Abstract
Toxoplasma gondii infections are common in humans and animals worldwide. Wild and domestic avian species are important in the epidemiology of T. gondii infections because felids prey on them and excrete millions of oocysts in the environment, disseminating the infection. Herbivorous birds are also excellent sentinels of environmental contamination with T. gondii oocysts because they feed on the ground. Toxoplasma gondii infections in birds of prey reflect infections in intermediate hosts. Humans can become infected by consuming undercooked avian tissues. Here, the authors reviewed prevalence, persistence of infection, clinical disease, epidemiology and genetic diversity of T. gondii strains isolated from turkeys, geese, ducks, ratites and avian species (excluding chickens) worldwide 2009–2020. Genetic diversity of 102 T. gondii DNA samples isolated worldwide is discussed. The role of migratory birds in dissemination of T. gondii infection is discussed.
Key words: Birds, clinical disease, epidemiology, genotype, oocyst, prevalence, Toxoplasma gondii
Introduction
Toxoplasma gondii infections are prevalent in humans and animals worldwide. The ingestion of undercooked infected meat or consumption of food and water contaminated with oocysts excreted in cat feces are the main sources of infection. Cats are everywhere and a single cat can excrete millions of oocysts that can remain viable in the environment for months under natural conditions (Dubey, 2010). Estimation of oocyst contamination of the environment is difficult because of low numbers present in soil or water (Lélu et al., 2012). Wild and domestic birds are excellent sentinels of environmental contamination with T. gondii oocysts because herbivorous birds feed on the ground, and birds of prey consume hundreds of rodents and other small mammals yearly that are important intermediate hosts of T. gondii (Dubey et al., 2020; Iemmi et al., 2020). Migratory birds (penguins, geese and others) can transport the parasite across seas (Sandström et al., 2013). Some species (turkeys, geese, ducks and ostriches) are part of food supply for humans. A study estimated that billions of birds are consumed by cats yearly (Loss et al., 2013). Thus, there is great potential for the spread of T. gondii oocysts in the environment.
We recently reviewed the biology of T. gondii infections in chickens (Gallus domesticus) (Dubey et al., 2020). Here, T. gondii infections in other avian species, including domestic turkeys, ducks, geese, ratites and other avian species, are reviewed.
Turkeys (Meleagris gallopavo)
Antibodies to T. gondii were detected from 11.0 to 89.8% of turkeys surveyed (Table 1). Using a kinetic recombinant antigen (GRA7 and GRA8) ELISA, T. gondii antibodies were detected in 387 (20.2%) of 1913 sera from 14 turkey farms in different areas of Germany (Koethe et al., 2011). Seroprevalence varied greatly among farms and within the individual farms, depending on fattening cycles and season which turkeys were slaughtered. Seroprevalences were higher in turkeys slaughtered in summer vs in fall or winter (Koethe et al., 2011).
Table 1.
Country | Area | Source | No. tested | No. positive | % Positive | Test | Cut-off | Remarks | Reference |
---|---|---|---|---|---|---|---|---|---|
Brazil | Pernambuco | 28 Farms | 204 | 21 | 11.0 | MAT | 1:25 | Sá et al. (2016) | |
Egypt | Kafr El-Sheikh | Farms | 17 | 5 | 29.4 | IHAa | 1:80 | Harfoush and Tahoon (2010) | |
Germany | 5 States | 14 Farms, abattoirs | 1913 | 387 | 20.2 | ELISA-in house | 1:50 | Sex, season association | Koethe et al. (2011) |
Iran | Fars | FR, abattoir | 54 | 49 | 89.8 | MAT | 1:40 | T. gondii DNA and isolation | Sarkari et al. (2014) |
Iran | Shiraz | Farms, abattoir | 9 | 1 | 11.1 | MAT | 1:20 | Asgari et al. (2013) | |
Iraq | Ninevah | Farms | 107 | 82 | 76.6 | LATb | 1:20 | Butty (2009) | |
Nigeria | Ondo, Osun, Oyo | Farms | 320 | 13 | 4.1 | MAT | 1:20 | Sex association | Ayinmode et al. (2017) |
USA | Pennsylvania | Hunted | 20 | 6 | 30.0 | MAT | 1:5 | T. gondii isolated | Cerqueira-Cézar et al. (2019) |
ELISA, enzyme-linked immunosorbent assay; FR, free-range; IHA, indirect haemagglutination assay; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987).
IHA (Toxo-IHA Fumouze, Diagnostics, France).
LAT (Toxo latex kit from Bio-kit-SA, Barcelona, Spain).
A very high rate of infection was reported in a study from Iran (Sarkari et al., 2014). Antibodies to T. gondii were found in 89.8% of turkeys (Table 1) and T. gondii DNA was detected in 61.6% of turkey tissues (Table 2). Viable T. gondii was isolated from the muscle of 5 wild hunted turkeys in the USA (Table 3).
Table 2.
Host | Country | Location | No. tested | Tissues | No. isolated | Strain designation | PCR-RFLP genotype (Toxo DB) | Notes | Reference | |
---|---|---|---|---|---|---|---|---|---|---|
Accipitriformes | ||||||||||
Bald eagle (Haliaeetus leucocephalus) | USA | Alabama | 1 | B | 1 | TgBeAl | 1 genotype: #5 (1, TgBeA1) | Yu et al. (2013) | ||
Bald eagle (Haliaeetus leucocephalus) | USA | California | 5 | H | 1 | TgHlUs1 | 1 genotype: #1, Type II (1, TgHlUs1) | Dubey et al. (2011a), Shwab et al. (2014) | ||
Common buzzard (Buteo buteo) | Turkey | Seferihisar, Manisa | 25 | B, H | 9 | TgBirdTr_Izmir4,6,7 TgBirdTr_Manisa1-3,5-7 | Genotyped by microsatellites. 2 genotypes: Type II, ToxoDB #1 or #3 (6, TgBirdTr_Izmir4, TgBirdTr_Manisa2, TgBirdTr_Manisa3, TgBirdTr_Manisa6, TgBirdTr_Manisa7, TgBirdTr_Izmir7). Type III, ToxoDB #2 (1, TgBirdTr_Manisa1). Mixed types (2, TgBirdTr_Izmir6, TgBirdTr_Manisa5) | Karakavuk et al. (2018) | ||
Ferruginous hawk (Buteo regalis) | USA | Colorado | 7 | B, H | 1 | TgBrCoUs1 | 1 genotype: #1 (1, TgBrCoUs1) | Dubey et al. (2010) | ||
Red-shouldered hawk (Buteo lineatus) | USA | Alabama | 1 | B | 1 | TgRshAL | 1 genotype: #10, Type I (1, TgRshAL) | Yu et al. (2013) | ||
Red-tailed hawk (Buteo jamaicensis) | USA | Colorado | 25 | B, H | 1 | TgBjCoUs1 | 1 genotype: #1 (1, TgBjCoUs1) | Dubey et al. (2010) | ||
Red-tailed hawk (Buteo jamaicensis) | USA | Wisconsin | 1 | H | 1 | TgBjUS1 | 1 genotype: #15 (1, TgBjUS1) | Dubey et al. (2011a), Shwab et al. (2014) | ||
Roadside hawk (Rupornis magnirostris) | Brazil | Minas Gerais | 7 | B, H | 1 | TgWildBrMG1 | 1 genotype: #108 (1, TgWildBrMG1) | Rêgo et al. (2018) | ||
Rough-legged hawk (Buteo lagopus) | USA | Colorado | 4 | B, H | 1 | TgBlCoUs1 | 1 genotype: #2, Type III (1, TgBlCoUs1) | Dubey et al. (2010) | ||
Swainson's hawk (Buteo swainsoni) | USA | Colorado | 13 | B, H | 2 | TgBsCoUs1,2 | 2 genotypes: #1, Type II (1, TgBsCoUs2), #167 (1, TgBsCoUs1) | Dubey et al. (2010) | ||
Anseriformes | ||||||||||
Canada geese (Branta canadensis) | USA | Maryland | Hunted | H | 9 | TgGooseUS1-9 | 5 genotypes #1 (1, TgGooseUS9), #2 (4, TgGooseUS3,5,6,7), #4 (2, TgGooseUS2,8), #266 (1, TgGooseUS1), #267 (1, TgGooseUS4) | One isolate by bioassay in cat | Verma et al. (2016) | |
Domestic duck (unspecified) | China | Chongqing | 12 | B, H, K, Li, Lu, Sp | 1 | ND | PCR (ITS-1) | Zhao et al. (2015) | ||
Domestic duck (unspecified) | Malaysia | Peninsular | 23 | B, H | 4 | DK1-4 | PCR-RFLP-partial genotyping data | Backyards of homes | Puvanesuaran et al. (2013) | |
Mallard duck (Anas platyrhynchos) | France | Hunted | 2 | H | 1 | ND | Microsatellite markers, 1 genotype: type II, ToxoDB, #1 or #3 (1, one isolate) | Wild | Aubert et al. (2010) | |
Mallard duck (Anas platyrhynchos) | Malaysia | 4 states | 30 hunted | B, H | 4 | NS | ND | T. gondii DNA was detected by PCR-RFLP in tissues of inoculated mice | Puvanesuaran et al. (2013) | |
Mallard duck (Anas platyrhynchos) | Senegal | Saint-Louis | 1 | B, H | 1 | TgA117073 | Genotyped by 15 microsatellite markers as Type II ToxoDB #1 or #3 (1, TgA117073) | Galal et al. (2019) | ||
Muskovy duck (Cairina moschata) | Senegal | Dakar, Kedougou, Saint-Louis | 15 | B, H | 11 | TgA117015, 117017, 117018, 117025, 117032, 117038, 117041, 117054, 117060, 117061, 117070. | 12 strains genotyped with 15 microsatellites 4 genotypes: Type II, ToxoDB #1 or #3 (3, TgA117038, 117041, 117054), Type III, ToxoDB #2 (1, TgA117015), Africa 1, ToxoDB #6 (1, TgA117070), Africa 4, ToxoDB #20 (6, TgA117017, 177018, 177025, 177032, 177060, 117061). | Galal et al. (2019) | ||
Mute swan (Cygnus olor) | USA | Great lakes | 14 | H | 3 | TgSwanUs1-3 | 2 genotypes: #2 (2, TgSwanUs1,2), #216 (1, TgSwanUs3) | Dubey et al. (2013) | ||
Charadriiformes | ||||||||||
Yellow-legged gull (Larus michahellis) | Turkey | Balçova | 2 | B, H | 2 | TgBirdTr_Izmir2,3 | Genotyped by microsatellite. 2 genotypes: Type II, ToxoDB #1 or #3 (1, TgBirdTr_Izmir2). Type III, ToxoDB #2 (1, TgBirdTr_Izmir3) | Karakavuk et al. (2018) | ||
Columbiformes | ||||||||||
Eared dove (Zenaida auriculata) | Brazil | Paraná | 46 | Several tissues | 12 | TgDoveBr1-12 | Nine strains typed. 5 genotypes: #1 (4, TgDoveBr1,2,8,9), #6 (1, TgDoveBr7), #17 (1, TgDoveBr11), #65 (1, TgDoveBr12), #182 (2, TgDoveBr6,10) | de Barros et al. (2014) | ||
Rock pigeon (Columba livia) | Mexico | Durango | 7 | B, H | 1 | TgPigeonMx1 | PCR-RFLP ToxoDB genotype # 9 (1, TgPigeonMx1) | MAT 1:400 | Alvarado-Esquivel et al. (2011), Shwab et al. (2014) | |
Rock pigeon (Columba livia) | Portugal | Lisbon | 41 | B | 24 | NS | Genotyping by SAG2 (26 type II, two type III, one type I) and 5 microsatellites markers (12 type II, two type III, one type I and one recombinant) | Waap et al. (2012), Vilares et al. (2014) | ||
Rock pigeon (Columba livia) | Serbia | Belgrade | 4 | H | 3 | NS | 529 bp, PCR-RFLP-incomplete | Marković et al. (2014) | ||
Falconiformes | ||||||||||
American kestrel (Falco sparverius) | USA | Colorado | 5 | B, H | 1 | TgFsCoUs1 | 1 genotype: #157 (1, TgFsCoUs1) | Dubey et al. (2010) | ||
Southern caracara (Caracara plancus) | Brazil | Minas Gerais | 7 | B, H | 2 | TgWildBrMG4,6 | 2 genotypes: #13 (1, TgWildBrMG6) #290 (1, TgWildBrMG4) | Rêgo et al. (2018) | ||
Galliformes | ||||||||||
Double-spurred spurfowl (Pternistis bicalcaratus) | Senegal | Kedougou | 4 | B, H | 1 | TgA117077 | Genotyped with 15 microsatellites. 1 genotype: Africa 1, ToxoDB #6 (1, TgA117077) | Galal et al. (2019) | ||
Guinea fowl (Numida meleagris) | Brazil | Minas Gerais | 2 | B, H | 1 | TgNmBr1 | 1 genotype: # 1, type II (1, TgNmBr1) | Dubey et al. (2011b) | ||
