Leporidae	Domestic rabbit‐Oryctolagus cuniculus
	Perissodactyla	Equidae	Domestic horse‐Equus equus przewalski caballus Donkey‐Equus asinus Mule

(c) Denotes either a captive or farmed animal(s). Virus or viral RNA was detected in animal tissue unless followed by an (a), which denotes detectable antibodies only have been reported (Source: USGS, National Wildlife Health Center (USGS, online)).

Parameter 3 – Experimentally susceptible wildlife species (or family/orders)

Several wild birds of the orders Passeriformes, Falconiformes, Accipitriformes, Strigiformes, Galliformes, Pelecaniformes, Columbiformes, Gruiformes, Anseriformes, Charadriiformes, Psittaciformes and Piciformes were successfully infected (see Table A.3 in Appendix A for the outcomes of experimental infections of WNV performed in wild birds (adapted from Pérez‐Ramírez et al. (2014) (Pérez‐Ramírez et al., 2014)).

Table A.3.

Summary outcomes of experimental infections of West Nile virus performed in wild birds (adapted from Pérez‐Ramírez et al. (2014))

Order	Family	Species	Strain	Mortality	Viraemia	Distribution	References
Passeriformes	Turdidae	American robin (Turdus migratorius)	NY	< 20%	H	AM	Komar et al. (2003), VanDalen et al. (2013)
		Swainson's thrush (Catharus ustulatus)	NY	< 20%	M	AM	Owen et al. (2006)
		Clay‐coloured thrush (Turdus grayi)	TEC/TAB	20–50%/< 20%	M	AM	Guerrero‐Sánchez et al. (2011)
	Corvidae	Carrion crow (Corvus corone)	FR/ISR	20–50%/> 50%	L	EUR/ASIA	Dridi et al. (2013)
		American crow (Corvus brachyrhynchos)	NY/TEX/MEX	> 50%	H	AM	McLean et al. (2001), Komar et al. (2003), Brault et al. (2004), Weingartl et al. (2004), Kinney et al. (2006), Kipp et al. (2006), Brault et al. (2007, 2011), Nemeth et al. (2011)
			KEN/KUN	20–50%/< 20%	M
		Fish crow (Corvus ossifragus)	NY	> 50%	H	AM	Komar et al. (2003), Kipp et al. (2006), Nemeth et al. (2011)
		Little raven (Corvus mellori)	NY	< 20%	M	OCE	Bingham et al. (2010)
			KUN	< 20%	L
		Hooded crow (Corvus cornix)	EGY	> 50%	H	EUR/ASIA/AFR	Work et al. (1955)
		Western scrub‐jay (Aphelocoma californica)	NY	> 50%	H	AM	Reisen et al. (2005)
		Blue jay (Cyanocitta cristata)	NY	> 50%	H	AM	Komar et al. (2003), Weingartl et al. (2004)
		Black‐billed magpie (Pica hudsonia)	NY	> 50%	H	AM	Komar et al. (2003)
		Jungle crow (Corvus macrorhynchos)	NY	> 50%	H	ASIA	Shirafuji et al. (2008)
	Passeridae	House sparrow (Passer domesticus)	NY/CA/KEN/EGY/TAB/TEC/SP/IT09	> 50%	H	WORLDWIDE	Work et al. (1955), Komar et al. (2003, 2005), Langevin et al. (2005), Reisen et al. (2005, 2006), Nemeth et al. (2008), LaPointe et al. (2009); Nemeth et al. (2009a,b), Brault et al. (2011), Guerrero‐Sánchez et al. (2011), Wheeler et al. (2012), Del Amo et al. (2014)
			TEX/KUN/IT08	< 20%	M
			MEX	< 20%	L
		Cape sparrow (Passer melanurus)	SA*	Und	L	AFR	McIntosh et al. (1969)
	Icteridae	Red‐winged blackbird (Agelaius phoeniceus)	NY	< 20%	M/L	AM	Komar et al. (2003), Reisen and Hahn (2007), Nemeth et al.(2009b)
		Brown‐headed cowbird (Molothrus ater)	NY	< 20%	L	AM	Reisen et al. (2006), Reisen and Hahn (2007)
		Brewer's blackbird (Euphagus cyanocephalus)	NY	< 20%	H	AM	Reisen et al. (2006), Reisen and Hahn (2007)
		Tricolored blackbird (Agelaius tricolor)	NY	< 20%	H	AM	Reisen and Hahn (2007)
		Common grackle (Quiscalus quiscula)	NY	20–50%	H	AM	Komar et al. (2003)
		Great‐tailed grackle (Quiscalus mexicanus)	TAB/TEC	> 50%/20–50%	H	AM	Guerrero‐Sánchez et al. (2011)
		Bay‐winged cowbird (Agelaioides badius)	ARG	< 20%	L	AM	Diaz et al. (2011)
		Shiny cowbird (Molothrus bonariensis)	ARG	< 20%	L	AM	Diaz et al. (2011)
	Emberizidae	Song sparrow (Melospiza melodia)	NY	< 20%	M	AM	Reisen and Fang (2007)
		White‐crowned sparrow (Zonotrichia leucophrys)	NY	Und	na	AM	Reisen et al. (2006)
	Fringillidae	Hawai'i ‘amakihi (Hemignathus virens)	NY	20–50%	H	AM	LaPointe et al. (2009)
		House finch (Haemorhous mexicanus)	NY	> 50%	H	AM	Komar et al. (2003), Reisen et al. (2005), Fang and Reisen (2006), Reisen et al. (2006)
	Ploceidae	African masked weaver (Ploceus velatus)	SA*	Und	M	AFR	McIntosh et al. (1969)
		Red‐billed quelea (Quelea quelea)	SA*	Und	L	AFR	McIntosh et al. (1969)
		Red bishop (Euplectes orix)	SA*	Und	M	AFR	McIntosh et al. (1969)
	Hirundinidae	Cliff swallow (Petrochelidon pyrrhonota)	NY	< 20%	M	AM	Oesterle et al. (2009, 2010)
	Mimidae	Gray catbird (Dumetella carolinensis)	NY	< 20%	M	AM	Owen et al. (2006)
		Northern mockingbird (Mimus polyglottos)	NY	< 20%	H	AM	Komar et al. (2005)
	Sturnidae	European starling (Sturnus vulgaris)	NY	< 20%	M	WORLDWIDE	Komar et al. (2003); Reisen et al. (2006)
	Cardinalidae	Northern cardinal (Cardinalis cardinalis)	NY	< 20%	H	AM	Komar et al. (2005); Owen et al. (2012)
	Paridae	Tufted titmouse (Baeolophus bicolor)	NY	> 50%	H	AM	Kilpatrick et al. (2013)
	Troglodytidae	Carolina wren (Thryothorus ludovicianus)	NY	20–50%	H	AM	Kilpatrick et al. (2013)
Falconiformes	Falconidae	Gyrfalcon (Falco rusticolus)	AUS*	20–50%	H	AM/EUR/AS	Ziegler et al. (2013)
			NY	20–50%	M
		Hybrid falcon (Falco rusticolus x Falco cherrug)	NY	< 20%	L	WORLDWIDE	Busquets et al. (2012)
		American kestrel (Falco sparverius)	NY	< 20%	H	AM	Komar et al. (2003), Nemeth et al. (2006a)
		Common kestrel (Falco tinnunculus)	EGY	< 20%	L	EUR/AS/AFR	Work et al. (1955)
Accipitriformes	Accipitridae	Red‐tailed hawk (Buteo jamaicensis)	NY	< 20%	H	AM	Nemeth et al. (2006a)
Strigiformes	Tytonidae	Barn owl (Tyto alba)	NY	< 20%	L	WORLDWIDE	Nemeth et al. (2006a)
	Strigidae	Great horned owl (Bubo virginianus)	NY	< 20%	H	AM	Komar et al. (2003), Nemeth et al. (2006a)
		Eastern screech‐owl (Megascops asio)	NY	> 50%	H	AM	Nemeth et al. (2006a)
Galliformes	Odontophoridae	California quail (Callipepla californica)	NY	< 20%	L	AM	Reisen et al. (2005, 2006)
		Gambel's quail (Callipepla gambelii)	NY	< 20%	L	AM	Reisen et al. (2006)
		Northern bobwhite (Colinus virginianus)	NY	< 20%	L	AM	Komar et al. (2003)
	Phasianidae	Red‐legged partridge (Alectoris rufa)	SP/MO	20–50%/> 50%	H	EUR	Sotelo et al. (2011b)
			NY	> 50%	L		Escribano‐Romero et al. (2013)
		Japanese quail (Coturnix japonica)	NY	< 20%	L	WORLDWIDE	Komar et al. (2003)
		Ring‐necked pheasant (Phasianus colchicus)	NY	< 20%	L	WORLDWIDE	Komar et al.(2003)
		Greater sage‐grouse (Centrocercus urophasianus)	NY	> 50%	M	AM	Clark et al. (2006)
Pelecaniformes	Ardeidae	Rufous night‐heron (Nycticorax caledonicus)	KUN	< 20%	L	OCE	Boyle et al. (1983b,a)
		Little egret (Egretta garzetta)	KUN	< 20%	L	EUR/AS/AFR/OCE	Boyle et al. (1983a,b)
		Intermediate heron (Mesophoyx intermedia)	KUN	< 20%	L	AFR/AS	Boyle et al. (1983a,b)
		Cattle egret (Bubulcus ibis)	SA*/EGY	Und/< 20%	L	WORLDWIDE	Work et al. (1955); McIntosh et al. (1969)
	Threskiornithidae	African sacred ibis (Threskiornis aethiopicus)	SA*	Und	L	AFR/AS	McIntosh et al. (1969)
Columbiformes	Columbidae	Rock pigeon (Columba livia)	SA*/NY/TEC/TAB	Und/< 20%	L	WORLDWIDE	McIntosh et al. (1969); Guerrero‐Sánchez et al. (2011)
		Ring‐necked dove (Streptopelia capicola)	SA*	Und	L	AFR	McIntosh et al. (1969)
		Eurasian collared‐dove (Streptopelia decaocto)	NY/CO	< 20%/< 20%	M	AM/EUR/AS/AFR	Panella et al. (2013)
		Laughing dove (Spilopelia senegalensis)	SA*/EGY	Und/< 20%	L	AFR/AS	Work et al. (1955), McIntosh et al. (1969)
		Common ground‐dove (Columbina passerina)	NY	Und	na	AM	Reisen et al. (2006, 2008)
		Mourning dove (Zenaida macroura)	NY	< 20%	M	AM	Komar et al. (2003), Reisen et al. (2005, 2006)
		Picui ground‐dove (Columbina picui)	ARG	< 20%	M	AM	Diaz et al. (2011)
Gruiformes	Rallidae	American coot (Fulica americana)	NY	< 20%	L	AM	Komar et al. (2003)
		Crested coot (Fulica cristata)	SA*	Und	L	AFR/EUR	McIntosh et al. (1969)
	Gruidae	Sandhill crane (Grus canadensis)	NY	< 20%	L	AM	Olsen et al. (2009)
Anseriformes	Anatidae	Common goose (Anser anser)	SA*	> 50%	M	WORLDWIDE	Banet‐Noach et al. (2003)
		Canada goose (Branta canadensis)	NY	< 20%	M	AM/EUR	Komar et al. (2003)
		Mallard (Anas platyrhynchos)	NY	< 20%	H	WORLDWIDE	Komar et al. (2003)
		Yellow‐billed duck (Anas undulata)	SA*	Und	L	AFR	McIntosh et al. (1969)
		Red‐billed teal (Anas erythrorhyncha)	SA*	Und	L	AFR	McIntosh et al. (1969)
		Southern pochard (Netta erythrophthalma)	SA*	Und	L	AFR	McIntosh et al. (1969)
Charadriiformes	Charadriidae	Killdeer (Charadrius vociferus)	NY	< 20%	H	AM	Komar et al. (2003)
	Laridae	Ring‐billed gull (Larus delawarensis)	NY	> 50%	H	AM	Komar et al. (2003)
Psittaciformes	Psittacidae	Monk parakeet (Myiopsitta monachus)	NY	< 20%	L	AM	Komar et al. (2003)
		Budgerigar (Melopsittacus undulatus)	NY	< 20%	L	OCE	Komar et al. (2003)
Piciformes	Picidae	Northern flicker (Colaptes auratus)	NY	< 20%	M	AM	Komar et al. (2003)

CA: California 04; NY: New York 99; CO: Colorado 08; SA: South Africa; ARG: Argentina 06; EGY: Egypt; KUN: Kunjin; SP: Spain 07; MO: Morocco 03; AUS: Austria 09; MEX: Mexico 03; TEX: Texas 03; KEN: Kenya 3829; FR: France 00; ISR: Israel 98; TEC: Tecato (Mexico); TAB: Tabasco (Mexico); IT08: Italy 08; IT09: Italy 09.* Lineage 2.