Guinea fowl (Numida meleagris) | Senegal | Kedougou | 1 | B, H | 1 | TgA117058 | Genotyped with 15 microsatellites. 1 genotype: Type Africa 1, ToxoDB genotype #6 (1, TgA117058) | Galal et al. (2019) | ||
Turkeys (Meleagris gallopavo) | USA | Pennsylvania | 20 hunted | H, Sk | 5 | TgturkeyPa1-5 (designated here) | 2 genotypes: #5 (4, TgturkeyPa1-4), #216 (1, TgturkeyPa5) | 18NC0055- (TgturkeyPa1) 18-WITU-0002 (TgturkeyPa2) 18-WITU-0012 (TgturkeyPa3) 18-WITU-0015 (TgturkeyPa4) 18-WITU-0019 (TgturkeyPa5) | Cerqueira-Cézar et al. (2019) | |
Passeriformes | ||||||||||
Hawaiian crow (Corvus hawaiiensis) | USA | Hawaii | 2 | B, Li, Sp, Lu | 2 | TgHcUS1, 2 | 1 genotype: #177 (2, TgHcUS1, 2) | Work et al. (2000), Shwab et al. (2014) | ||
Pelecaniformes | ||||||||||
Striated heron (Butorides striata) | Brazil | Pernambuco | 2 | B, H, Sk | 1 | TgButstBrPE1 | 1 genotype: #13 (1, TgButstBrPE1) | Silva et al. (2018b) | ||
Piciformes | ||||||||||
Campo flicker (Colaptes campestris) | Brazil | Minas Gerais | 1 | B, H | 1 | TgWildBrMG3 | 1 genotype: #11 (1, TgWildBrMG3) | Rêgo et al. (2018) | ||
Keel-billed toucan (Ramphastos sulfuratus) | Costa Rica | Zoo | 1 | Sk | 1 | TgRsCr1 | 1 genotype: #52 (1, TgRsCr1) | Dubey et al. (2009), Shwab et al. (2014) | ||
Toco toucan (Ramphastos toco) | Brazil | Minas Gerais | 3 | B, H | 1 | TgWildBrMG2 | 1 genotype: #290 (1, TgWildBrMG2) | Rêgo et al. (2018) | ||
Psittaciformes | ||||||||||
Peach-Faced Lovebird (Agapornis roseicollis) | Australia | Sydney | 1 pet | B | 1 | AgapornisTg1 | 1 genotype: #3, Type II variant (1, AgapornisTg1) | T. gondii genotyping in B of the bird | Cooper et al. (2015) | |
Strigiformes | ||||||||||
Barn owl (Tyto alba) | Turkey | Konak | 2 | B, H | 2 | TgBirdTr_Izmir1,5 | Genotyped by microsatellites. 2 genotypes: Type II, ToxoDB #1 or #3 (1, TgBirdTr_Izmir5), Type III, ToxoDB #2 (1, TgBirdTr_Izmir1) | Karakavuk et al. (2018) | ||
Barn owl (Tyto alba) | USA | Colorado | 1 | B, H | 1 | TgTaCoUs1 | PCR-RFLP ToxoDB genotype # 5 | MAT<1:25 | Dubey et al. (2010) | |
Barred owl (Strix varia) | USA | Alabama | 1 | B | 1 | TgSaUS1 | 1 genotype: #3, Type II variant (1, TgSaUS1) | MAT 1:50 | Love et al. (2016) | |
Eurasian eagle-owl (Bubo bubo) | Turkey | Salihli | 2 | B, H | 1 | TgBirdTr_Manisa4 | Mixed types (1, TgBirdTr_Manisa4) | Karakavuk et al. (2018) | ||
Tropical screech owl (Megascops choliba) | Brazil | Minas Gerais | 4 | B, H | 1 | TgWildBrMG5 | 1 genotype: #8 (1, TgWildBrMG5) | Rêgo et al. (2018) | ||
Struthioniformes | ||||||||||
Ostrich (Struthio camelus) | Brazil | São Paulo | 38 | B | 14 | TgOsBr1,2 | 2 genotypes: # 161 (1, TgOsBr2), #206 (1, TgOsBr1) | Abattoirs | da Silva and Langoni (2016) | |
Suliformes | ||||||||||
Great cormorant (Phalacrocorax carbo) | Turkey | Çiğli | 1 | B, H | 1 | NS | ND | Karakavuk et al. (2018) |
B, brain; H, heart; K, kidney; Li, liver; Lu, lung; Sk, skeletal muscle; Sp, spleen; NS, not stated; ND, no data; PCR, polymerase chain reaction; PCR-RFLP, Restriction fragment length polymorphism.
Table 3.
Host | Country | Region | No. tested | Tissue | No. positive | % Positive | Remarks and PCR (gene) | Genotyping | Reference |
---|---|---|---|---|---|---|---|---|---|
Accipitriformes | |||||||||
Black kite (Milvus migrans) | Spain | Several | 3 | B | 1 | 33.3 | N-PCR (529 bp – TOX9,11 primers) | ND | Darwich et al. (2012) |
Common buzzard (Buteo buteo) | Turkey | Bergama, Bornova, Çiğli, Kemalpaşa, Konak, Manisa Salihli, Saruhanli, Seferihisar, Turgutlu | 25 | B, H | 23 | 92.0 | RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated | 15 Microsatellite markers – ToxoDB #1 or #3 in 6, #2 in 1 and mixed in 2 | Karakavuk et al. (2018) |
Eurasian sparrow hawk (Accipiter nisus) | Turkey | Bornova, Çiğli, Karabağlar, Salihli, Saruhanlı | 5 | B, H | 4 | 80.0 | RT-PCR, (529 bp – TOX-SE,AS primers). | Karakavuk et al. (2018) | |
Griffon vulture (Gyps fulvus) | Spain | Several | 105 | B | 1 | 0.9 | N-PCR (529 bp – TOX9,11 primers) | ND | Darwich et al. (2012) |
Anseriformes | |||||||||
Canada geese (Branta canadensis) Snow geese (Chen caerulescens) | Canada | Nunavik | 156 | B, G, H, Li, Sk | 14 | 9.0 | RT-PCR (529 bp – TOX9,11 primers), highest concentration of parasite DNA (tachyzoite equivalent) in H = 744, B = 300, Sk = 104, Li = 33, G = 8 | PCR-RFLP using GRA6 – type II | Bachand et al. (2019) |
Eurasian green-winged teal (Anas crecca) | Italy | NS | 8 | B, H | 5 | 62.5 | N-PCR (B1) | ND | Nardoni et al. (2019) |
Eurasian teal (Anas crecca) | Italy | Tuscany | 3 | B | 1 | 33.3 | N-PCR (B1) | 10 PCR-RFLP markers – genotype incomplete | Mancianti et al. (2013) |
Falcated teal (Falcated teal) | China | Jilin | 8 | H or Lu | 1 | 12.5 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype incomplete | Zhang et al. (2015) |
Geese (unspecified) | China | Shandong | 42 | Sk | 2 | 4.7 | N-PCR (B1) | Zou et al. (2017) | |
Hawaiian geese (Branta sandvicensis) | USA | Hawaii | 4 | Li, Lu | 4 | 100.0 | ND | 10 PCR-RFLP markers – ToxoDB genotype #261 (21729-Li,21774-Lu, 25022-Li), #262 (21850-Li) (DNA from frozen tissues of IHC confirmed toxoplasmosis) | Work et al. (2016) |
Mallard (Anas platyrhynchos) | China | Jilin | 25 | H or Lu | 5 | 20.0 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype incomplete | Zhang et al. (2015) |
Mallard (Anas platyrhynchos) | China | Shandong | 115 | Sk | 9 | 7.8 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #9 in a duck | Zou et al. (2017) |
Mallard (Anas platyrhynchos) | Czech Republic | Several | 280 | B, H, Sk | 15 | 5.4 | RT-PCR, (B1,529 bp), Tg genotyped | 6 PCR-RFLP markers – 6 type II, 7 type III, 6 type II/III | Skorpikova et al. (2018) |
Mallard (Anas platyrhynchos) | Italy | Tuscany | 2 | B | 1 | 50.0 | N-PCR (B1) | 10 PCR-RFLP markers – genotype incomplete | Mancianti et al. (2013) |
Northern shoveler (Anas clypeata) | Italy | Tuscany | 2 | B | 1 | 50.0 | N-PCR (B1) | 10 PCR-RFLP markers – genotype incomplete | Mancianti et al. (2013) |
Bucerotiformes | |||||||||
Southern-Yellow-billed hornbill (Tockus leucomelas) | South Africa | Limpopo | 4 | B | 1 | 25.0 | PCR (B1 – Tg1,2 primers) | Lukášová et al. (2018) | |
Charadriformes | |||||||||
Eurasian stone curlew (Burhinus oedicnemus) | Turkey | Çiğli | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Little tern (Sternula albifrons) | Turkey | Çiğli | 1 | B, H | 0 | 0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Woodcock (Scolopax rusticola) | Greece | Macedonia, Mesolonghi | 86 | B | 4 | 4.7 | PCR (529 bp – Tox -9upAu, Tox-11doAu primers) | ND | Moustakidis et al. (2017) |
Yellow-legged gull (Larus michahellis) | Turkey | Balçova, Konak | 2 | B, H | 2 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated | 15 Microsatellite markers – ToxoDB #1 or #3 in 1, #2 in 1 | Karakavuk et al. (2018) |
Ciconiiformes | |||||||||
Black stork (Ciconia nigra) | Turkey | NS | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
White stork (Ciconia ciconia) | Turkey | Konak | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Columbiformes | |||||||||
Laughing dove (Streptopelia senegalensis) | South Africa | Limpopo | 4 | B | 1 | 25.0 | PCR (B1 – Tg1,2 primers) | Lukášová et al. (2018) | |
Mourning dove (Zenaida macroura) | USA | Tennessee | 186 | B | 2 | 1.0 | PCR (529 bp, TOX4,5 primers) | Ammar et al. (2020) | |
Red-eyed dove (Streptopelia semitorquata) | South Africa | Limpopo | 5 | B | 1 | 20.0 | PCR (B1 – Tg1,2 primers) | 15 microsatellites markers – genotyping type II | Lukášová et al. (2018) |
Rock pigeon (Columba livia) | Iran | Khuzestan | 43 | B, H | 3 | 6.9 | PCR (B1 – TG1,2 primers) | PCR-RFLP using GRA6, 1 type II and 2 type III | Khademvatan et al. (2013) |
Rock pigeon (Columba livia) | Pakistan | Punjab | 54 | H, Sk | 19 | 35.1 | PCR (B1 – TOX4,5 primers) | ND | Nazir et al. (2018) |
Rock pigeon (Columba livia) | Portugal | Lisbon | 41 | B | 28 | 68.2 | PCR (B1) | Genotyping by SAG2 (26 type II, 2 type III, 1 type I), and 5 microsatellites markers (12 type II, 2 type III, 1 type 1, 1 recombinant) | Vilares et al. (2014) |
Rock pigeon (Columba livia) | Serbia | Belgrade | 7 | H | 5 | 71.4 | RT-PCR (529 bp) | 6 PCR-RFLP markers – 2 type II and 1 type III | Marković et al. (2014) |
Wood pigeon (Columba palumbus) | Italy | NS | 1 | B, H | 1 | 100.0 | N-PCR (B1) | ND | Nardoni et al. (2019) |
Wood pigeon (Columba palumbus) | Turkey | Konak | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Falconiformes | |||||||||
Common kestrel (Falcus tinnunculus) | Italy | NS | 3 | B, H | 2 | 66.6 | N-PCR (B1) | ND | Nardoni et al. (2019) |
Common kestrel (Falco tinnunculus) | Poland | Several | 3 | B, H, Li, Sk | 1 | 33.3 | PCR (B1) | 5 PCR-RFLP markers – type II/III | Sroka et al. (2019) |
Common kestrel (Falco tinnunculus) | Turkey | Konak | 1 | B, H | 0 | 0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Eurasian jay (Garrulus glandarius) | Slovakia | Tatra National Park | 2 | Sk | 1 | 50.0 | PCR (TGR1E – TGR1E-1,2 primers) | PCR-RFLP using SAG2 – type III | Turčeková et al. (2014) |
New Zealand falcon (Falco novaeseelandiae) | New Zealand | Palmerston | 35 | H, Li, Lu, Sp | 2 | 5.7 | N-PCR (Pppk-dhps) | 7 PCR-RFLP markers – genotype incomplete | Mirza et al. (2017) |
Northern goshawk (Accipiter gentilis) | Slovakia | Tatra National Park | 2 | Sk | 1 | 50.0 | PCR (TGR1E – TGR1E-1,2 primers) | PCR-RFLP using SAG2 – type II | Turčeková et al. (2014) |
Peregrine falcon (Falco peregrinus) | Turkey | Çiğli | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Galliformes | |||||||||
Quail (Coturnix coturnix) | China | Shandong | 390 | Sk | 25 | 6.4 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #9 in 5 | Cong et al. (2017b) |
Turkeys (Meleagris gallopavo) | Iran | Fars | 54 | B, Sk, T | 33 | 66.0 | N-PCR (B1). Samples from abattoirs | ND | Sarkari et al. (2014) |
Gruiformes | |||||||||
Eurasian coot (Fulica atra) | China | Jilin | 25 | H or Lu | 1 | 4.0 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype incomplete | Zhang et al. (2015) |
Passeriformes | |||||||||
Hooded crow (Corvus cornix) | Iran | Tehran | 55 | B | 9 | 16.3 | N-PCR (GRA6) | PCR-RFLP using GRA6 – type III | Abdoli et al. (2018) |
Hooded crow (Corvus cornix) | Israel | Haifa | 101 | B | 1 | 1.0 | PCR (529 bp – TOX4,5 primers) | 11 PCR-RFLP markers – type II | Salant et al. (2013) |
House sparrows (Passer domesticus) | Brazil | Bahia, Pernambuco | 40 | B | 10 | 10.0 | N-PCR (ITS1) | ND | Gondim et al. (2010) |
House sparrows (Passer domesticus) | Brazil | Pernambuco | 10 | B | 3 | 30.0 | N-PCR (B1) | Vilela et al. (2011) | |
House sparrows (Passer domesticus) | China | Lanzhou | 39 | B, H, Lu | 11 | 28.2 | N-PCR (B1) | 9 PCR-RFLP markers – ToxoDB genotype #3 in 3 and a new type in 1 | Cong et al. (2013) |
House sparrows (Passer domesticus) | China | Several | 22 | Sk | 1 | 4.5 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #3 | Huang et al. (2012) |
House sparrows (Passer domesticus) | Iran | Khuzestan | 64 | B, H | 17 | 26.5 | PCR (B1 – TG1,2 primers) | PCR-RFLP using GRA6, 1 type II and 16 type III | Khademvatan et al. (2013) |
House sparrows (Passer domesticus) | Iran | Tehran | 200 | B | 17 | 8.5 | LAMP, PCR (529 bp – B3,F3, TOX4,5 primers) | ND | Abdoli et al. (2016) |
Magpie (Pica pica) | Italy | Tuscany | 41 | Bl, H | 15 | 36.6 | N-PCR (B1) | 5 PCR-RFLP markers – 8 type II and 7 type III | Mancianti et al. (2020) |
Magpie (Pica pica) | Slovakia | Tatra National Park | 3 | Sk | 1 | 33.3 | PCR (TGR1E – TGR1E-1,2 primers) | PCR-RFLP using SAG2 – type III | Turčeková et al. (2014) |
Magpie (Pica pica) | Spain | Several | 33 | B | 5 | 12.8 | N-PCR (529 bp – TOX9,11 primers) | ND | Darwich et al. (2012) |
Olive-backed pipit (Anthus hodgsoni) | China | Hunan | 44 | B | 1 | 2.2 | N-PCR (B1) | Liu et al. (2019) | |
Oriental skylark (Alauda gulgula) | China | Lanzhou, Tianshui | 34 | B | 3 | 8.8 | N-PCR (B1) | 10 PCR-RFLP markers – type II variant in 2, ToxoDB genotype #3 | Cong et al. (2014) |
Starling (Sturnus vulgaris) | Iran | Khuzestan | 39 | B, H | 5 | 12.8 | PCR (B1 – TG1,2 primers) | PCR-RFLP using GRA6, 2 type II and 3 type III | Khademvatan et al. (2013) |
Thrush nightingale (Luscinia luscinia) | Turkey | Konak | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Tree sparrows (Passer montanus) | China | Hunan | 131 | B | 11 | 8.4 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #10 in 3 sparrows | Liu et al. (2019) |
Tree sparrows (Passer montanus) | China | Several | 35 | Sk | 1 | 2.8 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #10 | Huang et al. (2012) |
Yellow-breasted bunting (Emberiza aureola) | China | Hunan | 26 | B | 1 | 3.8 | N-PCR (B1) | Liu et al. (2019) | |
Phoenicopteriformes | |||||||||
Great flamingo (Phoenicopterus roseus) | Turkey | Konak | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Psittaformes | |||||||||
Black-headed gull (Chroicocephalus ridibundus) | Italy | NS | 4 | B, H | 4 | 100.0 | N-PCR (B1) | ND | Nardoni et al. (2019) |
Black-headed gull (Chroicocephalus ridibundus) | Poland | Several | 2 | B, H, Li, Sk | 1 | 50.0 | PCR (B1) | 5 PCR-RFLP markers type II/III | Sroka et al. (2019) |
Strigiformes | |||||||||
Barn owl (Tyto alba) | Turkey | Çiğli, Konak | 2 | B, H | 2 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated | 15 Microsatellite markers – ToxoDB #1 or #3 in 1, #2 in 1 | Karakavuk et al. (2018) |
Eurasian eagle-owl (Bubo bubo) | Turkey | Kemalpaşa, Salihli | 2 | B, H | 2 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | 15 Microsatellite markers – mixed type in 1 | Karakavuk et al. (2018) |
Little owl (Athene noctua) | Turkey | Çiğli | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Morepork (Ninox novaeseelandiae) | New Zealand | Palmerston | 36 | H, Li, Lu, Sp | 3 | 8.3 | PCR (Pppk-dhps) | 7 PCR-RFLP markers – genotype incomplete | Mirza et al. (2017) |
Struthioniformes | |||||||||
Ostrich (Struthio camelus) | Brazil | São Paulo | 38 | B | 25 | 65.7 | PCR (529 bp and 18S rRNA – TOX4,5 and Tg18s48F,359R primers). Tg isolated | 10 PCR-RFLP markers – ToxoDB #161 and #206 in 2 | da Silva and Langoni (2016) |
Ostrich (Struthio camelus) | Egypt | Ismailia | 120 | Bl | 9 | 7.5 | N-PCR (B1) | ND | El-Madawy and Metawea (2013) |
Suliformes | |||||||||
Australasian harrier (Circus approximans) | New Zealand | Palmerston | 46 | H, Li, Lu, Sp | 4 | 8.7 | PCR (Pppk-dhps) | 7 PCR-RFLP markers – genotype incomplete | Mirza et al. (2017) |
Baikal teal (Anas formosa) | China | Jilin | 50 | H or Lu | 11 | 22.0 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #9 in 2 | Zhang et al. (2015) |
Common pheasants (Phasianus colchicus) | China | Several | 98 | Sk | 2 | 2.0 | N-PCR (B1) | 10 PCR-RFLP markers – ToxoDB genotype #3 | Huang et al. (2012) |
Common pheasant (Phasianus colchicus) | Czech Republic | Several | 350 | B, H, Sk | 12 | 3.4 | RT-PCR, (B1,529 bp), Tg genotyped | 6 PCR-RFLP markers – 1 type II, 4 type III, 4 type II/III | Skorpikova et al. (2018) |
Dalmatian pelican (Pelecanus crispus) | Turkey | Çiğli | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers) | Karakavuk et al. (2018) | |
Eurasian jays (Garrulus glandarius) | Spain | Several | 23 | B | 5 | 21.7 | N-PCR (529 bp – TOX9,11 primers) | ND | Darwich et al. (2012) |
Eurasian siskin (Carduelis spinus) | China | Lanzhou | 41 | B | 5 | 12.2 | N-PCR (B1) | 10 PCR-RFLP markers – type II variant in 2, ToxoDB #3 | Cong et al. (2014) |
Great cormorant (Phalacrocorax carbo) | Turkey | Çiğli | 1 | B, H | 1 | 100.0 | RT-PCR, (529 bp – TOX-SE,AS primers). Tg isolated | Karakavuk et al. (2018) |
B, brain; Bl, blood; H, heart; G, gizzard; Li, liver; Lu, lung; Sk, muscle; Sp, spleen; Tg, Toxoplasma gondii; ND, not done; NS, not stated; PCR, polymerase chain reaction; N-PCR, nested PCR; RT-PCR, real-time PCR; PCR, polymerase chain reaction; PCR-RFLP, Restriction fragment length polymorphism.
Turkeys are considered resistant to clinical toxoplasmosis and there were no reports of clinical toxoplasmosis since 2009. Experimentally, turkeys inoculated intravenously with T. gondii tachyzoites or oocysts orally remained healthy, irrespective of the dose (Bangoura et al., 2013; Zöller et al., 2013; Hotop et al., 2014; Maksimov et al., 2018). A kinetic ELISA was developed based on a mixture of recombinant dense granule antigens GRA7 and GRA8 using sera from turkeys inoculated intravenously with Me49 tachyzoites; SAG1 antigen was not suitable in this ELISA using recombinant SAG1 (Koethe et al., 2011). In a subsequent study, information on a large panel of 101 synthetic peptides was obtained on sera from 18 turkeys intravenously inoculated with tachyzoites of 3 strains of T. gondii (RH-Type I, Me49-Type II and NED-Type III). The authors concluded that by using selected peptides, it was possible to serotype strains up to 9 weeks post-inoculation (p.i.) (Maksimov et al., 2018). Antibodies peaked at 5–7 weeks p.i., using the SAG1-ELISA, and the results varied with the T. gondii isolate. Similar results were obtained by the indirect fluorescent antibody assay (IFA) (Maksimov et al., 2018).
In turkeys orally inoculated with oocysts, the parasite was widely disseminated in turkey tissues (Bangoura et al., 2013). Inoculated turkeys were euthanized 6 or 12 weeks p.i. and parasite distribution was assessed by polymerase chain reaction (PCR); no difference was found with respect to 6 or 12 weeks p.i. Brain, heart and drumstick were most frequently infected tissues. The route of inoculation could affect the distribution of parasite DNA. In turkeys inoculated intravenously with tachyzoites, liver, pectoral muscle, heart and brain were affected in decreasing order (Zöller et al., 2013). Judging from the histopathological results, the number of T. gondii in turkey tissues was low. Tissue cysts were found in imprints of 1 liver, and 2 pectoral muscles of turkeys parenterally inoculated with tachyzoites (Zöller et al., 2013). By using magnetic-capture PCR and 100 g samples, most T. gondii were found in the brain and heart (Koethe et al., 2015). Parasite burden was higher in the drumstick vs pectoral muscles.
Ducks (Anas spp.) and geese
Ducks are important for the economy of some countries, especially China. Ducks are a good source of meat and eggs for human consumption. To our knowledge, there are no reports of clinical toxoplasmosis in domestic ducks or geese, but antibodies are common (Tables 4 and 5).
Table 4.
Country | Area | Source | No. tested | No. positive | % Positive | Test | Cut-off | Remarks | Reference |
---|---|---|---|---|---|---|---|---|---|
China | Chongqing | NS | 635 – FR | 84 | 13.3 | MAT | 1:25 | Tg isolated. Location, type of raising AS | Zhao et al. (2015) |
527 – caged | 35 | 6.6 | |||||||
China | Guangzhou | Abattoirs | 349 | 56 | 16.0 | MAT | 1:5 | 6 had MAT titers of 1:40 or higher | Yan et al. (2009) |
China | Jilin | Farms | 268 | 29 | 0.8 | LATa | 1:64 | Li et al. (2020) | |
China | Lanzhou | Abattoirs | 111 – caged | 7 | 6.3 | MAT | 1:5 | Cong et al. (2012) | |
223 – FR | 31 | 13.9 | |||||||
China | Liaoning | Farms | 268 | 26 | 9.7 | MAT | 1:25 | Wang et al. (2014) | |
China | Shenyang | Abattoirs | 146 – caged | 11 | 7.5 | MAT | 1:25 | Yang et al. (2012) | |
122 – FR | 15 | 12.3 | |||||||
Czech Republic | Several | Abattoirs | 360 | 52 | 14.0 | IFA | 1:40 | Bártová et al. (2009) | |
Egypt | Behera | Abattoirs | 151 | 21 | 13.9 | MAT | 1:25 | AbouLaila et al. (2011) | |
Egypt | Kafr El-Sheikh | Farms | 58 | 32 | 55.0 | IHAa | 1:80 | Harfoush and Tahoon (2010) | |
Egypt | 5 regions | Market | 142 | 15 | 10.5 | ELISA | IHC 3 positive. Region AS | Ibrahim et al. (2018) | |
Germany | Lower Saxony | 61 farms | 2534 | 145 | 5.7 | ELISA – SAG1 | 1:200 | Protection AS to indoors kept animals | Maksimov et al. (2011) |
Iraq | Al-Qadisiya | Farms | 50 | 28 | 56.0 | LATa | 1:2 | Alkhaled et al. (2012) | |
Iran | Mazandaran | Market | 87 | 40 | 46.0 | MAT | 1:20 | Amouei et al. (2018) | |
Malaysia | Johor, Kedah, Melaka, Perak | Farms, FR | 205 | 30 | 14.6 | MAT | 1:6 | Tg DNA and genotyping | Puvanesuaran et al. (2013) |
Poland | Lublin | Farms | 33 | 7 | 21.2 | MATa | 1:40 | Sroka et al. (2010) | |
Senegal | Dakar, Saint-Louis | Households | 306 | 16 | 5.2 | MAT | 1:20 | Tg isolated | Galal et al. (2019) |
NS, not stated; ELISA, enzyme-linked immunosorbent assay; IFA, indirect fluorescent antibody test; IHAT, indirect haemagglutination test; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987); FR, free range; Tg, Toxoplasma gondii; AS, association; IHC, immunohistochemical.