L: Low viraemia (mean peak viraemia ≤ 104 PFU/mL); M: Medium viraemia (mean peak viraemia 104–106 PFU/mL); H: High viraemia (mean peak viraemia > 106 PFU/mL); na: Data not available.

AFR: Africa; AM: America; AS: Asia; EUR: Europe; OCE: Oceania.

Und: Undetermined.

Parameter 4 – Experimentally susceptible domestic species (or family/orders)

Table A.4 in Appendix A lists the outcomes of experimental infections of WNV performed in domestic animal species. Infections have been successfully established in cats, dogs, horses, pigs, rabbits and sheep.

Table A.4.

Summary outcomes of systematic review of experimental infections of domestic animals with WNV (papers published up to January 2016)

Species	References	Number of animal groupsa	Agent detectionb		Observation of clinical signsc		Clinical signs (and number of groups in which were reported)
			Min day	Max day	Min day	Max day
Cats	Austgen et al. (2004)	3 (19 animals)	Virus isolation from blood: 1 (0.5–3)	Virus isolation from blood: 7 (4.5–8)	1	6	No clinical signs observed (2), fever (1), depression/apathy (1)
							0 dead animals
Dogs	Austgen et al. (2004), Karaca et al. (2005)	2 (19 animals)	Virus isolation from blood: 1.3 (0.5–2)	Virus isolation from blood: 5.3 (4.5–6)	1	1	No clinical signs observed (1), fever (1)
							0 dead animals
Horses	Bunning et al. (2002), Shirafuji et al. (2009), Castillo‐Olivares et al. (2011)	4 (17 animals)	Virus isolation from blood (3 groups): 3(1–4)	Virus isolation from blood (3 groups): 6 (6–7)	6.5 (3–8)	10 (9–11)	No clinical signs observed (1), twitching/tremors (1), neurological signs (2), fever (1)
			PCR from blood (1 group): 3	PCR from blood (1 group): 7			1 dead animal in 1 group
Pigs	Teehee et al. (2005)	2 (12 animals)	Virus isolation from blood: 1.5 (1.5–4.5)	Virus isolation from blood: 5 (4.5–5)	Not reported		No clinical signs observed (1), not reported (1)
							0 dead animals
Rabbits	Suen et al. (2015)	2 (27 animals)	Not reported		1	Not reported	No clinical signs observed (1), fever (1)
							0 dead animals
Sheep	Barnard and Voges (1986)	1 (2 animals)	Virus isolation from blood: 3	Virus isolation from blood: 11	3	3	Fever

^all data were analysed at animal group level, reflecting the animal groups followed and reported in the individual references. Some references reported more than one animal group.

^bMin = first day (in dpi) that pathogen/RNA was detected in a sample for each reported animal group; Max = last day (in dpi) that virus/RNA was detected in a sample for each reported animal group. Min and Max were recorded individually for each animal group, and median (min‐max) for each of those values were calculated from all group data (each group representing one observation, with no weighting based on the size of the animal groups). Contact transmission groups were not included in the summary.

^cMin = first day (in dpi) in which clinical signs were observed in each whole animal group reported; Max = last day (in dpi) in which clinical signs were observed in each whole animal group reported. Min and Max were recorded individually for each animal group, and median (min‐max) for each of those values were calculated from all group data (each group representing one observation, with no weighting based on the size of the animal groups). Contact transmission groups were not included in the summary.

Reservoir animal species

Parameter 5 – Wild reservoir species (or family/orders)

Several bird species, particularly passerine species (jays, finches, sparrows, and crows) can be potential reservoirs of WNV. House finches (Carpodacus mexicanus) and house sparrows (Passer domesticus) experimentally inoculated showed persistent infection in spleen and kidney 28 weeks p.i. (post infection). The virus was still detected by real time reverse transcription polymerase chain reaction (RT‐PCR) in the spleen of two house sparrows at 36 weeks p.i. However, viral isolation attempts were unsuccessful (Wheeler et al., 2012). In a previous work (Nemeth et al., 2009a), a higher number of organs were analysed in WNV‐infected house sparrows, and viral RNA was detected in juvenile sparrows up to 65 days p.i in kidney and spleen, although infectious virus could be isolated at low titres only in one sparrow at 43 days p.i. Reisen et al. (2006) confirmed the persistent infection in five species of Passeriformes and in common ground‐dove (Columbina passerina) detecting the virus in spleen and kidney, but also in lungs at > 6 weeks p.i. (Reisen et al., 2006).

Outside the United States of America (USA), clinical symptoms signs due to WNV infection have been reported in few cases and limited to scarce number of avian species in course of outbreaks: domestic geese (Anser anser domesticus) and white storks (Ciconia ciconia) during the WNV epidemic in Israel (Malkinson et al., 2002), goshawks (Accipiter gentilis) in Hungary (Bakonyi et al., 2006), Eurasian jays (Garrulus glandarius), little owl (Athene noctua), mallard (Anas plathyrynchos), and common buzzard (Buteo buteo) in Italy (Monaco et al., 2015). However, mass mortality of highly susceptible species (such as corvids or other species) is less frequently observed in the Old than in the New World although some species, as the jackdaws (Corvus monedula) could potentially function as sentinel (Lim et al., 2014). Surveillance activities carried out in Italy where WNV is endemic since 2008, pointed out the high susceptibility to the viral infection of three species of synantropic resident wild birds, namely carrion crow (Corvus corone), magpie (Pica pica) and Eurasian jay (Garrulus glandarius) which justifies their use as sentinel in endemic areas (Italian Ministry of Health, 2016).

Some species of mammals including squirrels (Sciurus sp.), eastern chipmunks (Tamias striatus) and eastern cottontail rabbits (Sylvilagus floridanus) may be capable of transmitting WNV to mosquitoes, although their epidemiological role importance as reservoir hosts is still uncertain.

Among reptiles, clinical signs were mainly reported during outbreaks in alligators, although there is also a report on neurological signs associated with WNV infection in a crocodile monitor (Varanus salvadori) lizard. Some infections in garter snakes (Thamnophis sirtalis) experimentally inoculated with WNV were also fatal. Green iguanas (Iguana iguana) can be infected.

Amphibians including lake frogs (Rana ridibunda) and North American bullfrogs (Rana catesbeiana) can also be infected with WNV. Some alligators (e.g. American alligators, Alligator mississippiensis) and frogs (e.g. Rana ridibunda in Russia) may develop viraemia sufficient to infect mosquitoes. As with mammals, their epidemiological importance as reservoir hosts is still uncertain.

Based on preliminary research carried out in Italy and Spain, only a few bird species seem to play a major role in the transmission of infection to the mosquitoes (Hamer et al., 2009; Munoz et al., 2012; Roiz et al., 2012; Spedicato et al., 2016). Unfortunately, the reservoir competence for many European bird species is still unknown even though the persistence of WNV in infected birds has been assessed in some species through experimental trials. Table B.1 in Appendix B provides an overview of wild and domestic WNV reservoir/sentinel animal species.

Table B.1.

List of wild and domestic WNV reservoir/sentinel animal species

Family	Reservoir	Sentinel	Notes
Turdidae	ND	Y	Intense viraemia and clinical signs developed by infected birds
Corvidae	Potential	Y	Intense viraemia and clinical signs developed by the infected birds with high mortality
Passeridae	Y	Y	Intense and long viraemia and clinical signs developed by infected birds
Anatidae	–	Y	Intense viraemia and clinical signs developed by infected birds
Columbidae	Y	–	Common ground‐dove (Columbina passerina): WNV detection in spleen and kidney and lung at > 6 weeks p.i
Fringillidae	Y	–	Persistent infection in house finches (Haemorhous mexicanus)
Falconidae	–	Y	Intense viraemia and clinical signs developed by infected birds
Phasianidae	–	Y	Viraemia short and scarce, asymptomatic infection, detectable serological response
Laridae	–	Y	Intense viraemia and clinical signs developed by infected birds
Strigidae		Y	Intense viraemia and clinical signs developed by infected birds
Equidae	–	Y	Viraemia short and scarce, development of clinical symptoms, detectable serological response
Canidae	–	Potential	Viraemia short and scarce, rare development of clinical symptoms, detectable serological response. Potential use as sentinel in urban areas
Felidae	–	Potential	Viraemia short and scarce, rare development of clinical symptoms, detectable serological response. Potential use as sentinel in urban areas

Parameter 6 – Domestic reservoir species (or family/orders)

WNV has been associated with sporadic disease infection in small numbers of domestic animal species (see above in parameter 2 and Table A.2 in Appendix A); however, these species do not play a role in the further transmission of WNV to mosquitoes and are thus considered as dead‐end hosts. See also Table B.1 in Appendix B which lists wild and domestic WNV reservoir/sentinel animal species.

3.1.1.2. Article 7(a)(ii) The morbidity and mortality rates of the disease in animal populations

Parameter 1 – Prevalence/incidence

WNV has been found in all the continents from tropical to north temperate latitudes (Reisen, 2013). Table 1 lists the number of horses positive for WNV detections (either by immunoglobulin M enzyme‐linked immunosorbent assay (IgM‐ELISA) or PCR), reported to the Animal Diseases Notification System since between (ADNS) 2013 and 2016.

Table 1.

Number of horses positive for WNV reported to the ADNS

Country	Year	Number of positive horses
France	2015	46
Italy	2013	43
Italy	2014	19
Italy	2015	31
Italy	2016	53
Greece	2013	15
Greece	2014	4
Spain	2013	37
Spain	2014	12
Spain	2015	17
Spain	2016	79
Portugal	2015	9
Portugal	2016	6
Austria	2016	1
Hungary	2013	1
Hungary	2014	1
Hungary	2015	7
Hungary	2016	49
Bulgaria	2015	1

Source: Animal Diseases Notification System (2013–2016).

Table C.1 in Appendix C summarises the prevalence of cases reported to the OIE in Europe, namely in Portugal, Spain, France, Croatia, Greece, Romania, Former Yugoslav Republic of Macedonia and Bulgaria. Also, the cases in Italy reported to the Italian authorities are summarised in Table C.1.

Table C.1.