IHA (Toxo-IHA Fumouze Diagnostics, France); LAT (PLASMATECH Co., UK); MAT (Toxo-Screen DA®, Biomerieux, Lyon, France). This is the same test as MAT.
Table 5.
Country | Area | Source | No. tested | No. positive | % Positive | Test | Cut-off | Remarks | Reference |
---|---|---|---|---|---|---|---|---|---|
China | Guangdong | Farms | 274 | 41 | 14.9 | MAT | 1:5 | – | Yan et al. (2011b) |
China | Guangdong | Farms | 520 | 9 | 1.7 | MAT | Age, management | Wang et al. (2012) | |
China | Hainan | Farms | 600 | 102 | 17.0 | IHAa | 1:64 | Presence of cats, hygiene AS. Tg DNA and genotyping | Rong et al. (2014) |
China | Jilin | Farms | 379 | 50 | 13.2 | IHAa | 1:64 | Li et al. (2020) | |
China | Liaoning | Farms | 128 | 9 | 7.0 | MAT | 1:25 | Wang et al. (2014) | |
China | Shenyang | Abattoirs | 83 – caged | 5 | 6.0 | MAT | 1:25 | Yang et al. (2012) | |
45 – FR | 4 | 8.9 | |||||||
Czech Republic | Bohemia, Olomouc | Abattoirs | 178 | 77 | 43.0 | IFA | 1:40 | Bártová et al. (2009) | |
Germany | Lower Saxony | 13 farms | 373 | 94 | 25.2 | ELISA-SAG1 | 1:200 | Protection AS to indoors kept animals | Maksimov et al. (2011) |
Iran | Mazandaran | Market | 5 | 5 | 100.0 | MAT | 1:20 | – | Amouei et al. (2018) |
USA | Maryland | Hunted | 169 | 12 | 7.1 | MAT | 1:25 | Canada geese, Tg isolated | Verma et al. (2016) |
AS, association; FR, free-range; Tg, Toxoplasma gondii; ELISA, enzyme-linked immunosorbent assay; IFA, indirect fluorescent antibody test; IHA, indirect haemagglutination assay; MAT, modified agglutination test (Dubey and Desmonts, 1987).
IHA kit (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China).
Toxoplasma gondii DNA was found in 9 (7.8%) of 115 muscle samples from 115 ducks and 2 of 42 geese (4.7%) (Zou et al., 2017). Viable T. gondii was isolated from tissues of ducks in China, France and Malaysia (Table 3).
Ostriches (Struthio camelus) and other ratites
Ratite meat is lean and its human consumption is increasing. Serologic data are summarized in Table 6. Antibodies to T. gondii were detected up to 80.0% of sera (Table 6).
Table 6.
Host | Country | Area | Source | No. tested | No. positive | % positive | Test | Cut-off | Remarks | Reference |
---|---|---|---|---|---|---|---|---|---|---|
Emus (Dromaius novaehollandiae) | Brazil | Goiás | Farm | 16 | 8 | 50.0 | MAT | 1:25 | Gallo et al. (2019) | |
Ostriches (Struthio camelus) | Brazil | Mato Grosso, Rio Grande do Sul, São Paulo | 3 Farms | 46 | 8 | 17.4 | MAT | 1:16 | Almeida et al. (2013) | |
Ostriches (Struthio camelus) | Brazil | Rio de Janeiro | Abattoirs | 20 | 16 | 80.0 | MAT | 1:25 | Gallo et al. (2019) | |
Ostriches (Struthio camelus) | Brazil | São Paulo | Farms | 195 | 28 | 14.3 | MAT | 1:16 | MAT titer 1:16384 in 2 ostriches | Contente et al. (2009) |
Ostriches (Struthio camelus) | Brazil | São Paulo | Abattoir, 4 farms | 344 | 38 | 11.0 | MAT | 1:8 | Tg DNA and parasite isolation, Water source, presence of non-ostrich feces AS | da Silva and Langoni (2016) |
Ostriches (Struthio camelus) | China | Hebei, Henan | Abattoirs | 315 | 20 | 6.4 | MAT | 1:25 | Tg DNA and parasite isolation | Feng et al. (2017) |
Ostriches (Struthio camelus) | Egypt | Ismailia | Farm | 120 | 15 | 12.5 | MAT | 1:25 | Tg DNA. 5 (4.2%) IgM positive | El-Madawy and Metawea (2013) |
Rheas (Rhea americana) | Brazil | Espírito Santo, Goiás, São Paulo | Farm | 68 | 18 | 26.5 | MAT | 1:25 | Gallo et al. (2019) | |
Rheas (Rhea americana) | Brazil | Rio Grande do Sul, Santa Catarina | 2 Farms | 20 | 10 | 50.0 | MAT | 1:25 | Almeida et al. (2013) |
MAT, modified agglutination test (Dubey and Desmonts, 1987); AS, association; Tg, Toxoplasma gondii.
Viable T. gondii was demonstrated in ostrich tissues. In a Brazilian report, T. gondii was detected in brains of ostriches and in soil samples from paddocks (da Silva and Langoni, 2016). Brain (25 g) samples of 38 seropositive and 20 seronegative ostriches were bioassayed in mice. Toxoplasma gondii was isolated from 14 seropositive but not from seronegative ostriches. All strains were apparently pathogenic for mice. Toxoplasma gondii DNA was found in peritoneal exudates of mice inoculated from tissues of 8 ostriches, and in brains of mice inoculated with 6 ostrich samples. Nothing was said concerning finding viable T. gondii. Of interest is the report of finding T. gondii-like oocysts microscopically in soil samples from 5 of 20 paddocks; all were confirmed by PCR. In repeat sampling, T. gondii-like oocysts were found microscopically in soil samples from 9 of 20 paddocks and results were confirmed by PCR. It should be noted that only a few oocysts are normally present in soil and their detection is a challenge (J.P.D. own observation).
In marked contrast to the Brazilian report, in a Chinese study, T. gondii DNA was not detected in any of the 293 hearts and 77 brains of ostriches (Feng et al., 2017).
A study in Egypt found T. gondii DNA in the blood of 9 of 120 ostriches (El-Madawy and Metawea, 2013). These authors also tested tissues of 5 ostriches that had died of toxoplasmosis-like illness; T. gondii DNA was found in the brains of 5, hearts of 3 and leg muscle of 1 (El-Madawy and Metawea, 2013) (Comment J.P.D. – tissues of these ostriches should be examined histologically for verification of molecular results).
Other wild avian species
Data on T. gondii seroprevalence, viable parasite and DNA characterization are arranged by scientific order of birds, by region and chronologically in Tables 2, 3 and 7.
Table 7.
Order, common name, (scientific name) | Country | Region | No. tested | No. positive | % Positive | Test | Cut-off | Notes | Reference |
---|---|---|---|---|---|---|---|---|---|
Accipitriformes | |||||||||
Bald eagle (Haliaeetus leucocephalus) | Czech Republic | Zoos | 1 | 1 | 100.0 | LATa | Bártová et al. (2018) | ||
Bald eagle (Haliaeetus leucocephalus) | USA | Alabama | 13 | 12 | 92.3 | MAT | 1:25 | Love et al. (2016) | |
Bearded vulture (Gypaetus barbatus) | Spain | Several | 15 | 6 | 42.8 | MAT | 1:25 | Cabezón et al. (2011) | |
Black kite (Milvus migrans) | Portugal | Central, northern | 1 | 1 | 100.0 | MAT | 1:20 | Lopes et al. (2011) | |
Black kite (Milvus migrans) | Senegal | Dakar | 2 | 2 | 100.0 | MAT | 1:20 | Galal et al. (2019) | |
Black kite (Milvus migrans) | Spain | Several | 17 | 5 | 29.4 | MAT | 1:25 | Cabezón et al. (2011) | |
Bonelli's eagle (Aquila fasciata) | Spain | Several | 9 | 1 | 11.1 | MAT | 1:25 | Cabezón et al. (2011) | |
Booted eagle (Hieraaetus pennatus) | Spain | Southern | 1 | 1 | 100.0 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Broad-winged hawk (Buteo platypterus) | USA | Alabama | 20 | 6 | 30.0 | MAT | 1:25 | Love et al. (2016) | |
Cinereous vulture (Aegypius monachus) | Czech Republic | Zoos | 11 | 7 | 64.0 | LATa | – | Bártová et al. (2018) | |
Cinereous vulture (Aegypius monachus) | Spain | Several | 23 | 6 | 26.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Common buzzard (Buteo buteo) | Portugal | Central, northern | 26 | 18 | 69.2 | MAT | 1:20 | Lopes et al. (2011) | |
Cooper's hawk (Accipiter cooperii) | USA | Alabama | 12 | 6 | 50.0 | MAT | 1:25 | Love et al. (2016) | |
Crested goshawk (Accipiter trivirgatus) | Taiwan | Several | 41 | 7 | 17.0 | MATb | 1:40 | Chen et al. (2015) | |
Eagle (Aquila spp.) | Mexico | Durango | 2 | 1 | 50.0 | MAT | 1:25 | Location AS | Alvarado-Esquivel et al. (2011) |
Eurasian buzzard (Buteo buteo) | Italy | Northern | 12 | 1 | 8.3 | MATb | 1:40 | Gazzonis et al. (2018) | |
Eurasian buzzard (Buteo buteo) | Spain | Several | 96 | 49 | 51.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Eurasian griffon (Gyps fulvus) | Czech Republic | Zoos | 4 | 3 | 75.0 | LATa | – | Bártová et al. (2018) | |
Eurasian sparrow hawk (Accipiter nisus) | Italy | Northern | 2 | 1 | 50.0 | MATb | 1:40 | Gazzonis et al. (2018) | |
Golden eagle (Aquila chrysaetos) | Spain | Several | 8 | 5 | 62.5 | MAT | 1:25 | Cabezón et al. (2011) | |
Golden eagle (Aquila chrysaetos) | USA | Alabama | 1 | 1 | 100.0 | MAT | 1:25 | Love et al. (2016) | |
Griffon vulture (Gyps fulvus) | Israel | 4 Areas | 101 | 40 | 39.6 | MAT | 1:25 | Salant et al. (2013) | |
Griffon vulture (Gyps fulvus) | Spain | Several | 175 | 31 | 17.7 | MAT | 1:25 | Cabezón et al. (2011) | |
Montagu's harrier (Circus pygargus) | Spain | Several | 7 | 1 | 14.3 | MAT | 1:25 | Cabezón et al. (2011) | |
Northern goshawk (Accipiter gentilis) | Portugal | Central, northern | 3 | 3 | 100.0 | MAT | 1:20 | Lopes et al. (2011) | |
Northern goshawk (Accipiter gentilis) | Spain | Several | 5 | 2 | 40.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Osprey (Pandion haliaetus) | Spain | Several | 7 | 2 | 28.5 | MAT | 1:25 | Cabezón et al. (2011) | |
Red kite (Milvus milvus) | Spain | Several | 3 | 1 | 33.3 | MAT | 1:25 | Cabezón et al. (2011) | |
Red-shouldered hawk (Buteo lineatus) | USA | Alabama | 41 | 9 | 21.9 | MAT | 1:25 | Love et al. (2016) | |
Red tailed hawk (Buteo jamaicensis) | USA | Alabama | 71 | 22 | 30.9 | MAT | 1:25 | Love et al. (2016) | |
Roadside hawk (Rupornis magnirostris) | Brazil | São Paulo | 1 | 1 | 100.0 | MAT | 1:16 | Gonçalves et al. (2013) | |
Serpent eagle (Spilornis cheela) | Taiwan | Several | 43 | 20 | 46.5 | MATb | 1:40 | Chen et al. (2015) | |
Short-toed Snake-eagle (Circaetus gallicus) | Spain | Several | 10 | 5 | 50.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Spanish Imperial eagle (Aquila adalberti) | Spain | Several | 146 | 25 | 17.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Tawny eagle (Aquilla rapax) | Czech Republic | Zoos | 1 | 1 | 100.0 | LATa | – | Bártová et al. (2018) | |
Western marsh-harrier (Circus aeruginosus) | Italy | Northern | 2 | 1 | 50.0 | MATb | 1:40 | Gazzonis et al. (2018) | |
Western marsh-harrier (Circus aeruginosus) | Spain | Several | 6 | 3 | 50.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Anseriformes | |||||||||
Bar-headed goose (Anser indicus) | Spain | Córdoba | 11 | 1 | 9.1 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Barnacle goose (Branta leucopsis) | Europe | Russia, Svalbard, The Netherlands | 1087 | 98 | 9.0 | MATb | 1:40 | See text | Sandström et al. (2013) |
Black swan (Cygnus atratus) | Portugal | Zoo | 7 | 1 | 14.3 | MATb | 1:20 | Tidy et al. (2017) | |
Canada goose (Branta canadensis) | Canada | Saskatoon | 71 | 2 | 2.8 | MATb | 1:40 | Al-Adhami et al. (2016) | |
Canada goose (Branta canadensis) | Canada | Nunavik | 148 | 16 | 10.8 | MATa | 1:25 | Bachand et al. (2019) | |
Canada goose (Branta canadensis) | Europe | The Netherlands | 38 | 3 | 7.9 | MATb | 1:40 | See text | Sandström et al. (2013) |
Common teal (Anas crecca) | Italy | Tuscany | 41 | 3 | 7.3 | MATb | 1:10 | PCR positive in 1 seropositive | Mancianti et al. (2013) |
Coscoroba swan (Coscoroba coscoroba) | Czech Republic | Zoos | 2 | 1 | 50.0 | LATa | Bártová et al. (2018) | ||
Domestic geese (Anser anser) | Europe | The Netherlands | 161 | 13 | 8.1 | MATb | 1:40 | See text | Sandström et al. (2013) |
Emperor goose (Chen canagica) | Spain | Southern | 2 | 1 | 50.0 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Eurasian green-winged teal (Anas crecca) | Iran | Mazandaran | 20 | 12 | 60.0 | MAT | 1:20 | Amouei et al. (2018) | |
Garganey (Spatula querquedula) | Senegal | Dakar | 28 | 8 | 28.5 | MAT | 1:20 | Galal et al. (2019) | |
Geese (Anser sp.) | Brazil | Paraná | 149 | 27 | 18.1 | IFA | 1:25 | Higher prevalence in animals from urban parks | Konell et al. (2019) |
Lesser snow geese (Chen caerulescens) | Canada | Karrak Lake Nunavut | 121 | 43 | 36.0 | IFA | 1:20 | Results higher than MATb at 1:40 dilution | Elmore et al. (2014) |
Lesser snow geese (Chen caerulescens) | Canada | Nunavut | 233 | 66 | 28.3 | ELISA | Elmore et al. (2015) | ||
Lesser snow geese (Chen caerulescens) | Canada | Nunavik | 8 | 2 | 25.0 | MATa | 1:25 | Bachand et al. (2019) | |
Ross's geese (Chen rossi) | Canada | Nunavut | 234 | 76 | 32.4 | ELISA | Elmore et al. (2015) | ||
Mallard duck (Anas brachyrhynchus) | Europe | Denmark, Svalbard | 573 | 59 | 10.2 | MATb | 1:40 | See text | Sandström et al. (2013) |
Mallard duck (Anas platyrhynchos) | Mexico | Durango | 2 | 1 | 50.0 | MAT | 1:25 | Location AS | Alvarado-Esquivel et al. (2011) |
Mallard duck (Anas platyrhynchos) | Iran | Mazandaran | 20 | 9 | 45.0 | MAT | 1:20 | – | Amouei et al. (2018) |
Mallard duck (Anas platyrhynchos) | Italy | Tuscany | 17 | 2 | 11.7 | MATb | 1:10 | PCR positive in 1 seropositive | Mancianti et al. (2013) |
Mallard duck (Anas platyrhynchos) | Portugal | Zoo | 4 | 3 | 75.0 | MATb | 1:20 | Tidy et al. (2017) | |
Mallard duck (Anas platyrhynchos) | Spain | Several | 6 | 2 | 33.3 | MAT | 1:25 | Cabezón et al. (2011) | |
Mallard duck (Anas platyrhynchos) | Spain | Southern | 4 | 1 | 25.0 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Mallard duck (Anas platyrhynchos) | Taiwan | Several | 1 | 1 | 100.0 | MATb | 1:40 | Chen et al. (2015) | |
Mandarian duck (Aix galericulata) | Portugal | Zoo | 6 | 3 | 50.0 | MATb | 1:20 | Tidy et al. (2017) | |
Mexican duck (Anas diazi) | Mexico | Durango | 2 | 1 | 50.0 | MAT | 1:25 | Location AS | Alvarado-Esquivel et al. (2011) |
Mute swan (Cygnus olor) | USA | Northeastern | 632 | 54 | 8.5 | MAT | 1:25 | Tg isolated | Dubey et al. (2013) |
Northern pintail (Anas acuta) | Spain | Several | 1 | 1 | 100.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Orinoco (Neochen jubata) | Brazil | Goiás | 41 | 35 | 85.3 | IFA | 1:20 | N. caninum in 12.1% | André et al. (2019) |
Paradise shelduck (Tadorna variegata) | Czech Republic | Zoos | 1 | 1 | 100.0 | LATa | – | Bártová et al. (2018) | |
Ross's geese (Chen rossi) | Canada | Karrak Lake Nunavut | 123 | 48 | 39.0 | IFA | 1:20 | Results higher than MATb at 1:40 dilution | Elmore et al. (2014) |
Shoveller duck (Anas clypeata) | Italy | Tuscany | 11 | 2 | 18.1 | MATb | 1:10 | PCR positive in 1 seropositive | Mancianti et al. (2013) |
Sudanese duck (Anas platyrhynchos) | Egypt | Several | 142 | 15 | 10.5 | ELISA | Region AS. IHC | Ibrahim et al. (2018) | |
Swan goose (Anser cygnoides) | Portugal | Zoo | 1 | 1 | 100.0 | MATb | 1:20 | Tidy et al. (2017) | |
Tundra swan (Cygnus columbianus) | China | Jiangxi | 9 | 2 | 22.2 | IHAb | 1:64 | Luo et al. (2017) | |
Wood duck (Aix sponsa) | Portugal | Zoo | 7 | 2 | 28.6 | MATb | 1:20 | Tidy et al. (2017) | |
Bucerotiformes | |||||||||
Eurasian hoopoe (Upupa epops) | Spain | Several | 1 | 1 | 100.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Cariamiformes | |||||||||
Crested seriema (Cariama cristata) | Brazil | Minas Gerais, São Paulo | 1 | 1 | 100.0 | MAT | 1:5 | Vitaliano et al. (2014) | |
Charadriformes | |||||||||
Audouin's gull (Larus audouinii) | Spain | Alboran Island | 46 | 1 | 2.2 | MAT | 1:25 | Age, food source, year AS | Cabezón et al. (2016) |
Caracara (Caracara plancus) | Brazil | Pernambuco | 115 | 6 | 5.2 | MAT | 1:25 | Silva et al. (2018a) | |
Common kestrel (Falco tinnunculus) | Italy | Northern | 18 | 1 | 5.5 | MATb | 1:40 | Gazzonis et al. (2018) | |
Common snipe (Gallinago gallinago) | Italy | Tuscany | 8 | 2 | 25.0 | MATb | 1:10 | Mancianti et al. (2013) | |
Common snipe (Gallinago gallinago) | Pakistan | Punjab | 4 | 1 | 25.0 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Yellow-legged gull (Larus michahellis) | Europe | France, Spain, Tunisia | 988 nests | 233 | 23.6 | ELISAb | ELISA in 1122 egg yolk. Different prevalence between colonies AS | Gamble et al. (2019) | |
Yellow-legged gull (Larus michahellis) | Spain | Iberian Peninsula | 479 | 109 | 22.8 | MAT | 1:25 | Age, food source, year AS | Cabezón et al. (2016) |
Ciconiiformes | |||||||||
Black stork (Ciconia nigra) | Spain | Several | 1 | 0 | 0 | MAT | 1:25 | Cabezón et al. (2011) | |
White stork (Ciconia ciconia) | Spain | Several | 64 | 9 | 14.1 | MAT | 1:25 | Cabezón et al. (2011) | |
Columbiformes | |||||||||
Dove (Spilopelia sp.) | Senegal | Dakar | 1 | 1 | 100.0 | MAT | 1:20 | Galal et al. (2019) | |
Eared dove (Zenaida auriculata) | Brazil | Paraná | 206 | 46 | 22.3 | MAT | 1:16 | Location AS. Tg isolated | de Barros et al. (2014) |
Eurasian collared dove (Streptopelai decaocto) | Pakistan | Punjab | 10 | 2 | 20.0 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Feral pigeon (Columba livia var. domestica) | Spain | Southern | 142 | 13 | 9.2 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Gray-fronted dove (Leptotila rufaxilla) | Brazil | Paraíba | 5 | 1 | 20.0 | MAT | 1:25 | Andrade et al. (2016) | |
Oriental turtle dove (Streptopelia orientalis) | Taiwan | Several | 16 | 4 | 25.0 | MATb | 1:40 | Chen et al. (2015) | |
Picazuro pigeon (Patagioenas picazuro) | Brazil | Minas Gerais, São Paulo | 3 | 1 | 33.3 | MAT | 1:5 | Vitaliano et al. (2014) | |
Rock pigeon (Columba livia) | Brazil | São Paulo | 126 | 0 | 0 | MAT | 1:5 | Tg not isolated by bioassay of any of 126 pigeons | de Godoi et al. (2010) |
Rock pigeon (Columba livia) | Brazil | São Paulo | 120 | 1 | 0.8 | IFA | 1:20 | de Sousa et al. (2010) | |
Rock pigeon (Columba livia) | Brazil | São Paulo | 238 | 12 | 5.0 | MAT | 1:8 | Tg not isolated | de Lima et al. (2011) |
Rock pigeon (Columba livia) | China | Guangdong | 275 | 24 | 8.7 | MAT | 1:5 | Yan et al. (2011a) | |
Rock pigeon (Columba livia) | China | Several | 963 | 104 | 10.8 | IHAb | 1:64 | Age, gender AS | Zhang et al. (2019) |
Rock pigeon (Columba livia) | Egypt | Several | 310 | 42 | 13.5 | ELISA | IHC | Ibrahim et al. (2018) | |
Rock pigeon (Columba livia) | Israel | Several | 495 | 20 | 4.0 | MAT | 1:5 | Climate, population near to human settlement | Salant et al. (2009) |
Rock pigeon (Columba livia) | Mexico | Durango | 521 | 7 | 1.9 | MAT | 1:25 | Location AS. Tg isolated | Alvarado-Esquivel et al. (2011) |
Rock pigeon (Columba livia) | Portugal | Lisbon | 1507 | 39 | 2.6 | MATb | 1:20 | Tg isolated in cell cultures seeded with 13 of 20 seropositive pigeons | Waap et al. (2012) |
Rock pigeon (Columba livia) | Russia | Circus animals | 28 | 10 | 35.7 | ELISAa | Sivkova and Neprimerova (2017) | ||
Rock pigeon (Columba livia) | Spain | Córdoba | 142 | 13 | 9.2 | MAT | 1:25 | Cano-Terriza et al. (2015) | |
Rock pigeon (Columba livia) | Taiwan | Several | 62 | 1 | 1.6 | MATb | 1:40 | Chen et al. (2015) | |
Rock pigeon (Columba livia) | Turkey | Niğde | 216 | 2 | 0.9 | DT | 1:16 | Karatepe et al. (2011) | |
Rock pigeon (Columba livia) | USA | Colorado | 129 | 5 | 3.9 | MAT | 1:25 | Dubey et al. (2010) | |
Rock pigeon (Columba livia) | USA | Tennessee | 1 | 1 | 100.0 | MAT | 1:32 | Gerhold et al. (2017) | |
Spotted-necked dove (Streptopelia chinensis) | Taiwan | Several | 17 | 5 | 29.4 | MATb | 1:40 | Chen et al. (2015) | |
Cuculiformes | |||||||||
Coucal (Centropus sp.) | Senegal | Dakar | 1 | 1 | 100.0 | MAT | 1:20 | Galal et al. (2019) | |
Falconiformes | |||||||||
Common kestrel (Falco tinnunculus) | Italy | Parma | 238 | 62 | 26.1 | MATb | 1:25 | Age, year sampled, AS | Iemmi et al. (2020) |
Common kestrel (Falco tinnunculus) | Spain | Several | 13 | 4 | 30.7 | MAT | 1:25 | Cabezón et al. (2011) | |
Crested caracara (Caracara plancus) | Brazil | Minas Gerais, São Paulo | 2 | 1 | 50.0 | MAT | 1:5 | Vitaliano et al. (2014) | |
Eurasian hobby (Falco subbuteo) | Italy | Northern | 3 | 1 | 33.3 | MATb | 1:40 | Gazzonis et al. (2018) | |
Lesser kestrel (Falco naumanni) | Spain | Several | 5 | 2 | 40.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Peregrine falcon (Falco peregrinus) | Spain | Several | 4 | 1 | 25.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Yellow-headed caracara (Milvago chimachima) | Brazil | São Paulo | 3 | 2 | 66.6 | MAT | 1:16 | Gonçalves et al. (2013) | |
Galliformes | |||||||||
Common quail (Coturnix coturnix) | China | 3 Provinces | 620 | 59 | 9.5 | MAT | 1:5 | Cong et al. (2017b) | |
Common quail (Coturnix coturnix) | Mexico | Durango | 7 | 1 | 14.2 | MAT | 1:25 | Location AS | Alvarado-Esquivel et al. (2011) |
Common quail (Coturnix coturnix) | Turkey | Niğde | 144 | 0 | 0 | DT | NS | Kiliç et al. (2017) | |
Guinea fowl (Numida meleagris) | Brazil | Minas Gerais | 10 | 2 | 20.0 | MAT | 1:10 | Tg isolated | Dubey et al. (2011a) |
Guinea fowl (Numida meleagris) | Brazil | Rio de Janeiro | 114 | 14 | 12.3 | MAT | 1:16 | Ferreira et al. (2013) | |
Guinea fowl (Numida meleagris) | Senegal | Dakar | 13 | 1 | 7.7 | MAT | 1:20 | Tg isolated | Galal et al. (2019) |
Hawaiian goose (Branta sandvicensis) | USA | Hawaii | 94 | 26 | 27.6 | MAT | 1:25 | 48% in Molokai, 23% in Maui, and 21% in Kauai | Work et al. (2016) |