WNV morbidity and mortality rates in horses (2010–2016 EU outbreaks)

Outbreaks in equids
Country	Year	No outbreaks	No outbreaks with clinical symptoms	No horses present	No total cases	No horses with symptoms	Died/culled	Prevalence of infection	Case‐morbidity rate	Case‐fatality rate
Italy	2008	273	18	1,941	563	32	5	29%	2%	1%
	2009	137	32	1,398	223	37	9	16%	3%	24%
	2010	67	11	415	128	11	5	31%	3%	45%
	2011	91	41	881	197	58	14	22%	7%	24%
	2012	30	13	313	63	15	3	20%	24%	20%
	2013	35	11	308	50	12	1	16%	24%	8%
	2014	17	6	257	27	6	2	11%	22%	33%
	2015	26	6	302	30	6	5	10%	20%	17%
	2016a	33	13	310	37	13	4	7%	35%	11%
Portugal	2016	1	1	2	1	1	0	50%	50%	0%
	2015	3	3	82	4	4	0	5%	5%	0%
	2010	2	2	71	2	2	1	3%	3%	1%
Spain	2011	5	Unknown	44	11	Unknown	1	25%	Unknown	9%
	2010	31	2	845	39	2	2	4%	0%	5%
France	2015	35	26	262	49	34	5	19%	13%	0–5,26%
	2006	4	1	63	4	1	1	6%	2%	25%
Croatia	2014	1	0	2	1	0	0	50%	0%	0%
	2012	11	0	87	12	0	0	14%	0%	0%
Greece	2014	4	0	51	4	0	0	8%	0%	0%
	2013	10	2	559	15	2	1	3%	0%	7%
	2012	14	3	100	15	3	0	15%	3%	0%
	2011	17	0	374	23	0	1b	6%	0%	0%
	2010	27	3	559	30	3	3	5%	1%	10%
Romania	2010	3	Unknown	9	6	Unknown	0	67%	Unknown	Unknown
Former Yugoslav Republic of Macedonia	2011	4	0	51	10	0	0	20%	0%	0%
Bulgaria	2010	2	0	118	8	0	0	7%	0%	0%

^a2016 Italian data: updated to 14 October 2016.

^bDeath may have been the result of conditions other than West Nile virus infection (possible snake bite reported).

Source: Italian National information system and (OIE, online).

Parameter 2 – Case‐morbidity rate (% clinically diseased animals out of infected ones)

WNF can cause disease in horses, several species of birds and rarely in other species such as camels, dogs, cats, sheep, squirrels and alligators (Go et al., 2014; Hubalek et al., 2014). In horses, the majority of the infections are asymptomatic, but some individuals (about 10%) can develop severe neurological illness (ataxia, weakness, recumbency and muscle fasciculation). Experimental infections have shown that the clinical picture of the disease can be quite divergent depending on the species. High susceptible species (e.g. corvids) can develop an hyperacute phase resulting in death without exhibiting symptoms, whereas other species (e.g. raptors, owls, Passeriformes) can develop only mild lesions with low mortality rates or chronic disease (Pérez‐Ramírez et al., 2014). The case‐morbidity rate in the outbreaks reported to the OIE and the Italian National Authorities are shown in Table C.1 in Appendix C.

Parameter 3 – Case‐fatality rate

The case‐fatality rate in the outbreaks in equids reported to the OIE and the Italian National Authorities are shown in Table C.1 in Appendix C.

LaDeau et al. (2007) demonstrated that the American crow population declined by up to 45% since WNV arrival in 1999 and only two of the seven species with documented impact recovered to pre‐WNV levels by 2005 (LaDeau et al., 2007).

3.1.1.3. Article 7(a)(iii) The zoonotic character of the disease

Presence

Parameter 1 – Report of zoonotic human cases (anywhere)

WNV zoonotic transmission is known to be present in Europe for many years: in the 1960s, the virus emerged in southern France in the Camargue. Yet, the first large outbreak in humans was reported from Bucharest, Romania in 1996–1997. Up to 2010, infection in humans and/or horses have been reported in the Czech Republic (1997), France (2000, 2003, 2004, 2006), Italy (1998, 2008, 2009), Hungary (2000–2009), Romania (1997–2001, 2003–2009), Spain (2004) and Portugal (2004). In 2010, a human outbreak was reported in northern Greece, and human cases were reported in Romania, Hungary, Italy, Spain and in Volgograd (Russian Federation). The number of human cases notified in Europe and in the Mediterranean Basin since 2010 is reported in Table 5.

3.1.1.4. Article 7(a)(iv) The resistance to treatments, including antimicrobial resistance

Parameter 1 – Resistant strain to any treatment even at laboratory level

This is not applicable to WNV since there is no specific antiviral therapy.

3.1.1.5. Article 7(a)(v) The persistence of the disease in an animal population or the environment

Animal population

Parameter 1 – Duration of infectious period in animals

Viral titres in blood equal or greater than 10⁵ TCID₅₀/mL have been considered able to infect competent mosquito species. In relation to viraemia duration, the following results of experimental infections in European bird species are reported:

Parameter 2 – Presence and duration of latent infection period

Evidence of persistent WNV infection has been demonstrated in experimentally infected monkeys (Pogodina et al., 1983) and hamsters (Tesh et al., 2005). WNV is also capable of long‐term persistence in human patients, particularly in the presence of chronic clinical symptoms (Murray et al., 2010). The importance of these persistent infections, however, needs still to be elucidated, as virus titres are low and these hosts are considered to be dead‐end hosts.

Parameter 3 – Presence and duration of the pathogen in healthy carriers

Refer to the data reported in Section 3.1.1.1 parameter 5.

Environment

Parameter 4 – Length of survival (dpi) of the agent and/or detection of DNA in selected matrices (soil, water, air) from the environment (scenarios: high and low T)

WNV is rapidly inactivated in the environment outside hosts. Low temperatures preserve infectivity, with stability being greatest below −60°C. It is inactivated by heat (50–60°C for at least 30 min), ultraviolet light, and gamma irradiation (Burke and Monath, 2001). The virus is also susceptible to disinfectants such as 3–8% formaldehyde, 2% glutaraldehyde, 2–3% hydrogen peroxide, 500–5,000 ppm available chlorine, alcohol, 1% iodine and phenol iodophors.

Data related to the persistence of the virus in the vectors are provided in Table 3.

Table 3.

Detailed outcomes of systematic review on survival time of WNV in mosquitoes at different temperatures (data extracted from (Turell et al., 2002))

Matrix	Target	Test	Temperatures	Maximum detection
Mosquito	Nucleic acid	RT‐PCR	4°, 20°, 70°C	14 days
Mosquito	Virus	Culture	4°, 20°, 70°C	2 days

RT‐PCR: reverse transcription polymerase chain reaction.

3.1.1.6. Article 7(a)(vi) The routes and speed of transmission of the disease between animals, and, when relevant, between animals and humans

Routes of transmission

WNV is maintained in nature by a primary cycle of transmission mosquito–bird–mosquito (endemic cycle): adult ornithophilic mosquitoes (vectors) become infected by biting viraemic birds (amplifying hosts). A secondary cycle (epidemic cycle) is characterised by the involvement in the transmission cycle of accidental hosts such as horses and humans due to particular ecological conditions. In this case, arthropod vectors, called bridge vectors, are able to transmit the virus to hosts other than birds, such as horses and humans. Humans, equids and other mammals are considered to be dead‐end accidental hosts. In these hosts, the virus does not reach a concentration in the bloodstream high enough to infect vectors, so the transmission cycle is not perpetuated. In Europe, the transmission cycle of WNV can be restricted to two main ecosystems: the rural (sylvatic) cycle, which occurs near wet/marshy areas between wild birds and ornithophilic mosquitoes, and the synanthropic/urban cycle, which arises between synanthropic or domestic birds and mosquitoes which can feed on the blood of birds and humans.

WNF vectors are mosquitos belonging to the Culex, Aedes and Coquillettidia genera (family Culicidae) (link to storymap VBD: https://efsa.maps.arcgis.com/apps/MapJournal/index.html?appid=512a03aa8df84d54a51bcb69d1b62735) (EFSA AHAW Panel, 2017b).

Parameter 1 – Types of routes of transmission from animal to animal (horizontal, vertical)

Results of experimental trials on WNV transmission routes in wild birds are summarised in Table 4 and Table A.3 in Appendix A.

Table 4.

Experimental data on WNV transmission in wild birds

Direct	Indirecta	Horizontal	Vertical	Species	Reference
C	Y	Y	NT	American crow (Corvus brachyrhynchos)	Komar et al. (2003)
C	Y	Y	NT	Blue jay (Cyanocitta cristata)	Komar et al. (2003)
C	Y	Y	NT	Black‐billed magpie (Pica hudsonia)	Komar et al. (2003)
C	Y	Y	NT	Ring‐billed gull (Larus delawarensis)	Komar et al. (2003)
C	Y	Y	N	Chicken (Gallus gallus domesticus)b	Langevin et al. (2001)
C	NT	Y	N	Domestic geese (Anser anser domesticus)	Swayne et al. (2001)
C	NT		NT	Common goose (Anser anser domesticus)	Banet‐Noach et al. (2003)
C	NT	Y	NT	Red‐legged partridge (Alectoris rufa)	Sotelo et al. (2011b)
NT	Y	NT	NT	Canada goose (Branta canadensis)	Komar et al. (2003)
N	Y	N	NT	Mallard (Anas platyrhynchos)	Komar et al. (2003)
O	Y	Y	NT	American kestrel (Falco sparverius)	Komar et al. (2003) (C); Nemeth et al. (2006a) (O)
N	Y	N	NT	Northern bobwhite (Colinus virginianus)	Komar et al. (2003)
N	Y	N	NT	Japanese quail (Coturnix japonicus)	Komar et al. (2003)
NT	Y	NT	NT	Ring‐necked pheasant (Phasianus colchicus)	Komar et al. (2003)
N	Y	N	NT	American coot (Fulica americana)	Komar et al. (2003)
NT	Y	NT	NT	Killdeer (Charadrius vociferus)	Komar et al. (2003)
N	Y	N	NT	Mourning dove (Zenaida macroura)	Komar et al. (2003)
N	Y	N	NT	Rock dove (Columba livia)	Komar et al. (2003)
N	Y	N	NT	Monk parakeet (Myiopsitta monachus)	Komar et al. (2003)
N	Y	N	NT	Budgerigar (Melopsittacus undulatus)	Komar et al. (2003)
O	Y	Y	NT	Great horned owl (Bubo virginianus)	Komar et al. (2003) (C); Nemeth et al. (2006a) (O)
NT	Y	NT	NT	Northern flicker (Colaptes auratus)	Komar et al. (2003)
N	Y	N	NT	Fish crow (Corvus ossifragus)	Komar et al. (2003)
N	Y	N	NT	American robin (Turdus migratorius)	Komar et al. (2003)
N	Y	N	NT	European starling (Sturnus vulgaris)	Komar et al. (2003)
NT	Y	NT	NT	Red‐winged blackbird (Agelaius phoeniceus)	Komar et al. (2003)
N	Y	N	NT	Common grackle (Quiscalus quiscula)	Komar et al. (2003)
N	Y	N	NT	House finch (Carpodacus mexicanus)	Komar et al. (2003)
N	Y	N	NT	House sparrow (Passer domesticus)	Komar et al. (2003)
N	NT	N	NT	Red‐tailed hawk (Buteo jamaicensis)	Nemeth et al. (2006a)
N	NT	N	NT	Song sparrow (Melopiza melodia)	Reisen and Fang (2007)
O	NT	Y	NT	Eastern screech owls (Megascops asio)	Nemeth et al. (2006b)

C: Contact transmission; O: oral transmission; N: no evidence of direct transmission; NT: not tested.

^aMosquitoes‐exposed.

^bOnly 1 animal in 16 in contact hens.

Mosquito bites are the usual source of WNV for mammals, reptiles and amphibians; however, in some animals, there is also evidence for transmission by other routes. Carnivorous mammals and reptiles (e.g. cats and alligators) can be infected by eating contaminated tissues. Direct transmission during close contact has also been reported in alligators, possibly via faecal shedding of virus. Chipmunks, squirrels and raccoons can also shed WNV in faeces, oral secretions and/or urine. WNV has been found in the urine of experimentally infected hamsters, and in very small amounts in the oral and/or cloacal fluids of experimentally infected North American bullfrogs (Rana catesbeiana) and green iguanas (Iguana iguana). Transplacental transmission was reported in experimentally infected sheep and mice, as well as in a horse that was fatally infected with a Lineage 1 virus in Africa, and aborted in the final stage of the disease. The epidemiological significance (if any) of mammalian, reptilian and amphibian hosts in the maintenance or amplification of WNV remains to be established.