Silver pheasant (Laphura nycthemera) | Portugal | Zoo | 6 | 1 | 16.6 | MATb | 1:20 | Tidy et al. (2017) | |
Rock ptarmigan (Lagopus muta) | Canada | Saskatoon | 25 | 1 | 4.0 | MATb | 1:40 | Al-Adhami et al. (2016) | |
Gruiformes | |||||||||
Common coot (Fulica atra) | Spain | Several | 1 | 1 | 100.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Common moorhen (Gallinula chloropus) | Pakistan | Punjab | 5 | 1 | 20.0 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Common moorhen (Gallinula chloropus) | Spain | Several | 1 | 1 | 100.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Eurasian coot (Fulica atra) | Iran | Mazandaran | 10 | 5 | 50.0 | MAT | 1:20 | Amouei et al. (2018) | |
Grey crowned crane (Balearica regulorum) | Portugal | Zoo | 4 | 0 | 0.0 | MATb | 1:20 | Tidy et al. (2017) | |
Japanese crane (Grus japonensis) | Portugal | Zoo | 2 | 1 | 50.0 | MATb | 1:20 | Tidy et al. (2017) | |
Rail (Rallus sp.) | Senegal | Dakar | 2 | 1 | 50.0 | MAT | 1:20 | Galal et al. (2019) | |
Otidiformes | |||||||||
Great bustard (Otis tarda) | Spain | Several | 7 | 1 | 14.2 | MAT | 1:25 | Cabezón et al. (2011) | |
Passeriformes | |||||||||
Ashy-throated casiornis (Casiornis fuscus) | Brazil | Bahia | 1 | 1 | 100.0 | MAT | 1:25 | Andrade et al. (2016) | |
Black drongo (Dicrurus macrocercus) | Pakistan | Punjab | 9 | 1 | 11.1 | LATb | 1:64 | Age, health status AS. | Naveed et al. (2019) |
Buff-browed foliage-gleaner (Syndactyla rufosuperciliata) | Brazil | São Paulo | 7 | 4 | 57.1 | MAT | 1:5 | Gennari et al. (2014) | |
Common babbler (Turdoides caudatus) | Pakistan | Punjab | 2 | 1 | 50.0 | LATb | 1:64 | Age, health status AS. | Naveed et al. (2019) |
Common myna (Acridotheres tristis) | Pakistan | Punjab | 11 | 2 | 18.1 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Common raven (Corvus corax) | Spain | Northeast | 113 | 91 | 80.5 | MAT | 1:25 | Year sampled AS | Molina-López et al. (2012) |
Creamy-bellied thrush (Turdus amaurochalinus) | Brazil | São Paulo | 2 | 1 | 50.0 | MAT | 1:5 | Gennari et al. (2014) | |
Curve-billed thrasher (Toxostoma curvirostre) | Mexico | Durango | 2 | 1 | 50.0 | MAT | 1:25 | Alvarado-Esquivel et al. (2011) | |
European goldfinch (Carduelis carduelis) | Spain | Several | 1 | 1 | 100.0 | MAT | 1:25 | Cabezón et al. (2011) | |
European starling (Sturnus vulgaris) | USA | Colorado | 27 | 4 | 15.0 | MAT | 1:50 | Dubey et al. (2010) | |
Formosan blue magpie (Urocissa caerulea) | Taiwan | Several | 16 | 6 | 37.5 | MATb | 1:40 | Chen et al. (2015) | |
Golden-crowned warbler (Basileuterus culicivorus) | Brazil | São Paulo | 12 | 2 | 16.7 | MAT | 1:5 | Gennari et al. (2014) | |
Great-tailed grackle (Quiscalus mexicanus) | Mexico | Durango | 18 | 5 | 27.8 | MAT | 1:25 | Location AS | Alvarado-Esquivel et al. (2011) |
Hooded crow (Corvus cornix) | Israel | 6 areas | 101 | 48 | 47.5 | MAT | 1:25 | Geographic location AS | Salant et al. (2013) |
Hooded crow (Corvus cornix) | Italy | Pisa | 120 | 4 | 3.3 | MATb | 1.25 | Mancianti et al. (2020) | |
House crow (Corvus splendens) | Israel | Eilat | 16 | 2 | 12.5 | MAT | 1:25 | Salant et al. (2013) | |
House crow (Corvus splendens) | Pakistan | Punjab | 17 | 6 | 35.3 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
House sparrow (Passer domesticus) | Brazil | Bahia, Pernambuco | 293 | 3 | 1.0 | IHA | 1:32 | Tg DNA | Gondim et al. (2010) |
House sparrow (Passer domesticus) | Brazil | Pernambuco | 151 | 91 | 60.3 | IHAa | 1:16 | Tg DNA | Vilela et al. (2011) |
House sparrow (Passer domesticus) | China | Lanzhou | 313 | 39 | 12.4 | MAT | 1:5 | Tg DNA in 11 tissues of 39 seropositive | Cong et al. (2013) |
House sparrow (Passer domesticus) | Pakistan | Punjab | 9 | 1 | 11.1 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Indian silverbill (Lonchura malabarica) | Pakistan | Punjab | 4 | 2 | 50.0 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Jackdaw crow (Corvus monedula) | Israel | Ganei Yavne | 5 | 2 | 40.0 | MAT | 1:25 | – | Salant et al. (2013) |
Java sparrows (Lonchura oryzivora) | China | Beijing, Shangqiu | 350 | 120 | 34.3 | MAT | 1:20 | Gender, colour AS | Huang et al. (2019) |
Jungle babbler (Turdoides striatus) | Pakistan | Punjab | 6 | 1 | 16.6 | LATb | 1:64 | Age, health status AS | Naveed et al. (2019) |
Lesser woodcreeper (Xiphorhynchus fuscus) | Brazil | São Paulo | 2 | 1 | 50.0 | MAT | 1:5 | Gennari et al. (2014) | |
Magpie (Pica pica) | Italy | Pisa | 651 | 41 | 6.2 | MATb | 1:40 | Mancianti et al. (2020) | |
Magpie (Pica pica) | Taiwan | Several | 22 | 10 | 45.5 | MATb | 1:40 | Chen et al. (2015) | |
Pale-breasted thrush (Turdus leucomelas) | Brazil | São Paulo | 1 | 1 | 100.0 | MAT | 1:5 | Gennari et al. (2014) | |
Pied crow (Corvus albus) | Senegal | Dakar | 2 | 2 | 100.0 | MAT | 1:20 | Galal et al. (2019) | |
Plain antvireo (Dysithamnus mentalis) | Brazil | São Paulo | 11 | 5 | 45.4 | MAT | 1:5 | Gennari et al. (2014) | |
Red-crowned ant-tanager (Habia rubica) | Brazil | São Paulo | 13 | 8 | 61.5 | MAT | 1:5 | Gennari et al. (2014) | |
Red vented bulbul (Pycnonotus cafer) | Pakistan | Punjab | 11 | 3 | 27.2 | LATb | 1:64 | Age, health AS | Naveed et al. (2019) |
Ruby-crowned tanager (Tachyphonus coronatus) | Brazil | São Paulo | 6 | 1 | 16.7 | MAT | 1:5 | Gennari et al. (2014) | |
Rufous-bellied thrush (Turdus rufiventris) | Brazil | São Paulo | 18 | 15 | 83.3 | MAT | 1:5 | Gennari et al. (2014) | |
Rufous-breasted leaftosser (Sclerurus scansor) | Brazil | São Paulo | 1 | 1 | 100.0 | MAT | 1:5 | Gennari et al. (2014) | |
Rufous gnateater (Conopophaga lineata) | Brazil | São Paulo | 15 | 6 | 40.0 | MAT | 1:5 | Gennari et al. (2014) | |
Squamate antbird (Myrmeciza squamosa) | Brazil | São Paulo | 4 | 3 | 75.0 | MAT | 1:5 | Gennari et al. (2014) | |
White-browed warbler (Basileuterus leucoblepharus) | Brazil | São Paulo | 5 | 1 | 20.0 | MAT | 1:5 | Gennari et al. (2014) | |
White-eyed foliage-gleaner (Automolus leucophthalmus) | Brazil | São Paulo | 14 | 3 | 21.4 | MAT | 1:5 | Gennari et al. (2014) | |
White-lined tanager (Tachyphonus rufus) | Brazil | Bahia | 16 | 1 | 6.2 | MAT | 1:25 | Andrade et al. (2016) | |
White-necked thrush (Turdus albicollis) | Brazil | São Paulo | 5 | 5 | 100.0 | MAT | 1:5 | Gennari et al. (2014) | |
White-shouldered fire-eye (Pyriglena leucoptera) | Brazil | São Paulo | 11 | 4 | 36.4 | MAT | 1:5 | Gennari et al. (2014) | |
White-spotted woodpecker (Veniliornis spilogaster) | Brazil | São Paulo | 1 | 1 | 100.0 | MAT | 1:5 | Gennari et al. (2014) | |
White-throated woodcreeper (Xiphocolaptes albicollis) | Brazil | São Paulo | 2 | 1 | 50.0 | MAT | 1:5 | Gennari et al. (2014) | |
White-vented myna (Acridotheres javanicus) | Taiwan | Several | 1 | 1 | 100.0 | MATb | 1:40 | Chen et al. (2015) | |
White wagtail (Motacilla alba) | Pakistan | Punjab | 11 | 1 | 9.0 | LATb | 1:64 | Age, health AS | Naveed et al. (2019) |
Pelecaniformes | |||||||||
Black-crowned night heron (Nycticorax nycticorax) | Taiwan | Several | 2 | 2 | 100.0 | MATb | 1:40 | Chen et al. (2015) | |
Buff-necked ibis (Theristicus caudatus) | Brazil | Minas Gerais, São Paulo | 2 | 2 | 100.0 | MAT | 1:5 | Vitaliano et al. (2014) | |
Cattle egret (Bubulcus ibis) | Brazil | Fernando de Noronha | 197 | 157 | 79.7 | MAT | 1:5 | Costa et al. (2012) | |
Cattle egret (Bubulcus ibis) | Taiwan | Several | 7 | 4 | 57.1 | MATb | 1:40 | Chen et al. (2015) | |
Eurasian spoonbill (Platalea leucorodia) | Spain | Several | 81 | 5 | 6.2 | MAT | 1:25 | Cabezón et al. (2011) | |
Grey heron (Ardea cinerea) | Spain | Several | 5 | 3 | 60.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Malay night heron (Gorsachius melanolophus) | Taiwan | Several | 21 | 5 | 23.8 | MATb | 1:40 | Chen et al. (2015) | |
Purple heron (Ardea purpurea) | Spain | Several | 4 | 0 | 0 | MAT | 1:25 | Cabezón et al. (2011) | |
Roseate spoonbill (Platalea ajaja) | Czech Republic | Zoos | 6 | 1 | 16.6 | LATa | – | Bártová et al. (2018) | |
Phaethontiformes | |||||||||
Red-billed tropic bird (Phaeton aethereus) | Brazil | Abrolhos Archipelago | 25 | 7 | 28.0 | MAT | 1:5 | Gennari et al. (2016b) | |
Phoenicopteriformes | |||||||||
Lesser flamingo (Phoenicopterus minor) | Portugal | Zoo | 3 | 1 | 33.0 | MATb | 1:20 | Tidy et al. (2017) | |
Piciformes | |||||||||
Black vulture (Coragyps atratus) | Brazil | São Paulo | 121 | 16 | 13.2 | MAT | 1:5 | Gennari et al. (2017) | |
Black vulture (Coragyps atratus) | USA | Alabama | 8 | 1 | 12.0 | MAT | 1:25 | Love et al. (2016) | |
Crescent-chested puffbird (Malacoptila striata) | Brazil | São Paulo | 3 | 2 | 66.7 | MAT | 1:5 | Gennari et al. (2014) | |
Psittaformes | |||||||||
Alexandrine parakeets (Psittacula eupatria) | China | Beijing, Weifang | 61 | 4 | 6.5 | MAT | 1:5 | Season AS | Zhang et al. (2014) |
Black-goggled tanager (Lanio melanops) | Brazil | São Paulo | 15 | 5 | 33.3 | MAT | 1:5 | Gennari et al. (2014) | |
Black-headed gull (Chroicocephalus ridibundus) | China | Dianchi Lake | 659 | 131 | 19.9 | MAT | 1:5 | Miao et al. (2014) | |
Budgerigars (Melopsittacus undulatus) | China | Beijing, Weifang | 202 | 18 | 8.9 | MAT | 1:5 | Season AS | Zhang et al. (2014) |
Cockatiels (Nymphicus hollandicus) | China | Beijing, Weifang | 22 | 3 | 13.6 | MAT | 1:5 | Season AS | Zhang et al. (2014) |
Lovebirds (Agapornis sp.) | China | Beijing, Weifang | 26 | 1 | 3.8 | MAT | 1:5 | Season AS | Zhang et al. (2014) |
Rainbow lorikeet (Trichoglossus haematodus) | Czech Republic | Zoos | 4 | 1 | 25.0 | LATa | – | Bártová et al. (2018) | |
Red-tailed Amazon parrot (Amazona brasiliensis) | Brazil | Paraná | 51 | 0 | 0 | IFA | 1:16 | Sato et al. (2020) | |
Turquoise-fronted Amazon (Amazona aestiva) | Brazil | São Paulo | 71 | 7 | 10.0 | MAT | 1:16 | Gonçalves et al. (2013) | |
Sphenisciformes | |||||||||
Galapagos penguin (Spheniscus mendiculus) | Republic of Ecuador | Galapagos | 298 | 7 | 2.3 | MAT | 1:50 | Region AS | Deem et al. (2010) |
Humboldt penguin (Spheniscus humboldti) | Czech Republic | Zoos | 4 | 2 | 50.0 | LATa | – | Bártová et al. (2018) | |
Magellanic penguin (Spheniscus magellanicus) | Brazil | Bahia, Espírito Santo, Rio de Janeiro | 145 | 18 | 12.4 | MAT | 1:20 | Tg not isolated | Acosta et al. (2018) |
Magellanic penguin (Spheniscus magellanicus) | Brazil | Espírito Santo, Santa Catarina, São Paulo | 100 | 28 | 28.0 | MAT | 1:20 | Captive | Gennari et al. (2016a, 2016b) |