Parameter 2 – Types of routes of transmission between animals and humans (direct, indirect, including food‐borne)

There is no evidence of natural direct transmission between vertebrates and humans. However, human infections from the exposure of conjunctival membranes (Fonseca et al., 2005) and/or percutaneous injury to the body fluids or tissues of WNV‐infected birds (CDC, 2002) have been described.

Speed of transmission

Transmission rate of WNV infection between vector (mosquito) and avian population has been expressed through the calculation of the basic reproduction number (R₀) by using different mathematical models. In the EU context, Calistri et al. (2016) developed a transitional mathematical model to calculate the R₀ values for the various part of the Italian territory from May to September, which resulted in a mean R₀ value for the whole Italy varying between 0.4 and 4.8, with values > 1 from the end of May to the beginning of September.

3.1.1.7. Article 7(a)(vii) The absence or presence and distribution of the disease in the Union, and, where the disease is not present in the Union, the risk of its introduction into the Union

Presence and distribution

Parameter 2 – Type of epidemiological occurrence (sporadic, epidemic, endemic) at MS level

WNV introduction and circulation have been demonstrated on multiple occasions in southern Europe and in the Mediterranean basin since the 1960s when seropositive animals or virus isolates were discovered in France, Portugal and Cyprus (Filipe and Pinto, 1969; Joubert et al., 1970). Migratory birds have been associated with the introduction of viral strains from endemic areas (Calistri et al., 2010); however, the mechanism of virus persistence in animal hosts in Europe leading to endemicity of the infection is still unknown.

In Europe, WNV circulation was mainly detected in the Mediterranean and south‐eastern regions, where notifications of human and horses cases of WNV infection have increased in the last 5–7 years, with the involvement of new areas, where the infection was not notified before, such as Bulgaria and Greece in 2010, Albania and Former Yugoslav Republic of Macedonia in 2011, and Croatia, Serbia and Kosovo in 2012. Accordingly, alarming outbreaks were reported in several European countries in 2010; 261 confirmed human cases, including 34 deaths, occurred in Greece, 57 cases and five deaths occurred in Romania, and 480 cases and six deaths occurred in Russia (Papa et al., 2010; Onishchenko et al., 2011; Sirbu et al., 2011).

Sporadic occurrence of the disease has been reported in France since 1962, when it first appeared in Camargue. In the same region, WNV was detected in 2000, 2004 and, after a ten‐year period, in 2015 (Bahuon et al., 2016).

In Italy, WNV annual epidemics have been consistently registered since 2008 (Savini et al., 2008) caused by genetically divergent isolates and, to date, WNV is considered endemic in the north‐eastern regions of the country, in Sardinia and in Sicily (Italian Ministry of Health, 2016).

The geographic distribution of West Nile cases in Europe and in Mediterranean Basin from 2008 to 2016 shown in Figure 1.

Figure 1.

Geographic distribution of cases (confirmed and probable) of West Nile fever in Europe and in Mediterranean Basin (2008–2016) (source Arbozoonet: https://arbozoonet.izs.it/arbozoonet (ArboZoonet, online))

Risk of introduction

Data are not provided since the disease is already present in the Union. It should be noted, however, that a continuous introduction from Africa through migratory birds is suspected.

3.1.1.8. Article 7(a)(viii) The existence of diagnostic and disease control tools

Diagnostic tools

Parameter 1 – Existence of diagnostic tools

Details concerning the different types of diagnostic tools and their accuracy are listed in Table 7 in Section 3.1.4.1.

Table 7.

Diagnostic tests for WNV

Test	Target	Se	Sp	Matrix	Reference	Notes
NS1‐antigen protein microarray	Antibodies	95%	100%	Serum	Cleton et al. (in press)	Differential diagnosis of flavivirus infections in horses
Real‐time RT‐PCR	Antigen	From 1.5 to 15 copies per reaction	100%	Viral strains, human samples (cerebrospinal fluid, biopsies, serum and plasma) and mosquito pools	Vázquez et al. (2016)	Specificity evaluated using viral RNA from a panel of different flaviviruses and other encephalitic viruses belonging to several viral families
Real‐time RT‐PCR	Antigen	80 genome copies	100%	Viral strains Lineages 1 and 2	Faggioni et al. (2014)	Specificity evaluated using TBE, Usutu, Dengue 1, Dengue 4, YF, JEV
SYBR Green I‐based real‐time RT‐PCR	Antigen	20 copies	100%	Human serum/plasma	Kumar et al. (2014)	Specificity evaluated using DEN‐1–4, JEV, YFV, SLEV
Antigen capture ELISA	Antigen	90%	98%	Human serum	Saxena et al. (2013)	Detection of NS1 antigen
Real‐time RT‐PCR	Antigen	10 copies	100%	Viral strains	Barros et al. (2013)	Detection and differentiation between WNV and JEV; specificity evaluated using DEN‐1–4, JEV, YFV, ZIKAV, Ntaya, TBEV, USUV, Toscana, CHIKV
Real‐time RT‐PCR	Antigen	1.26 TCID50/ml for WNV‐L1, 6.3 TCID50/ml for WNV‐L2	100%	Tissue, feathers, oropharyngeal and cloacal swabs and blood from wild birds, samples from mice infected experimentally	Del Amo et al. (2013)	Detection and differentiation between WNV and USUV; specificity evaluated using SLEV, MVEV, JEV, BAGV, DEN‐1, TBEV, VEEV, VSV, AIV, EIV, NDV, AHS4
Competitive ELISA	Antibodies	100%	Wild birds: 79.5% compared to VNT	Sera from mammals and wild birds	Sotelo et al. (2011a)
			Horses: 96.5% compared to VNT
			South african mammals: 79.5% compared to HAI
			Giraffes: 67% compared to HAI
IgM capture ELISA	Antibodies	91.7%	99.2%	Horse sera	Long et al. (2006)
Real‐time RT‐PCR	Antigen	2–4 genome copies of WNV	100%	Viral strains	Eiden et al. (2010)	In OIE manual. For simultaneous detection and differentiation of WNV Lineage 1 and Lineage 2. Specificity evaluated using TBEV, YFV, JEV
Nested RT‐PCR	Antigen	10–8.0/100 μL	ND	Equine brain, blood, and cerebrospinal fluid; avian brain tissues	Johnson et al. (2001)	In OIE manual
Real‐time RT‐PCR	Antigen	0.1 PFU	100%	Human serum, CSF, brain tissue, mosquito pools, and avian tissues	Lanciotti et al. (2000)	In OIE manual. Specificity evaluated using DEN‐2, JEV, YFV, SLEV, Lacrosse virus, Powassan virus, MVE, WEEV, EEEV

RT‐PCR: reverse transcriptase polymerase chain reaction; IgM: immunoglobulin M; ELISA: enzyme linked immunosorbent assay; PFU: plaque‐forming unit.

Viral nucleic acid and viral antigens can be demonstrated in tissues of infected animals by RT‐PCR and immuno‐histochemistry, respectively.

Antibodies can be detected in equine serum by IgM capture ELISA, haemagglutination inhibition (HI), IgG ELISA, plaque reduction neutralisation (PRN) or virus neutralisation (VN). In some serological assays, antibody cross‐reactions with related flaviviruses, such as St. Louis encephalitis virus, Usutu virus, Japanese encephalitis virus or tick‐borne encephalitis (TBE) virus may be encountered.

According to the OIE, the following tests are suitable methods for confirmation of clinical cases: Nested RT‐PCR, real time RT‐PCR and IgM capture ELISA. The PRN and serum neutralisation tests are both suitable methods for detecting prevalence of infection, population freedom from infection and immune status in animals post‐vaccination (Table 7).

Equine WNV‐specific IgM antibodies are usually detectable from 7–10 days to 1–2 months post‐infection. Most of horses with WNV encephalitis test positive in the IgM capture ELISA at the time that clinical signs are first observed. WNV neutralising antibodies are detectable in equine serum by 2 weeks post‐infection and can persist for more than 1 year.

Several PCR methods are available as commercial kits. In view of the continued evolution and possible emergence of new WNV strains, it is important that the designs of PCR tests are constantly monitored and updated when necessary.

Control tools

Parameter 2 – Existence of control tools

In areas where the disease is endemic, horses may be protected from the clinical signs by vaccination (Table 7). In the infected areas, however, strategies aiming at reducing the circulation of the virus through the reduction of mosquito density (reduction/treatment of stagnant water, adulticidal and larvicidal targeted treatments) and of contacts between vectors and receptive hosts (application of repellent, mosquito netting, etc.) are the bases of any control policy for mosquito‐borne diseases. Among biocidal products, the use of pyrethrin (6%) and piperonyl butoxide (60%) by aerial spray, indicated that the odds of infection after spraying were around six times higher in the untreated area than in treated areas, and that the treatments successfully disrupted the WNV transmission cycle (Carney et al., 2008).

3.1.2. Article 7(b) The impact of diseases

3.1.2.1. Article 7(b)(i) The impact of the disease on agricultural and aquaculture production and other parts of the economy

The level of presence of the disease in the Union

Parameter 1 – Number of MSs where the disease is present

Since the beginning of the 2016 transmission season, the presence of WNV has been confirmed in MSs and neighbouring countries. As of 27 October 2016, 205 human cases of WNF have been reported in the EU and 261 cases in the neighbouring countries (Austria, Croatia, Cyprus, Egypt, Hungary, Italy, Israel, Portugal, Romania, Russian Federation, Serbia, Spain and Syrian Arab republic, Tunisia, Ukraine) (ECDC, 2016).

The loss of production due to the disease

Parameter 2 – Proportion of production losses (%) by epidemic/endemic situation

In European outbreaks, WNV has not been associated with any mortality in domestic birds but has been connected to a few cases in wild birds (see Section 3.1.1.1).

3.1.2.2. Article 7(b)(ii) The impact of the disease on human health

Transmissibility between animals and humans

Table 5.

Number of cases (confirmed and probable) of West Nile fever in Europe and in Mediterranean Basin (updated to 2 December 2016)

Country	Year	Species	No. total casesa	No. confirmed casesb	Source
Albania	2011	Human	2		ECDC (online)
Algeria	2012	Human	1	1	ECDC (online)
Austria	2016	Human	2	2	ECDC (online)
	2015	Human	3	3
	2014	Human	1	1
Bosnia and Herzegovina	2014	Human	13	0	ECDC (online)
	2013	Human	3	3
Bulgaria	2016	Human	1	1	ECDC (online)
	2015	Human	2	0
Croatia	2016	Human	1	0	ECDC (online)
	2013	Human	16	1	ECDC (online)
	2012	Human	5	3	ECDC (online)
	2013	Horses	–	12	OIE (online)
Cyprus	2016	Human	1	1	ECDC (online)
Egypt	2016	Human	1	1	ECDC (online)
France	2015	Human	1	1	ECDC (online)
Former Yugoslav Republic of Macedonia	2013	Human	1		ECDC (online)
	2012	Human	6	1
Greece	2014	Human	15	13	HCDCP (online)
	2014	Horses	4	4	OIE (online)
	2013	Human	86	58	HCDCP (online)
	2013	Horses	–	15	OIE (online)
	2012	Human	161	47	HCDCP (online)
	2012	Horses	–	15	OIE (online)
	2011	Human	101	–	HCDCP (online)
	2011	Horses	23	–	OIE (online)
	2010	Human	261	–	HCDCP (online)
	2010	Horses	30	–	OIE (online)
Hungary	2016	Human	39	16	ECDC (online)
	2015	Human	18	13	ECDC (online)
	2014	Human	11	3	ECDC (online)
	2013	Human	31	6	ECDC (online)
	2012	Human	12	7	ECDC (online)
	2011	Human	3	–	ECDC (online)
	2010	Human	3	–	ECDC (online)
Israel	2016	Human	80	47	ECDC (online)
	2015	Human	123	89
	2014	Human	17	7
	2013	Human	63	28
	2012	Human	59	31
	2011	Human	39	–
Italy	2016	Human	71	71	ISS (online)
	2016	Horses	51	51	IZSAM (online)
	2015	Human	61	61	ISS (online)
	2015	Horses	30	30	IZSAM (online)
	2014	Human	24	24	ISS (online)
	2014	Horses	27	27	IZSAM (online)
	2013	Human	70	70	ISS (online)
	2013	Horses	–	50	IZSAM (online)
	2012	Human	50	39	ISS (online)
	2012	Horses	–	63	IZSAM (online)
	2011	Human	–	15	ISS (online)
	2011	Horses	197	–	IZSAM (online)
Kosovo	2012	Human	4	0	ECDC (online)
Former Yugoslav Republic of Macedonia	2011	Human	4	–	ECDC (online)
	2011	Horses	10	–	OIE (online)
Montenegro	2013	Human	4	–	ECDC (online)
	2012	Human	1	1
Morocco	2010	Horses	25	–	OIE (online)
Palestine	2014	Human	1	1	ECDC (online)
	2012	Human	2	1
Portugal	2016	Horses	1	1	OIE (online)
	2015	Human	1	1	ECDC (online)
	2015	Horses	4	4	OIE (online)
Romania	2016	Human	93	80	ECDC (online)
	2015	Human	18	18	ECDC (online)
	2014	Human	23	22	ECDC (online)
	2013	Human	24	22	ECDC (online)
	2012	Human	14	13	ECDC (online)
	2011	Human	11	–	ECDC (online)
	2010	Human	52	–	Sirbu et al. (2011)
	2010	Horses	6	–	OIE (online)
Russian Federation	2016	Human	135	135	ECDC (online)
	2015	Human	39	39	ECDC (online)
	2014	Human	29	–	ECDC (online)
	2013	Human	177	–	ECDC (online)
	2012	Human	447	–	ECDC (online)
	2011	Human	153	–	ECDC (online)
	2010	Human	480	–	Promed (online)
Serbia	2016	Human	41	41	ECDC (online)
	2015	Human	28	28
	2014	Human	76	56
	2013	Human	302	200
	2012	Human	70	41
Spain	2016	Human	3	3	Andalucía Ministry of Agriculture (online)
	2016	Horses	70	70
	2015	Horses	18	18
	2013	Horses	40	–
	2011	Horses	12	–
Syrian Arab Republic	2016	Human	2	1	ECDC (online)
Tunisia	2016	Human	1	1	ECDC (online)
	2015	Horses	1	1	OIE (online)
	2013	Human	6	6	ECDC (online)
	2012	Human	63	33	ECDC (online)
	2011	Human	3	–	ECDC (online)
Turkey	2014	Horses	1	1	OIE (online)
	2011	Human	3	–	ECDC (online)
	2010	Human	7	–	ECDC (online)
Ukraine	2016	Human	1	0	ECDC (online)
	2013	Human	1	–
	2012	Human	12	–
	2011	Human	8	–

^aFor EU countries, probable and confirmed cases as per EU case definition (Commission Decision 2008/426/EC1).

^bFor EU countries, confirmed cases as per EU case definition (Commission Decision 2008/426/EC).

Transmissibility between humans

WNV is most commonly transmitted to humans by mosquitoes but additional routes of human‐to‐human transmission have also been documented as blood transfusions, organ transplants, exposure in a laboratory setting or the transmission from the mother to baby during pregnancy, delivery or breastfeeding. It is important to note that these methods of transmission represent a very small proportion of cases thus sufficient to evoke only a sporadic occurrence of the disease.

Humans are dead‐end hosts since are not able to infect mosquitoes during the viraemic phase of the infection. Thus, the above‐mentioned routes of direct transmission represent the main risk of infection dissemination among community. Laboratory acquired infections have also been reported (Campbell et al., 2002).

Parameter 3 – Human to human transmission is sufficient to sustain sporadic cases or community‐level outbreak

WNV transmission through blood transfusion and organ transplantation is able to sustain community‐level outbreak.

Parameter 4 – Sporadic, endemic, epidemic, or pandemic potential

Neuroinvasive human cases are usually sporadic, occurring mainly in immunocompromised persons or elderly.

The severity of human forms of the disease

Parameter 5 – Disability‐adjusted life year (DALY)

Human infections are mostly asymptomatic. However, in some cases, they can exhibit a mild form of the disease (less than 1%) with encephalitis, meningoencephalitis or meningitis mainly among elderly or immunosupressed individuals (Go et al., 2014). As for most arthropod‐borne diseases causing fever syndromes worldwide, the cumulative impact of WNV on global disease burden has not been fully assessed. Evaluations should include both the severe forms of the disease and the milder clinical manifestations which may result in neurological and ophthalmologic complications (Carson et al., 2006). WNV has been recognised able to induce a wide range of post‐infection, long‐term sequelae with the recovery of the affected patients within two years from the infection (Murray et al., 2008). However, a recent paper has emphasised that 40% of WNV‐infected patients continued to experience symptoms related to their WNV infection up to 8 years later demonstrating the health and economic impact of a result of prolonged recovery, continued morbidity, and related disability (Murray et al., 2014).

The availability of effective prevention or medical treatment in humans

Parameter 6 – Availability of medical treatment and their effectiveness (therapeutic effect and any resistance)

There is no specific recommended treatment, other than supportive care, at present. Intensive care and mechanical ventilation may be required in some cases. Various therapies including interferon, antisense nucleotides and intravenous immunoglobulins (passive immunisation) are being tested in clinical trials. While a few case reports suggest that some of these treatments may be promising, larger studies are still lacking. Screening for new drugs that may inhibit WNV is underway.

Parameter 7 – Availability of vaccines and their effectiveness (reduced morbidity)

There are no vaccines available for human use in EU.

3.1.2.3. Article 7(b)(iii) The impact of the disease on animal welfare

Parameter 1 – Severity of clinical signs at case level and related level and duration of impairment

The incubation period for equine WNV encephalitis following mosquito transmission is estimated to be 3–15 days. A fleeting viraemia of low virus titre precedes clinical onset (Bunning et al., 2002). WNV encephalitis occurs in only a small per cent of infected horses; the majority of infected horses do not display clinical signs (Ostlund et al., 2000). The disease in horses is frequently characterised by mild to severe ataxia. Additionally, horses may exhibit weakness, muscle fasciculation and cranial nerve deficits (Cantile et al., 2000; Ostlund et al., 2000, 2001; Snook et al., 2001). Fever is an inconsistently recognised feature. Treatment is supportive and signs may resolve or progress to terminal recumbency. The mortality rate is approximately one out of three neurologically affected horses.

Many species of birds can become infected with WNV; the clinical outcome of infection is variable. Some species appear resistant while others suffer fatal neurologic disease. WNV infection associated with severe clinical signs have been described in several species of European wild birds (Bakonyi et al., 2006; Hofle et al., 2008; Jimenez‐Clavero et al., 2008; Monaco et al., 2015).

3.1.2.4. Article 7(b)(iv) The impact of the disease on biodiversity and the environment

Biodiversity

Parameter 1 – Endangered wild species affected: listed species as in CITES and/or IUCN list

CITES (online)

• Phoenicopteridae spp. (App. II)

• Falco rusticolus (App. I)

• Aquila adalberti (App. I)

• Falconiformes spp. (App. II)

Parameter 2 – Mortality in wild species

A number of outbreaks have been reported recently in Europe, Russia and parts of the Middle East. Since 2004, one introduced Lineage 2 virus in Central Europe has affected significant numbers of wild and captive raptors (Erdélyi et al., 2007). Therefore, the potential for WNV to cause illness or deaths in other European birds should be re‐examined. Some virus lineages seem to have become endemic and are spreading (CFSPH, 2013). Species known to be susceptible to this isolate include sparrow hawks (Accipiter nisus), goshawks (Accipiter gentilis) and gyrfalcons (Falco rusticolus). The same virus was isolated from a dead collared dove (Streptopelia decaocto) in Italy, during an outbreak characterised by observed of mortality in collared doves and other species, including blackbirds. Different lineages of the WNV have also been found occasionally in other dead birds including European robins (Erithacus rubecula), raven (Corvus corax), common magpies (Pica pica), Eurasian jay (Garrulus glandarius), house sparrows (Passer domesticus), black redstart (Phoenicurus ochruros), sedge warbler (Acrocephalus schoenobaenus) and Savi's warbler (Locustella luscinioides).

LaDeau et al. (2007) demonstrated a high impact on the abundance of seven species of North American wild birds after the emergence of WNV in 1999. Host susceptibility, spatio‐temporal heterogeneity in pathogen transmission and other environmental impacts on populations were accounted for using Bayesian modelling techniques. These seven species included two members of the family Corvidae (American crow and blue jay), two from Turdidae (American robin and eastern bluebird), two from Paridae (chickadees and tufted titmouse) and one from Troglodytidae (house wren). Also, George et al. (2015) demonstrated significant negative effects on survival of 47–49% bird species in North America, using an extensive capture‐recapture technique study of nearly two decades, combined with recently developed models of WNV risk (George et al., 2015). The authors suggested that WNV in the US has a significant persistent effect on wild bird populations long after initial concerns had stopped.

3.1.3. Article 7(c) Its potential to generate a crisis situation and its potential use in bioterrorism

Parameter 1 – Listed in OIE/CFSPH classification of pathogens

WNV is listed in the CDC list of potential bioterrorism agents.

Parameter 2 – Listed in the Encyclopaedia of Bioterrorism Defence of Australia Group

WNV is not listed in the Encyclopaedia of Bioterrorism Defence of Australia Group.

Parameter 3 – Included in any other list of potential bio‐ agro‐terrorism agents

WNV is not reported in any other list of potential bio‐agro‐terrorism agents.

3.1.4. Article 7(d) The feasibility, availability and effectiveness of the following disease prevention and control measures

3.1.4.1. Article 7(d)(i) Diagnostic tools and capacities

Availability

Parameter 1 – Officially/internationally recognised diagnostic tool, OIE certified

Table 6.

Test methods available for the diagnosis of WNV and their purpose (Source: (OIE, 2013))

Method	Purpose
	Population freedom from infection	Individual animal freedom from infection	Confirmation of clinical signs	Prevalence of infection	Immune status in individual animals or populations post‐vaccination
Agent identification
Nested RT‐PCR	–	**	**	–	–
Real‐time RT‐PCR	–	**	**	–	–
Isolation in tissue culture	–	**	**	–	–
Detection of immune response
IGM capture ELISA	–	–	**	–
Plague reduction neutralisation	**	–	*	**	**
Serum neutralisation	**	–	*	**	**
Immunohistochemistry	–	–	*	–

*** = recommended method; ** = suitable method; * = may be used in some situations, but cost reliability, or other factors severity limits its application; – = not appropriate for this purpose.

Although not all of the rests listed as category *** have undergone formal validation, their routine nature and the fact that they have been used widely without dubious results, makes them acceptable.

RT‐PCR: reverse transcriptase polymerase chain reaction; IgM: immunoglobulin M; ELISA: enzyme linked immunosorbent assay.

Effectiveness

Parameter 2 – Se and Sp of diagnostic test

Diagnostic tests, their type, accuracy and basis for WNF diagnosis are listed in Table 7.

Feasibility

Parameter 3 – Type of sample matrix to be tested (blood, tissue, etc.)

See Table 7.

3.1.4.2. Article 7(d)(ii) Vaccination

WNV vaccines approved by EMA are listed in Table 8.

Table 8.