Magellanic penguin (Spheniscus magellanicus) | Chile | Magdalena Island | 132 | 57 | 43.2 | MAT | 1:20 | Acosta et al. (2019) | |
Struthioniformes | |||||||||
Greater rhea (Rhea americana) | Portugal | Zoo | 1 | 1 | 100.0 | MATb | 1:20 | Tidy et al. (2017) | |
Suliformes | |||||||||
Brown booby (Sula leucogaster) | Brazil | Abrolhos Archipelago | 19 | 9 | 47.4 | MAT | 1:5 | Gennari et al. (2016a, 2016b) | |
Masked booby (Sula dactylatra) | Brazil | Abrolhos Archipelago | 23 | 8 | 34.8 | MAT | 1:5 | Gennari et al. (2016a, 2016b) | |
Flightless cormorants (Phalacrocorax harrisi) | Republic of Ecuador | Galapagos | 258 | 6 | 2.3 | MAT | 1:50 | Tg isolated | Deem et al. (2010) |
Strigiformes | |||||||||
Barn owl (Tyto alba) | Brazil | São Paulo | 4 | 2 | 50.0 | MAT | 1:16 | Gonçalves et al. (2013) | |
Barn owl (Tyto alba) | Spain | Several | 45 | 6 | 13.3 | MAT | 1:25 | Cabezón et al. (2011) | |
Barred owl (Strix varia) | USA | Alabama | 54 | 25 | 46.2 | MAT | 1:25 | Tg isolated | Love et al. (2016) |
Burrowing owl (Athene cunicularia) | Brazil | Minas Gerais, São Paulo | 5 | 1 | 20.0 | MAT | 1:5 | Vitaliano et al. (2014) | |
Collard scops owl (Otus bakkamoena) | Taiwan | Several | 74 | 20 | 27.0 | MATb | 1:40 | Chen et al. (2015) | |
Common scops-owl (Otus scops) | Spain | Several | 4 | 1 | 25.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Eastern screech owl (Megascops asio) | USA | Alabama | 16 | 2 | 12.0 | MAT | 1:25 | Love et al. (2016) | |
Eurasian eagle owl (Bubo bubo) | Portugal | Central, northern | 3 | 1 | 33.3 | MATb | 1:20 | Lopes et al. (2011) | |
Eurasian eagle owl (Bubo bubo) | Spain | Several | 144 | 98 | 68.0 | MAT | 1:25 | Cabezón et al. (2011) | |
Grass owl (Tyto capensis) | Taiwan | Several | 20 | 3 | 15.0 | MATb | 1:40 | Chen et al. (2015) | |
Great horned owl (Bubo virginianus) | USA | Alabama | 28 | 13 | 46.4 | MAT | 1:25 | Love et al. (2016) | |
Little owl (Athene noctua) | Italy | Northern | 17 | 4 | 23.5 | MATb | 1:40 | Gazzonis et al. (2018) | |
Little owl (Athene noctua) | Spain | Several | 19 | 3 | 15.7 | MAT | 1:25 | Cabezón et al. (2011) | |
Long-eared owl (Asio otus) | Spain | Several | 9 | 1 | 11.1 | MAT | 1:25 | Cabezón et al. (2011) | |
Long-eared owl (Asio otus) | Taiwan | Several | 4 | 1 | 25.0 | MATb | 1:40 | Chen et al. (2015) | |
Short-eared owl (Asio flammeus) | Taiwan | Several | 11 | 1 | 9.0 | MATb | 1:40 | Chen et al. (2015) | |
Spotted owlet (Athene brama) | Pakistan | Punjab | 9 | 3 | 33.3 | LATb | 1:64 | Age, health AS | Naveed et al. (2019) |
Tawny owl (Strix aluco) | Italy | Northern | 12 | 1 | 8.3 | MATb | 1:40 | Gazzonis et al. (2018) | |
Tawny owl (Strix aluco) | Portugal | Central, northern | 5 | 1 | 20.0 | MAT | 1:20 | Lopes et al. (2011) | |
Tawny owl (Strix aluco) | Spain | Several | 38 | 5 | 13.6 | MAT | 1:25 | Cabezón et al. (2011) |
ELISA, enzyme-linked immunosorbent assay. Unless stated otherwise, ELISA=ELISA in-house; IFA, indirect fluorescent antibody test; IHA, indirect haemagglutination assay; LAT, latex agglutination test; MAT, modified agglutination test (Dubey and Desmonts, 1987); Tg, Toxoplasma gondii; AS, positive association; IHC, immunohistochemical.
ELISA Vekto-Toxo antibodies kits (Vektor-Best, Russian Federation); IHA (ImmunoHAI-Toxoplasmose, Wama Diagnostic, São Carlos, SP, Brazil); WAMA Diagnosis. Imuno-HAI; LAT Pastorex toxo, Bio-Rad Laboratories s.r.o., Prague, Czech Republic; MAT (New Life Diagnostic LLC, Carlsbad, CA, USA).
ELISA ID Screen Avian Toxoplasmosis Indirect (ID VET, France); IHA (Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, China); LAT Latex agglutination test (Antec Diagnostic Products, Bridport, Dorset, UK); MAT (Toxo-Screen DA®, Biomerieux, Lyon, France). This is the same test as MAT.
Carnivorous birds
Prevalence of T. gondii in carnivorous birds reflects the prevalence of the parasite in their prey. For example, owls consume hundreds of rodents yearly. In a recent survey of kestrels at an airport site in Italy, T. gondii antibodies were detected in 33.3% of kestrel trapped during 2016 and 14.3% of 91 kestrel during 2017; seroprevalence was lower in juveniles than in adults (Iemmi et al., 2020). Based on the remnants of animals in the feces of kestrels, rodents were a major component of the kestrel diet (Iemmi et al., 2020). In a large sample size of raptors in Spain, T. gondii antibodies were found in 51.0% of 96 common buzzard, 17.7% of 175 Griffon vulture and 17.0% of Spanish Imperial eagle (Cabezón et al., 2011). Among the raptors, vultures are considered resistant to clinical toxoplasmosis and other microbial infections in general. In 2 large surveys, T. gondii antibodies were found in 17.7% of 175 Gyps fulvus in Spain (Cabezón et al., 2011) but twice (39.6% of 101) more were infected in Israel (Salant et al., 2013); the results are comparable because modified agglutination test (MAT) at the serum dilution of 1:25 was used in both studies. Finding of T. gondii DNA in tissues of 43 of 48 (89.6%) wild birds (mostly carnivorous) in Turkey suggests a very high prevalence of the parasite in local rodents (Karakavuk et al., 2018). Of 281 raptors from a rehabilitation centre in the USA, 34.5% were seropositive with highest (46.0%) prevalence in Barred owl (Love et al., 2016)
Viable T. gondii was isolated (Table 2) and DNA demonstrated (Table 3) from several species of carnivorous birds. The highest prevalence of DNA was in Buteo buteo from Turkey; 23 (92.0%) of 25 were infected (Table 3).
Experimental infection of crested caracara with T. gondii
An experiment on caracara in Brazil provided useful information. Caracaras are raptors/scavengers with wide distribution. Eight caracaras that could not be released from a rehabilitation centre were used in this experiment. They were serologically negative to T. gondii by IFA (cut-off 1:40). Five caracaras were fed rodent (Calomys callosus) infected with Me49 strain of T. gondii. The birds were euthanized 68 days p.i. Blood was collected for serological examination weekly or more often. Seroconversion occurred between 5 and 14 days p.i. The serological response was erratic. In 1 bird (No.6), transient antibody was observed on day 14 and then at 45 days p.i. The highest antibody titer was 1:650. Antibodies became undetectable at 68 days p.i. in 2 birds. By immunohistochemistry, T. gondii was detected in the hearts and muscles of all 5 caracaras and demonstrated by bioassay in the hearts of 2 birds. Three control caracaras not inoculated with T. gondii remained serologically negative to T. gondii (Vitaliano et al., 2010).
Herbivorous/insectivorous birds
Seroprevalence varied depending on the geography, host and the habitat (Table 7). For example, in the ground feeding pigeon (Columba livia), seroprevalences varied from 1.6 to 35.7% (Table 7). In a large sample size of pigeons, a low prevalence (1.9% of 521) was reported; the pigeons were from Durango City, Mexico that has a dry climate (Alvarado-Esquivel et al., 2011). This low prevalence is likely related to the effect of climate on oocyst survival. In another survey from cold climate, only 3.9% of pigeons from Colorado, USA were seropositive (Dubey et al., 2010). Toxoplasma gondii antibodies were detected in 11.8% of 35 pigeons and 9.5% of 620 quails that were destined for human consumption in China (Cong et al., 2012, 2017a). Finding of T. gondii DNA in the muscles of 6.4% of 390 quails indicates that the parasite was present in these birds destined for human consumption (Cong et al., 2017b). Similarly, T. gondii DNA was detected in 5.4% of 280 wild ducks and 3.4% of 350 common pheasants hunted for human consumption in the Czech Republic (Skorpikova et al., 2018).
Toxoplasma gondii infection in sea gulls and other scavenging birds indicates contamination of marine/lake waters with oocysts. In one study, 22.8% of 479 yellow-legged gulls (Larus michahellis) were seropositive to T. gondii (Cabezón et al., 2016). In another investigation, T. gondii antibodies (assessed by ELISA) were detected in 233 of 1122 freshly laid L. michahellis eggs (Gamble et al., 2019). The freshness of eggs was verified by immersion in water; such eggs do not float in water (Gamble et al., 2019). The occurrence of T. gondii antibodies in 4 other species of sea birds (Sula spp. and Phaeton spp.) from Brazil (Gennari et al., 2016b) and in 19.9% of 659 black-headed gulls (Chroicocephalus ridibundus) in China (Miao et al., 2014) indicates that T. gondii infection is common in sea birds. Toxoplasma gondii oocysts from feline feces can be washed into sewage and freshwater run-off and contaminate marine waters. Antibodies to T. gondii were detected in 8.5% of 632 mute swans (Cygnus olor) from the USA and viable T. gondii was isolated from hearts of 3 (Dubey et al., 2013). Mute swan is an invasive species present in US waters; infection in these hosts is indicative of oocyst contamination.
Reports of viable T. gondii and parasite DNA from tissues of wild birds are summarized in Tables 2 and 3, respectively.
Experimental infection of pigeons with T. gondii
Little information is available concerning the efficacy of different diagnostic methods for the detection of T. gondii infection in wild birds. A diagnostically useful experimental study was conducted in pigeons in Brazil (de Godoi et al., 2010). Sixteen seronegative pigeons (C. livia) were inoculated orally with 50 oocysts of the T. gondii VEG strain and divided into 4 groups of 4 pigeons each and euthanized at 15, 30, 45 and 60 days p.i. One pigeon died of toxoplasmosis on day 23 p.i. and tissue cysts were found in its brain; other pigeons remained healthy. All pigeons were seronegative by the MAT (cut-off 1:5) and IFA (cut-off 1:4) before feeding oocysts and developed antibody titers of more than 1:4000 by both MAT and IFA. Tissues (brain, heart, muscle) were tested by bioassay in mice and by PCR. Viable T. gondii was isolated from 5 of 12 pigeons and DNA was detected by nested PCR in tissues of 7 of 12 pigeons. By serology and bioassay, none of the 160 naturally exposed pigeons were positive for T. gondii providing further evidence of the validity of serology (de Godoi et al., 2010).