Vaccines for horses authorised for commercialisation in the EU by the European Medicines Agency (updated in October 2016) and their efficacy as emerged from a systematic review (updated to January 2016)

Commercial name of vaccine	Type of vaccine	Way of administration	Doses	Species for which authorised	Countries in which authorised	Manufacturer	Efficacy	Field protection	Yearly availability production capacity	Ref.
Proteq West Nile	West Nile recombinant canarypox virus, vCP2017 virus	IM		Horses	All EU	Merial	NA	NA	NA
Equilis West Nile	Inactivated chimaeric flavivirus strain YF‐WN	IM		Horses	All EU	Intervet International BV	NA	NA	NA
Equip WNV (previously Duvaxyn WNV)	Inactivated West Nile virus, strain VM‐2	IM	2 doses (21 days apart)	Horses	All EU	Zoetis Belgium SA	Viruses could be isolated from 8 out of 10 non‐vaccinated animals up to 14 days after challenge, but only 1 vaccinated animals. Sixty per cent of the controls had to be euthanised after challenge compared to none of the vaccinates. From 10 non‐vaccinated animals, all presented, up to 21 days after challenge, pyrexia, head tremors or muscle fasciculations, and anxiety, and 9 showed mild paresis. In controls, these numbers were 2, 2, 6 and 2, respectively	Experimental trial	NA	Bowen et al. (2014)

NA: data not available; IM: intramuscular.

3.1.4.3. Article 7(d)(iii) Medical treatments

There is no specific recommended treatment, other than supportive care, at present.

3.1.4.4. Article 7(d)(iv) Biosecurity measures

The biosecurity measures aiming at reducing the WNV spread are focused on controlling the vectors primarily responsible for the viral transmission. Farm‐to‐farm movement of infected horses is not effective to spread the disease since they are neither able to transmit the virus to biting mosquitoes nor, directly, to vertebrates including humans.

To minimise the possibilities of contact between the vectors and receptive hosts, it is advisable to use mosquito nets to avoid the vector entrance in the stables as well as the use of repellents on the animals. Data related to the efficacy of these substances has been detailed in Section 3.1.5.4 parameter 1.

To prevent any inter‐human spread, the screening of blood and organs for transplantation in areas with WNV circulation is a common measure.

3.1.4.5. Article 7(d)(v) Restrictions on the movement of animals and products

No specific measures are mentioned in the EU legislation for WNV outbreak control.

3.1.4.6. Article 7(d)(vi) Killing of animals

No specific measures are mentioned in the EU legislation for WNV outbreak control.

3.1.4.7. Article 7(d)(vii) Disposal of carcasses and other relevant animal by‐products

No specific measures are mentioned in the EU legislation for WNV outbreak control.

3.1.5. Article 7(e) The impact of disease prevention and control measures

3.1.5.1. Article 7(e)(i) The direct and indirect costs for the affected sectors and the economy as a whole

The major impact of WNV on animal health in the EU ecosystem is limited to the development of clinical signs in horses and, to date, there are no reports of clinical illness in domestic bird species. Thus, the major costs of WNV control in animals, namely horses, should include:

1. the cost of vaccination: primary vaccination consists of two doses, the second dose being administered 3–6 weeks later, depending on the vaccine used;

2. the cost to prevent mosquitoes bites: keeping horses indoor is not be very effective against Culex pipiens if additional measures such as mosquito nets or fans are not installed, as these mosquitoes are also active indoors. The use of insecticides or repellents is also able to reduce the possibilities for contact between the vectors and receptive hosts. Control of vectors can be recommended to individuals and to public health authorities in case of a severe epidemic, but the associated costs are difficult to estimate since emergency aerial spraying, even if proven to be effective in reducing mosquito populations and the number of human cases of WNV infection in the US (Barber et al., 2010), would not be the first option of vector control in MSs, given the substantial environmental risks and not easily accepted by the population (Humblet et al., 2016).

3. the costs of active surveillance activities, which may vary considerably between MSs. Usually animal surveillance encompasses domestic solipeds (horses and donkeys), birds and other animal species (e.g. cattle and farmed deer), as well as entomological surveillance activities. The main objective of the surveillance in humans during the transmission period is to ensure an immediate response in the implementation of the blood safety measures and the prevention of human cases, and, on an annual basis, to improve and adapt the surveillance and strengthen the preparedness.

4. WNV RNA screening of all blood donors in areas where the WNV circulation is in place. As an example in Italy during the 2015 epidemics, a total of 316,614 WNV NAT screening tests were conducted in blood donors in the affected provinces and 13 asymptomatic infected donors, were identified. No donor or organ transplant recipients were positive for WNV among the 168 tested.

3.1.5.2. Article 7(e)(ii) The societal acceptance of disease prevention and control measures

The control of the mosquito population through the intensive use of biocidal products, e.g. by aerial spray is not easily accepted by the population (Humblet et al., 2016).

3.1.5.3. Article 7(e)(iii) The welfare of affected subpopulations of kept and wild animals

Parameter 1 – Welfare impact of control measures on domestic animals

Since no specific measures are mentioned in the EU legislation for the WNV outbreak control, there is no impact on the welfare of domestic animals of official control measures.

Parameter 2 – Wildlife depopulation as control measure

Wild bird depopulation is not a control measure applied in course of WNV outbreak and its efficacy, as emerged from epidemiological models, not ascertained since the potential reduction of bird densities could enhance WNV transmission (Wonham et al., 2004).

3.1.5.4. Article 7(e)(iv) The environment and biodiversity

Environment

Parameter 1 – Use and potential residuals of biocides or medical drugs in environmental compartments (soil, water, feed, manure)

In WNV‐infected areas strategies must be implemented to reduce the circulation of the virus through measures that modify the density of the vectors (reduction of stagnant water, performance of adulticidal and larvicidal treatments) and to reduce the possibilities of contact between the vectors and receptive hosts (application of repellent, mosquito netting, etc.). Among biocidal products, the use of pyrethrin (6%) and piperonyl butoxide (60%) by aerial spray indicated that the odds of infection after spraying were around 6 times higher in the untreated area than in treated areas, and that the treatments successfully disrupted the WNV transmission cycle (Carney et al., 2008). Since Cx. pipiens is considered to be the main vector of WNV in Europe a list of biocidal products targeting mosquito control are reported in Table 9.

Table 9.

Biocidal products targeting mosquito control (genus Culex), for which reports were found in a systematic review of available treatments against the vectors of vector‐borne infections (papers published up to January 2016)

Active substance	Reference	Intended use (route investigated in the study)	Study findings
Studies not targeting any particular host
Deltamethrin	Marcombe et al. (2011)	Fogging	Efficacy was assessed by monitoring mortality rates of naturally resistant and laboratory susceptible mosquitoes placed in sentinel cages. Results showed high mortality rates of susceptible sentinel mosquitoes (64%) while resistant mosquitoes exhibited very low mortality (10%)
		Vehicle‐mounted thermal foggers (1 g/ha)
Studies focused on vector control in housing/environment
Deltamethrin	Akogbéto et al. (2010)	Indoor spraying	Deterrence ratea: Anopheles gambiae (31.25%, 24.75%, 30 and 60 dpt; Culex sp. and Mansonia sp. 30 dpt 46.15%)
		Huts were treated with insecticides. The absorption of the walls was 112 mL of insecticide per m2 and that of the ceiling (polyethylene), the entry slits, and the door (painted metal) was in total 53.13 mL/m2	Exophily rateb: Anopheles gambiae (45.4%, 26.3%, 30 and 60 dpt; Culex sp. and Mansonia sp. 30 dpt 33.3%)
			Blood‐feeding ratec: Anopheles gambiae (18.2%, 23.7%, 30 and 60 dpt; Culex sp. and Mansonia sp. 30 dpt, 14.3%)
			Immediate mortalityd: Anopheles gambiae (32.7%, 15.8%, 30 and 60 dpt; Culex sp. and Mansonia sp. 30 dpt, 8.5%)
			Overall mortalitye: Anopheles gambiae (72.7%, 31.6%, 30 and 60 dpt; Culex sp. and Mansonia sp. 30 dpt, 21%)
Deltamethrin	Badolo et al. (2014)		Mortality of mosquitoes was 90.5 (86–94)% in unwashed nets (3 min exposure, 24‐h mortality), and remained above 90% after 5 washes. Average mortality after 10, 15 and 20 washes were 81 (75–86)%, 68.7 (63–75)% and 66.3 (60–72)%, respectively
Deltamethrin	Dabiré et al. (2006)	Treated mosquito nets	Mosquito entrance rate was 10‐fold higher in control houses than in houses with long lasting impregnated nets (LLINs) and there was no difference between the two tested net types. Among mosquitoes found in the houses, 36% were dead in LLIN houses compared to 0% in control houses. Blood feeding rate was 80% in control houses compared to 43% in LLIN houses. The type of net did not significantly impact any of these parameters
		Concentration of 55 mg/m2
Deltamethrin	Darriet et al. (2000)	Treated mosquito nets	The 24‐h mortality was 56% for Anopheles gambiae females, and 45% for Culex spp. females (compared to 4 and 6% in controls)
		Concentration of 25 mg/m2
Deltamethrin	Moosa‐Kazemi et al. (2007)	Treated mosquito nets	Recorded 24‐h‐mortality was 100% even after 9 months
		Concentrations of 25 mg/m2
Deltamethrin	Muller et al. (2002)	Treated mosquito nets	Mortality of mosquitoes was 97% in washed nets, and reduced to 84%, 54% and 7% after 6, 12 and 18 months (with respective average of times washed of 1.1, 1.9 and 3)
		Concentrations from 55 mg/m2 (unwashed) to 1.6 mg/m2 (18 months old and washed 3 times)
Deltamethrin	Van Roey et al. (2014)	Treated mosquito nets	A positive control (commercial product PermaNet® 2.0, 55 mg a.i./m2) was able to kill over 90% of mosquitoes (3 min exposure, 24‐h‐mortality) for up to 30 months, while the observed mortality with the experimental product (Netprotect®, 68 mg a.i./m2) was 85.7% after 12 months, and remained below 90%
		Concentrations of 55 and 68 mg/m2
Diflubenzuron	Cetin et al. (2006)	Septic tank water treatment	Recorded adult inhibition for Culex pipiens was always 100% in the first 2 weeks, for all concentrations tested, and remained at 100% for up to 4 weeks with 30 g/L, and 2 weeks with 10 g/L
		0.01, 0.02, and 0.03 mg (AI)/L, using a 25% wettable powder or a 4% granular formulation in wastewater tank
Lambda‐cyhalothrin	Okumu et al. (2012)	Indoor spraying	Mortality (24‐h mortality of Anopheles arabiensis) was 90% after 30 days but reduced to 35% after 60 days
		0.03 g/m2 sprayed on mud walls
Lambda‐cyhalothrin	Trout et al. (2007)	Outdoors Spraying	The reduction in Aedes albopictus in sites was of 89.5% compared to controls, and in laboratory bioassays exposing mosquitoes to treated leaves, mortality varies from 80% after 2 weeks, to 35% after 8 weeks. In contrast, Culex spp. were not reduced
		Mist (concentration of 62.52 mL/L) directly applied to vegetation in the backyard of houses, and other resting sites
Permethrin	Rozendaal et al. (1989)	Treated mosquito nets	Cotton cloth impregnated with permethrin at a rate of 0.5 g/m2 killed all Anopheles darlingi females exposed for 2 min, but after the material had been washed twice in soapy water the bioassay mortality fell to only 21.4%. Bioassays with Culex quinquefasciatus females showed that sprayed nets were less effective than nets impregnated by soaking (at equivalent dosages of 0.16–1.34 g/m2)
		Concentrations of 125–1,000 mg/m2
Permethrin	Soleimani‐Ahmadi et al. (2012)	Treated mosquito nets	Mortality of mosquitoes was 100% in the first 90 days, 92.4% (88–97) after 5 months, and reduced to 81.6% (75–88) after 9 months, and 72.3% (65–79) after 12 months
		The nets were blended with 1,000 mg a.i/m2 (2%, w/w), and final concentrations varied from 814 to 937 mg/m2
Studies focused on humans as the host species (personal protection)
DEET	Soonwera and Phasornkusolsill (2015)	External use – topic/spray	DEET was used as control when evaluating other (non‐ECHA approved) substances. The formulation gave protection for up to 182 min, and 98.5% protection from bites of Aedes aegypti and Culex quinquefasciatus
		DEET 20% (w/w), 0.1 mL applied on a 3 × 10 cm area on the ventral portion of the forearm
DEET	Gupta et al. (1987)	Treated clothes and topic applications of repellent, in different concentrations and combinations	The field trials were arranged in a four‐way factorial design which compared fabric types, permethrin treatment and repellent treatments over a 14‐h test period. The repellent formulations and the permethrin‐treated clothing used as one system provided better protection (81% mortality) than the repellent formulations or permethrin‐treated clothing used separately
DEET + permethrin	Mani et al. (1991)	External use – soap	Percentage repellency (reduction in biting rates) was 96% for Culex vishnui, 89.6% for Culex tritaeniorhynchus and 94.8% for Culex pseudouishnui
		Containing 20% DEET and 5% permethrin
Metofluthrin	Dame et al. (2014)	‘Clip‐on’ spatial repellent device	Efficacy in reduction of Anopheles quadrimaculatus, in 2 study years, compared to control, were 16% and 8%)
		31.20%	19% and 8% for Psorophora columbiae and 69% for Culex erraticus. Total mosquito reduction was 13%
Metofluthrin	Revay et al. (2013)	External use	Biting on the arms of volunteers was reduced by 96.28% for Ae. albopictus, and by 94.94% for Cx. pipiens
		‘Clip‐on’ metofluthrin (31.2%)

^aPercentage of reduction in the number of mosquitoes caught in treated hut relative to the number caught in the control hut.

^bPercentage of mosquitoes that have escaped the hut and have taken refuge in the veranda trap divided by the total number of mosquitoes collected in the hut.

^cPercentage of blood fed mosquitoes collected divided by the total of mosquitoes collected in veranda and hut.

^dPercentage of dead mosquitoes collected in the morning compared to total mosquitoes collected in the hut.

^eImmediate mortality plus delayed mortality recorded after 24 h.

Biodiversity

Parameter 2 – Mortality in wild species

The main risk may be represented by the environmental residual of biocides which may interfere with ecology of wild species.

3.2. Assessment according to Article 5 criteria

This section presents the results of the expert judgement on the criteria of Article 5 of the AHL about WNF (Table 10). The expert judgement was based on Individual and Collective Behavioural Aggregation (ICBA) approach described in detail in the opinion on the methodology (EFSA AHAW Panel, 2017a). Experts have been provided with information of the disease fact‐sheet mapped into Article 5 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or ‘na’ judgement on each criterion of Article 5, and the reasoning supporting their judgement.

Table 10.

Outcome of the expert judgement on the Article 5 criteria for West Nile fever

Criteria to be met by the disease: According to AHL, a disease shall be included in the list referred to in point (b) of paragraph 1 of Article 5 if it has been assessed in accordance with Article 7 and meets all of the following criteria		Final outcome
A(i)	The disease is transmissible	Y
A(ii)	Animal species are either susceptible to the disease or vectors and reservoirs thereof exist in the Union	Y
A(iii)	The disease causes negative effects on animal health or poses a risk to public health due to its zoonotic character	Y
A(iv)	Diagnostic tools are available for the disease	Y
A(v)	Risk‐mitigating measures and, where relevant, surveillance of the disease are effective and proportionate to the risks posed by the disease in the Union	Y
At least one criterion to be met by the disease: In addition to the criteria set out above at points A(i)‐A(v), the disease needs to fulfil at least one of the following criteria
B(i)	The disease causes or could cause significant negative effects in the Union on animal health, or poses or could pose a significant risk to public health due to its zoonotic character	Y
B(ii)	The disease agent has developed resistance to treatments and poses a significant danger to public and/or animal health in the Union	na
B(iii)	The disease causes or could cause a significant negative economic impact affecting agriculture or aquaculture production in the Union	N
B(iv)	The disease has the potential to generate a crisis or the disease agent could be used for the purpose of bioterrorism	NC
B(v)	The disease has or could have a significant negative impact on the environment, including biodiversity, of the Union	NC

Colour code: green = consensus (Yes/No); yellow = no consensus (NC); red = not applicable (na), i.e. insufficient evidence or not relevant to judge.

The minimum number of judges in the judgement was 12. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, 2017a). For details on the interpretation of the questions, see Appendix B of the methodological opinion (EFSA AHAW Panel, 2017a).

3.2.1. Non‐consensus questions

This section displays the assessment related to each criterion of Article 5 where no consensus was achieved in form of tables (Tables 11 and 12). The proportion of Y, N or na answers are reported, followed by the list of different supporting views for each answer.

Table 11.

Outcome of the expert judgement related to criterion 5 B(iv)

Question		Final outcome	Response
			Y (%)	N (%)	na (%)
B(iv)	The disease has the potential to generate a crisis or the disease agent could be used for the purpose of bioterrorism	NC	83	17	0

NC: non‐consensus; number of judges: 12.

Table 12.

Outcome of the expert judgement related to criterion 5 B(v)

Question		Final outcome	Response
			Y (%)	N (%)	na (%)
B(v)	The disease has or could have a significant negative impact on the environment, including biodiversity, of the Union	NC	82	18	0

NC: non‐consensus; number of judges: 11.

Reasoning supporting the judgement

Supporting Yes:

• It is listed in OIE/CFSPH, there is public concern on the disease and the potential to create a crisis.

• There have been examples of public health crisis in Romania in the 1990s, in Greece in 2010, in Hungary and Russia following outbreaks in humans.

• US army indicates that virulent genes could be modified to increase pathogenicity for humans and used as a weapon (since transmitted by mosquitoes).

• There were crisis in naïve areas, but not in endemic areas like France.

Supporting No:

• Some MSs do not have any WNV monitoring system in place, while others have been operating systems for several years, e.g. Italy and Greece. The main objective of the surveillance in humans during the transmission period is to ensure an immediate response in the implementation of the blood safety measures and the prevention of human cases, and, on an annual basis, to improve and adapt the surveillance and strengthen the preparedness. In Italy, for example, though the repeated and constant WNV circulation, surveillance on blood samples has been put in place and this also has not generated a crisis. Moreover, WNV circulation in France have not generated crisis.

• The situation in the US is not related with bioterrorism.

• Every virus could be genetically modified and become a threat, a worst‐case scenario exists for every disease and should not be considered here.

Reasoning supporting the judgement

Supporting Yes:

• The North American experience shows that there is the potential for significant impact on the biodiversity.

Supporting No:

• There is no report of an impact of WNF at population level on endangered species in EU.

3.2.2. Outcome of the assessment of West Nile fever according to criteria of Article 5(3) of the AHL on its eligibility to be listed

As from the legal text of the AHL, a disease is considered eligible to be listed as laid down in Article 5 if it fulfils all criteria of the first set from A(i) to A(v) and at least one of the second set of criteria from B(i) to B(v). According to the assessment methodology (EFSA AHAW Panel, 2017a), a criterion is considered fulfilled when the outcome is ‘Yes’. According to the results shown in Table 10, WNF complies with all criteria of the first set and with one criterion of the second set, therefore it is considered eligible to be listed as laid down in Article 5 of the AHL.

3.3. Assessment according to Article 9 criteria

This section presents the results of the expert judgement on the criteria of Annex IV referring to categories as in Article 9 of the AHL about WNF (Tables 11, 12, 15, 16 and 17). The expert judgement was based on ICBA approach described in detail in the opinion on the methodology. Experts have been provided with information of the disease fact‐sheet mapped into Article 9 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or ‘na’ judgement on each criterion of Article 9, and the reasoning supporting their judgement.

Table 15.

Outcome of the expert judgement related to the criteria of Section 3 of Annex IV (category C of Article 9) for West Nile fever

Criteria to be met by the disease: The disease needs to fulfil all of the following criteria		Final outcome
1	The disease is present in the whole OR part of the Union territory with an endemic character	Y
2.1	The disease is moderately to highly transmissible	Y
2.2	The disease is transmitted mainly by direct or indirect transmission	Y
2.3	The disease affects single or multiple species	Y
2.4	The disease usually does not result in high morbidity and has negligible or no mortality AND often the most observed effect of the disease is production loss	N
At least one criterion to be met by the disease: In addition to the criteria set out above at point 1–2.4, the disease needs to fulfil at least one of the following criteria
3	The disease has a zoonotic potential with significant consequences on public health, or possible significant threats to food safety	Y
4(CI)	The disease has a significant impact on the economy of parts of the Union, mainly related to its direct impact on certain types of animal production systems	N
4(PI)	The disease has a significant impact on the economy of parts of the Union, mainly related to its direct impact on certain types of animal production systems	N
5(a)(CI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(a)(PI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(b)(CI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	N
5(b)(PI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	NC
5(c)(CI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	N
5(c)(PI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	NC
5(d)(CI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	N
5(d)(PI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	NC

Colour code: green = consensus (Yes/No); yellow = no consensus (NC).

Table 16.

Outcome of the expert judgement related to the criteria of Section 4 of Annex IV (category D of Article 9) for West Nile fever

Criteria to be met by the disease: The disease needs to fulfil all of the following criteria		Final outcome
D	The risk posed by the disease in question can be effectively and proportionately mitigated by measures concerning movements of animals and products in order to prevent or limit its occurrence and spread	N
The disease fulfils criteria of Sections 1, 2, 3 or 5 of Annex IV of AHL		Y

Colour code: green = consensus (Yes/No).

Table 17.

Outcome of the expert judgement related to the criteria of Section 5 of Annex IV (category E of Article 9) for West Nile fever

Diseases in category E need to fulfil criteria of Sections 1, 2 or 3 of Annex IV of AHL and/or the following:		Final outcome
E	Surveillance of the disease is necessary for reasons relating to animal health, animal welfare, human health, the economy, society or the environment (If a disease fulfils the criteria as in Article 5, thus being eligible to be listed, consequently category E would apply.)	Y

Colour code: green = consensus (Yes/No).

The minimum number of judges in the judgement was 12. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, 2017a). For details on the interpretation of the questions, see Appendix B of the methodological opinion (EFSA AHAW Panel, 2017a).

Table 13.

Outcome of the expert judgement related to the criteria of Section 1 of Annex IV (category A of Article 9) for West Nile fever

Criteria to be met by the disease: The disease needs to fulfil all of the following criteria		Final outcome
1	The disease is not present in the territory of the Union OR present only in exceptional cases (irregular introductions) OR present in only in a very limited part of the territory of the Union	N
2.1	The disease is highly transmissible	N
2.2	There be possibilities of airborne or waterborne or vector‐borne spread	Y
2.3	The disease affects multiple species of kept and wild animals OR single species of kept animals of economic importance	Y
2.4	The disease may result in high morbidity and significant mortality rates	N
At least one criterion to be met by the disease: In addition to the criteria set out above at points 1–2.4, the disease needs to fulfil at least one of the following criteria
3	The disease has a zoonotic potential with significant consequences on public health, including epidemic or pandemic potential OR possible significant threats to food safety	N
4 (CI)	The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals	N
4 (PI)	The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals	N
5(a)(CI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(a)(PI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(b)(CI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	N
5(b)(PI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	NC
5(c)(CI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	N
5(c)(PI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	NC
5(d)(CI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	N
5(d)(PI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	NC

Colour code: green = consensus (Yes/No); yellow = no consensus (NC).

Table 14.