Migratory birds
Toxoplasma gondii infections in migratory birds are of epidemiological significance because the parasite can be transported with the host and the introduction of T. gondii in new geographic locations can disturb the equilibrium (Gennari et al., 2014). For example, ToxoDB genotype #9 (Chinese 1) occurs mainly in China but has been occasionally found in other countries, including the USA and Mexico. Whether migratory birds could have transported the parasite is a possibility. Antibodies to T. gondii were detected in Magellanic penguins in Chile and these birds migrate throughout South American coastline (Acosta et al., 2018, 2019).
A study of migratory and non-migratory geese revealed interesting results (Sandström et al., 2013). A total of 2675 birds, both adults and juveniles, of 4 goose species (Anser anser, n = 266; A. brachyrhynchus, n = 787; Branta canadensis, n = 79; B. leucopsis, n = 1543) at Arctic brood-rearing areas in Russia and on Svalbard, and temperate wintering grounds in the Netherlands and Denmark (migratory populations) as well as temperate brood-rearing grounds (the Netherlands, non-migratory populations) were tested for T. gondii antibodies (MAT, 1:40). Only adult B. leucopsis were seropositive: T. gondii antibodies were found in 14.8% of 811 adults from Svalbard and 17.7% of 157 from Russia sampled during summer but not in any of the 456 juveniles sampled in summer (Arctic) and summer and winter in the Netherlands. Similar results were obtained with 3 other species of goose (Sandström et al., 2013). The authors concluded that geese become infected postnatally at wintering groups.
In a study of migratory birds and resident Nearctic brown lemmings (Lemmus trimucronatus) from Arctic Canada, T. gondii infections were detected only in migratory geese (Table 1) and not in resident lemmings (Elmore et al., 2015).
Clinical toxoplasmosis in wild birds
Little is known of clinical toxoplasmosis among wild birds in nature. Among all avian species, most severe toxoplasmosis has been reported in canaries (Serinus canaria), Hawaiian geese (Branta sandvicensis) and Hawaiian crows (Corvus hawaiiensis); reports between 1988 and 2009 were summarized previously (Dubey, 2010). In the past decade, few cases of fatal toxoplasmosis were documented in captive birds or those from National Parks (Table 8).
Table 8.
Host | Country | Observations | Diagnostic method | Remarks | Reference |
---|---|---|---|---|---|
Bar-shouldered dove (Geopelia humeralis) | France | A 6-year-old dove born in the zoo was found dead. Pneumonia was the main lesion and only lungs were studied histologically. Numerous tachyzoites were seen in lesions. Diagnosis was confirmed ultrastructurally | Histopathology and TEM | – | Rigoulet et al. (2014) |
Black-footed penguin (Spheniscus demersus) | The Netherlands | 3 captive penguins in a zoo died within a day after neurological signs were observed. All 3 had similar lesions. Liver, lungs, intestines, and brain had intralesional tachyzoites. Diagnosis confirmed by IHC and TEM | Histopathology, IHC, TEM | – | Ploeg et al. (2011) |
Guinea fowl (Numida meleagris) | Brazil | Nine of 29 guinea fowl on a farm became ill and 6 died. Two guinea fowl were necropsied. Both birds had disseminated toxoplasmosis with intralesional T. gondii. One of the 2 sera tested had a MAT titer of 1:1280. Diagnosis was confirmed by IHC | Serology, histopathology, IHC | – | Vielmo et al. (2019) |
Kereru (Hemiphaga novaeseelandiae) | New Zealand | 2 kererus were found dead in a wildlife park. Pneumonia was the main lesion in both birds. Tachyzoites and tissue cysts were associated with lesions | Histopathology, IHC | Limited genotyping revealed atypical Type II | Howe et al. (2014) |
Lovebird (Agapornis roseicollis) | Australia | A female pet bird developed ataxia 1 year after being caged. It had head tilt, tremors and was euthanized. The most important histologic findings were enlargement of spleen, encephalitis and cerebral haemorrhage | IHC, PCR | ToxoDB genotype #3 (Type II) DNA isolated from frozen brain sample | Cooper et al. (2015) |
North Island brown kiwi (Apteryx mantelli) | New Zealand | A juvenile hand raised kiwi was found dead. Most important lesion was hepatitis with tissue cysts. Lesions were seen in other organs, but protozoa were not identified | Histopathology, IHC | Limited genotyping revealed atypical Type II | Howe et al. (2014) |
North Island kaka (Nestor meridionalis) | New Zealand | 1 kaka was found dead in wild. Most important lesion was hepatitis with tissue cysts. Lesions were seen in other organs, but protozoa were not identified | Histopathology, IHC | Limited genotyping revealed atypical Type II | Howe et al. (2014) |
Valley quail (Callipepla californica) | Brazil | A captive raised quail recently acquired from another facility died suddenly with clinical signs of diarrhoea and dyspnoea. Disseminated toxoplasmosis involving most organs, many tachyzoites present | IHC, PCR, T. gondii DNA in many tissues | T. gondii DNA from kidney genotyped with 10 PCR-RFLP markers revealed ToxoDB genotype #87 | Casagrande et al. (2015) |
IHC, immunohistochemistry; PCR, polymerase chain reaction; TEM, transmission electron microscopy; PCR-RFLP, Restriction fragment length polymorphism.
Hawaiian crows (C. hawaiiensis) and Nene goose (B. sandvicensis) are endangered native species in Hawaii. Nene is the largest extant terrestrial bird in Hawaiian Island and the official state bird (Work et al., 2015). Of 300 Nene examined at necropsy, inflammatory conditions were found in 69 and 16.0% of these were thought to be toxoplasmosis (Work et al., 2015). Thus, 11 geese died of toxoplasmosis. The presence of cats in colonies near the native bird sites is thought to be a source of T. gondii oocysts for the birds (Lepczyk et al., 2020).
Two episodes of clinical toxoplasmosis were reported in guinea fowl in the USA and Brazil. An owner in Mississippi, USA lost 7 of 20 backyard guinea fowls. Birds were lethargic before death. Two dead birds were necropsied. Severe lesions of multifocal necrosis, fibrin exudation and inflammation of spleen, lung, heart and bone marrow were seen microscopically in 1 and mild lesions in the other guinea fowl. Toxoplasma gondii was identified histologically in tissues of both birds and the diagnosis was confirmed by PCR (Jones et al., 2012).
The Brazilian outbreak of clinical toxoplasmosis was reported in guinea fowl on a chicken farm; the farm had 47 chickens (G. domesticus) and 29 guinea fowl (Vielmo et al., 2019). Of these 76 birds, 22 (13 chickens and 9 guinea fowl) had clinical signs and 15 (9 chickens, 6 guinea fowl) died. Two guinea fowl were examined at necropsy and both had toxoplasmosis (Table 8).
Genetic diversity of T. gondii isolates
PCR-RFLP genetic data based on extraction of DNA from host tissue are summarized in Table 9 and from the live tachyzoites in Table 10. A total of 102 samples from birds were genotyped in this summary (Table 10), including 75 from viable T. gondii isolates (Table 2) and 27 from DNA extracted from tissues of birds (Table 10). Overall, genotype distribution follows the global patterns recognized previously (Shwab et al., 2014; Su and Dubey, 2020), with ToxoDB genotypes #1 and #3 (collectively known as Type II), and genotype #2 (known as Type III) being dominant in Africa and Europe. Most genotypes identified in the Americas were diverse and different from those in the Old World. Of interest is the predominance of ToxoDB genotype #9 (Chinese 1) in China and its rare occurrence in Mexico (Alvarado-Esquivel et al., 2011; Shwab et al., 2014). Type I isolates (ToxoDB genotype #10) are considered rare worldwide. It was detected in a hunted turkey in 4 tree sparrows in China (Table 3). As this genotype is highly virulent to mice and relatively easy to isolate by bioassay, future study to obtain isolates for genotyping is needed to confirm the findings. Also, of interest is the finding of ToxoDB genotypes #4 and #5, together known as Type 12, in North America but their rare frequency from the rest of the world.
Table 9.
Country | Host | No. | 10 PCR-RFLP markers ToxoDB genotype | Reference |
---|---|---|---|---|
China | Alauda gulgula | 2 | #3 | Cong et al. (2014) |
China | Anas formosa | 2 | #9 | Zhang et al. (2015) |
China | Anas sp. | 1 | #9 | Zou et al. (2017) |
China | Carduelis spinus | 2 | #3 | Cong et al. (2014) |
China | Coturnix coturnix | 5 | #9 | Cong et al. (2017a, 2017b) |
China | Passer domesticus | 1 | #3 | Huang et al. (2012) |
China | Passer domesticus | 4 | #3 in 3 and possible new type in 1 | Cong et al. (2013) |
China | Phasianus colchicus | 1 | #3 | Huang et al. (2012) |
China | Passer montanus | 1 | #10 | Huang et al. (2012) |
China | Passer montanus | 3 | #10 | Liu et al. (2019) |
Israel | Corvus cornix | 1 | #1 | Salant et al. (2013) |
South Africa | Streptopelia semitorquata | 1 | #1 or #3 (15 microsatellites) | Lukášová et al. (2018) |
USA | Branta sandvicensis | 4 | #261 in 3, #262 in 1 | Work et al. (2016) |
Table 10.
Continent/country | Total typed | I ToxoDB #10 | Classic types | III ToxoDB#2 | #4 | #5 | #6 | #9 | #11 | #20 | Others | |
---|---|---|---|---|---|---|---|---|---|---|---|---|
II ToxoDB #1 or #3 | ||||||||||||
Africa | ||||||||||||
Senegal | 15 | 5 | 1 | 3 | 6 | Galal et al. (2019) | ||||||
Asia | ||||||||||||
China | (22)a | 4 | 9 | 8 | 1 Possible new type | See Table 9 | ||||||
Israel | (1)a | 1 | Salant et al. (2013) | |||||||||
Oceania | ||||||||||||
Australia | 1 | 1 | Cooper et al. (2015) | |||||||||
Europe | ||||||||||||
France | 1 | 1 | Aubert et al. (2010) | |||||||||
Turkey | 9 | 7 | 2 | Karakavuk et al. (2018) | ||||||||
Central America | ||||||||||||
Costa Rica | 1 | 1 (#52) | Dubey et al. (2009), Shwab et al. (2014) | |||||||||
South America | ||||||||||||
Brazil | 19 | 5 | 1 | 1 | 12 (#8-1, #13-2, #17-1, #65-1, #108-1, #161-1, #182-2, #206-1, #290-2) | da Silva and Langoni (2016), de Barros et al. (2014), Dubey et al. (2011b), Rêgo et al. (2018), Silva et al. (2018a, 2018b) | ||||||
North America | ||||||||||||
Mexico | 1 | 1 | Alvarado-Esquivel et al. (2011), Shwab et al. (2014) | |||||||||
USA | 32(4)a | 1 | 6 | 4 | 2 | 6 | 13 (#15-1, #157-1, #167-1, #177-2, #216-2, # 61-3, #262-1, #266-1, #267-1) | Cerqueira-Cézar et al. (2019), Dubey et al. (2010), Dubey et al. (2011b), Dubey et al. (2013), Love et al. (2016), Shwab et al. (2014), Verma et al. (2016), Yu et al. (2013) | ||||
Grand total | 102 | 5 | 35 | 7 | 2 | 6 | 4 | 9 | 1 | 6 | 27 |
DNA from tissues. Twenty-seven of the 102 samples were DNA from bird tissues.
Conclusions
Here, we summarized seroprevalence, clinical disease, epidemiology and genetic diversity of T. gondii strains isolated from wild birds worldwide for the past decade. It is obvious that T. gondii infection in raptors is common and they are excellent sentinels to monitor T. gondii in rodents and small other animals. Detection of T. gondii antibodies in eggs offers a non-invasive sampling method. In one investigation, T. gondii antibodies (assessed by ELISA) were detected in 233 of 1122 freshly laid yellow-legged gulls (L. michahellis) eggs (Gamble et al., 2019). Finding antibodies in sea gulls indicates contamination of fresh and marine waters with T. gondii oocysts. In general, T. gondii infection in herbivorous birds is a good measure of oocyst contamination in the environment. Genetic studies revealed low genetic diversity in Europe, Asia, Africa and the USA, but higher diversity of T. gondii in South America. A study of migratory and non-migratory geese at Arctic brood-rearing areas in Russia and on Svalbard, and temperate wintering grounds in the Netherlands and Denmark (migratory populations) revealed that geese become infected postnatally at wintering groups (Sandström et al., 2013).
Acknowledgements
This research was supported in part by an appointment of Camila K. Cerqueira-Cézar and Fernando H. A. Murata to the Agricultural Research Service (ARS) Research Participation administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement between the US Department of Energy (DOE) and the US Department of Agriculture (USDA). ORISE was managed by ORAU under DOE contract number DE-SC 0014664. All opinions expressed in this paper were the authors' and did not necessarily reflect the policies and views of USDA, ARS, DOE or ORAU/ORISE. We thank Dr Yurong Yang for help with Chinese references.
Financial support
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
Ethical standards
Not applicable.
Conflict of interest
None.
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