Outcome of the expert judgement related to the criteria of Section 2 of Annex IV (category B of Article 9) for West Nile fever

Criteria to be met by the disease: The disease needs to fulfil all of the following criteria		Final outcome
1	The disease is present in the whole OR part of the Union territory with an endemic character AND (at the same time) several Member States or zones of the Union are free of the disease	Y
2.1	The disease is moderately to highly transmissible	Y
2.2	There be possibilities of airborne or waterborne or vector‐borne spread	Y
2.3	The disease affects single or multiple species	Y
2.4	The disease may result in high morbidity with in general low mortality	Y
At least one criterion to be met by the disease: In addition to the criteria set out above at point 1–2.4, the disease needs to fulfil at least one of the following criteria
3	The disease has a zoonotic potential with significant consequences on public health, including epidemic potential OR possible significant threats to food safety	Y
4 (CI)	The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals	N
4 (PI)	The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals	N
5(a)(CI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(a)(PI)	The disease has a significant impact on society, with in particular an impact on labour markets	N
5(b)(CI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	N
5(b)(PI)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	NC
5(c)(CI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	N
5(c)(PI)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	NC
5(d)(CI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	N
5(d)(PI)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	NC

Colour code: green = consensus (Yes/No); yellow = no consensus (NC).

3.3.1. Non‐consensus questions

This section displays the assessment related to each criterion of Annex IV referring to the categories of Article 9 of the AHL where no consensus was achieved in form of tables (Tables 18, 19 and 20). The proportion of Y, N or ‘na’ answers are reported, followed by the list of different supporting views for each answer.

Table 18.

Outcome of the expert judgement related to criterion 5(b)(PI) of Article 9

Question		Final outcome	Response
			Y (%)	N (%)	na (%)
5(b)	The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals	NC	83	17	0

NC: non‐consensus; number of judges: 12.

Table 19.

Outcome of the expert judgement related to criterion 5(c)(PI) of Article 9

Question		Final outcome	Response
			Y (%)	N (%)	na (%)
5(c)	The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it	NC	58	0	42

NC: non‐consensus; number of judges: 12.

Table 20.

Outcome of the expert judgement related to criterion 5(d)(PI) of Article 9

Question		Final outcome	Response
			Y (%)	N (%)	na (%)
5(d)	The disease has a significant impact on a long‐term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long‐term damage to those species or breeds	NC	67	33	0

NC: non‐consensus; number of judges: 12.

Reasoning supporting the judgement

Supporting Yes:

• WNF may have a potential impact on animal health and consequently welfare if introduced in naive populations in the absence of controls.

• The percentage of affected horses with severe clinical signs undergoes a significant impact on animal welfare.

Supporting No:

• Currently, there is no significant impact on welfare although the virus is circulating in many countries. It could have a potential impact in naïve populations.

• Although there has been extensive geographical expansion of the European territories with WNV circulation, the number of clinical cases in horses remains very limited.

Reasoning supporting the judgement

Supporting Yes:

• The impact on wild birds could be potentially significant, if there was a substantial increase in outbreaks.

• Impacts of controls on the environment may be substantial.

• Supporting na:

• There are no data on the potential effect of vector control easures on the environment.

Reasoning supporting the judgement

Supporting Yes:

• There may be a potential impact, given the range of bird species potentially affected. Some endangered species of, e.g. prey birds could disappear or be seriously threatened.

• The emergence of WNV strains more virulent for wild birds can affect larger numbers of animals.

Supporting No:

• There is an impact on individual animals, but no long‐term effect on a population scale. Furthermore there are periodic epidemic outbreaks, but the probability of long‐term epidemics in wild fauna is low.

3.3.2. Outcome of the assessment of criteria in Annex IV for West Nile fever for the purpose of categorisation as in Article 9 of the AHL

As from the legal text of the AHL, a disease is considered fitting in a certain category (A, B, C, D or E corresponding to point (a) to point (e) of Article 9(1) of the AHL) if it is eligible to be listed for Union intervention as laid down in Article 5(3) and fulfils all criteria of the first set from 1 to 2.4 and at least one of the second set of criteria from 3 to 5(d) as shown in Tables 11–17. According to the assessment methodology (EFSA AHAW Panel, 2017a), a criterion is considered fulfilled when the outcome is ‘Yes’. With respect to different type of impact where the assessment is divided into current and potential impact, a criterion will be considered fulfilled if at least one of the two outcomes is ‘Y’ and, in case of no ‘Y’, the assessment is inconclusive if at least one outcome is ‘NC’.

A description of the outcome of the assessment of criteria in Annex IV for WNF for the purpose of categorisation as in Article 9 of the AHL is presented in Table 21.

Table 21.

Outcome of the assessment of criteria in Annex IV for WNF for the purpose of categorisation as in Article 9 of the AHL (CI = current impact; PI = potential impact)

Category	Article 9 criteria
	1° set of criteria					2° set of criteria
	1	2.1	2.2	2.3	2.4	3	4	5a	5b	5c	5d
	Geographical distribution	Transmissibility	Routes of transmission	Multiple species	Morbidity and mortality	Zoonotic potential	Impact on economy	Impact on society	Impact on animal welfare	Impact on environment	Impact on biodiversity
A	N	N	Y	Y	N	N	N	N	CI: N PI: NC	CI: N PI: NC	CI: N PI: NC
B	Y	Y	Y	Y	Y	Y	N	N	CI: N PI: NC	CI: N PI: NC	CI: N PI: NC
C	Y	Y	Y	Y	N	Y	N	N	CI: N PI: NC	CI: N PI: NC	CI: N PI: NC
D	N
E	Y

According to the assessment here performed, WNF complies with the following criteria of the Sections 1–5 of Annex IV of the AHL for the application of the disease prevention and control rules referred to in points (a)–(e) of Article 9(1):

1. To be assigned to category A, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment WNF complies with criteria 2.2 and 2.3, but not with 1, 2.1 and 2.4. To be eligible for category A, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and WNF does not comply with criteria 3, 4 and 5a and the assessment is inconclusive on compliance with criteria 5b, 5c and 5d.

2. To be assigned to category B, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment WNF complies with all of them. To be eligible for category B, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and WNF complies with criterion 3, but not with criteria 4 and 5a and the assessment is inconclusive on compliance with criteria 5b, 5c and 5d.

3. To be assigned to category C, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment WNF complies with criteria 1, 2.1, 2.2 and 2.3, but not with 2.4. To be eligible for category C, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and WNF complies with criterion 3, but not with criteria 4 and 5a and this assessment is inconclusive on compliance with criteria 5b, 5c and 5d.

4. To be assigned to category D, a disease needs to comply with criteria of Sections 1, 2, 3 or 5 of Annex IV of the AHL and with the specific criterion D of Section 4. WNF does not comply with the latter.

5. To be assigned to category E, a disease needs to comply with criteria of Sections 1, 2 or 3 of Annex IV of the AHL and/or the surveillance of the disease is necessary for reasons relating to animal health, animal welfare, human health, the economy, society or the environment. The latter is applicable if a disease fulfils the criteria as in Article 5, with which WNF complies.

3.4. Assessment of Article 8

This section presents the results of the assessment on the criteria of Article 8(3) of the AHL about WNF. The Article 8(3) criteria are about animal species to be listed, as it reads below:

‘3. Animal species or groups of animal species shall be added to this list if they are affected or if they pose a risk for the spread of a specific listed disease because:

1. they are susceptible for a specific listed disease or scientific evidence indicates that such susceptibility is likely; or

2. they are vector species or reservoirs for that disease, or scientific evidence indicates that such role is likely’.

For this reason the assessment on Article 8 criteria is based on the evidence as extrapolated from the relevant criteria of Article 7, i.e. the ones related to susceptible and reservoir species or routes of transmission, which cover also possible role of biological or mechanical vectors.2 According to the mapping, as presented in Table 5, Section 3.2 of the scientific opinion on the ad hoc methodology (EFSA AHAW Panel, 2017a), the main animal species to be listed for WNF according to the criteria of Article 8(3) are several species of birds and mammals, displayed in details in Table A.1 in Appendix A, as susceptible species. Several bird species belonging to the families of Corvidae, Passeridae and Fringillidae (order of Passeriformes) and to the family of Columbidae (order Columbiformes) can be considered reservoir species for WNV in Europe, details are shown in Table B.1 in Appendix B. The main vectors are some species of mosquitoes belonging to the genera Culex, Aedes and Coquillettidia (family Culicidae, order Diptera). The vector species are listed in https://efsa.maps.arcgis.com/apps/MapJournal/index.html?appid=512a03aa8df84d54a51bcb69d1b62735 (EFSA AHAW Panel, 2017b).

4. Conclusions

TOR 1: for each of those diseases an assessment, following the criteria laid down in Article 7 of the AHL, on its eligibility of being listed for Union intervention as laid down in Article 5(3) of the AHL;

• According to the assessment here performed, WNF complies with all criteria of the first set and with one criterion of the second set and therefore can be considered eligible to be listed for Union intervention as laid down in Article 5(3) of the AHL.

TOR 2a: for each of the diseases which was found eligible to be listed for Union intervention, an assessment of its compliance with each of the criteria in Annex IV to the AHL for the purpose of categorisation of diseases in accordance with Article 9 of the AHL;

• According to the assessment here performed, WNF meets the criteria as in Sections 2 and 5 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in points (b) and (e) of Article 9(1) of the AHL.

TOR 2b: for each of the diseases which was found eligible to be listed for Union intervention, a list of animal species that should be considered candidates for listing in accordance with Article 8 of the AHL.

• According to the assessment here performed, the animal species that can be considered to be listed for WNF according to Article 8(3) of the AHL are, as susceptible species, several orders of birds and mammals and two orders of reptiles, as reported in Table A.1 in Appendix A of the present document. Reservoirs are several bird species belonging to the families of Corvidae, Passeridae and Fringillidae (order of Passeriformes) and to the family of Columbidae (order Columbiformes). Vectors are some species of mosquitoes belonging to the genera Culex, Aedes and Coquillettidia (family Culicidae, order Diptera).

Abbreviations

ADNS

Animal Diseases Notification System

AHAW

EFSA Panel on Animal Health and Welfare

AHL

Animal Health Law

ALF

Alfuy

CDC

Centers for Disease Control and Prevention

CFSPH

Center for Food Security and Public Health

CITES

Convention on International Trade in Endangered Species of Wild Fauna and Flora

CPC

Cacipacore

DALY

disability‐adjusted life year

ECDC

European Centre for Disease Prevention and Control

ELISA

enzyme‐linked immunosorbent assay

HCDCP

Hellenic Center for Disease Control & Prevention

HI

haemagglutination inhibition

ICBA

Individual and Collective Behavioural Aggregation

IgG

immunoglobulin G

IgM

immunoglobulin M

ISS

Istituto Superiore di Sanità

IZSAM

Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise

IUCN

International Union for Conservation of Nature

KOU

Koutango

KUN

Kunjin

LLIN

long lasting impregnated net

MS

Member State

MVE

Murray Valley encephalitis

OIE

World Organisation for Animal Health

PCR

polymerase chain reaction

p.i.

post infection

PFU

plaque‐forming unit

PRN

plaque reduction neutralisation

RNA

ribonucleic acid

RT‐PCR

reverse transcription polymerase chain reaction

SLE

St. Louis encephalitis

TBE

tick‐borne encephalitis

TCID₅₀

tissue culture infective dose, median

ToR

Terms of Reference

USU

Usutu

VN

virus neutralisation

WNF

West Nile fever

WNV

West Nile virus

YAO

Yaounde

Supporting information

Mapped fact‐sheet used in the individual judgement on West Nile Fever

Suggested citation: EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare) , More S, Bøtner A, Butterworth A, Calistri P, Depner K, Edwards S, Garin‐Bastuji B, Good M, Gortázar Schmidt C, Michel V, Miranda MA, Nielsen SS, Raj M, Sihvonen L, Spoolder H, Stegeman JA, Thulke H‐H, Velarde A, Willeberg P, Winckler C, Baldinelli F, Broglia A, Dhollander S, Beltrán‐Beck B, Kohnle L, Morgado J and Bicout D, 2017. Scientific Opinion on the assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): West Nile fever. EFSA Journal 2017;15(8):4955, 51 pp. 10.2903/j.efsa.2017.4955