Veterinary Parasitology 200 (2014) 233–241 Contents lists available at ScienceDirect Veterinary Parasitology jo u r nal homep age: www.elsevier.com/locate/vetpar Review Visceral leishmaniasis in zoo and wildlife Tayse Domingues Souza a,c , Andréia Pereira Turchetti a , Ricardo Toshio Fujiwara b,c , Tatiane Alves Paixão b,c , Renato Lima Santos a,c,∗ a Departamento de Clínica e Cirurgia Veterinárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte 31270-901, Minas Gerais, Brazil b Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte 31270-901, Minas Gerais, Brazil c Departamento de Patologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte 31270-901, Minas Gerais, Brazil a r t i c l e i n f o Article history: Received 7 November 2013 Received in revised form 23 December 2013 Accepted 23 December 2013 Keywords: Leishmania infantum Visceral leishamniasis Wildlife a b s t r a c t Visceral leishmaniasis (VL) is an emerging zoonosis caused by Leishmania (Leishmania) infantum. Although the domestic dog is the main vertebrate host, many zoo and wild mam- mal species have been diagnosed with L. infantum infection, especially in endemic areas. There are many available diagnostic approaches, including serological, parasitological and molecular tests. Among wild animals, carnivores and primates are more often clinically affected, with some species, such as the bush dog (Speothos venaticus) being especially sus- ceptible to development of clinical signs. There are also reports and research articles of VL in felids, rodents, and marsupials. This work aims to review the occurrence of VL in zoo and wildlife and raise awareness of its importance in the field of conservational veterinary medicine. © 2014 Elsevier B.V. All rights reserved. Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233 2. Visceral leishmaniasis in zoo and wild animals — diagnostic methods and pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234 3. Leishmania infection in zoo and wild carnivores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234 4. Visceral leishmaniasis in other wild mammalian species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237 5. Epidemio-ecological implications and concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240 1. Introduction Visceral leishmaniasis (VL) is an important systemic, often fatal, emerging zoonosis with a broad geographic ∗ Corresponding author at: Departamento de Clínica e Cirurgia Veter- inárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte 31270-901, Minas Gerais, Brazil. Tel.: +55 3134092239; fax: +55 3134092230. E-mail address: [email protected] (R.L. Santos). distribution, particularly in tropical and Mediterranean regions. The causative agent is Leishmania (Leishmania) infantum (synonym L. chagasi), a protozoan belonging to the L. donovani complex of the Order Kinetoplastida and Family Trypanosomatidae (Baneth et al., 2008). The dis- ease is primarily transmitted by phlebotomine sand flies of the genus Phlebotomus in the Old World and Lutzomyia in the Americas. Importantly, sexual, vertical and iatrogenic transmission has been reported (Morillas-Marquez et al., 2002; Pangrazio et al., 2009; Silva et al., 2009). 0304-4017/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.vetpar.2013.12.025
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Veterinary Parasitology 200 (2014) 233– 241
Contents lists available at ScienceDirect
Veterinary Parasitology
jo u r nal homep age: www.elsev ier .com/ locate /vetpar
eview
isceral leishmaniasis in zoo and wildlife
ayse Domingues Souzaa,c, Andréia Pereira Turchetti a,icardo Toshio Fujiwarab,c, Tatiane Alves Paixãob,c, Renato Lima Santosa,c,∗
Departamento de Clínica e Cirurgia Veterinárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627,elo Horizonte 31270-901, Minas Gerais, BrazilDepartamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627,elo Horizonte 31270-901, Minas Gerais, BrazilDepartamento de Patologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627,elo Horizonte 31270-901, Minas Gerais, Brazil
a r t i c l e i n f o
rticle history:eceived 7 November 2013eceived in revised form3 December 2013ccepted 23 December 2013
a b s t r a c t
Visceral leishmaniasis (VL) is an emerging zoonosis caused by Leishmania (Leishmania)infantum. Although the domestic dog is the main vertebrate host, many zoo and wild mam-mal species have been diagnosed with L. infantum infection, especially in endemic areas.There are many available diagnostic approaches, including serological, parasitological andmolecular tests. Among wild animals, carnivores and primates are more often clinically
eywords:eishmania infantumisceral leishamniasisildlife
affected, with some species, such as the bush dog (Speothos venaticus) being especially sus-ceptible to development of clinical signs. There are also reports and research articles of VLin felids, rodents, and marsupials. This work aims to review the occurrence of VL in zooand wildlife and raise awareness of its importance in the field of conservational veterinarymedicine.
© 2014 Elsevier B.V. All rights reserved.
ontents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2332. Visceral leishmaniasis in zoo and wild animals — diagnostic methods and pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2343. Leishmania infection in zoo and wild carnivores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2344. Visceral leishmaniasis in other wild mammalian species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2375. Epidemio-ecological implications and concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 240
. Introduction distribution, particularly in tropical and Mediterranean
Visceral leishmaniasis (VL) is an important systemic,ften fatal, emerging zoonosis with a broad geographic
∗ Corresponding author at: Departamento de Clínica e Cirurgia Veter-nárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Av.ntônio Carlos 6627, Belo Horizonte 31270-901, Minas Gerais, Brazil.el.: +55 3134092239; fax: +55 3134092230.
E-mail address: [email protected] (R.L. Santos).
304-4017/$ – see front matter © 2014 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.vetpar.2013.12.025
regions. The causative agent is Leishmania (Leishmania)infantum (synonym L. chagasi), a protozoan belonging tothe L. donovani complex of the Order Kinetoplastida andFamily Trypanosomatidae (Baneth et al., 2008). The dis-ease is primarily transmitted by phlebotomine sand flies of
the genus Phlebotomus in the Old World and Lutzomyia inthe Americas. Importantly, sexual, vertical and iatrogenictransmission has been reported (Morillas-Marquez et al.,2002; Pangrazio et al., 2009; Silva et al., 2009).
y Parasit
234 T.D. Souza et al. / VeterinarThe disease has been diagnosed in several parts of theworld with an increasing frequency in recent decades. Orig-inally distributed within the Mediterranean coast, Europeand Asia, the protozoan was introduced in the Ameri-cas during the colonization process (Kuhls et al., 2011).Historically, once established in a new area, the diseasebecomes endemic and its control has proven to be verychallenging (Diniz et al., 2008; Petersen, 2009). Microsatel-lite analysis of 98 strains of L. infantum from seven Southand Central American countries were compared to pro-files of 308 L. infantum strains from different countries inSouthern Europe, North Africa, Middle East, and Asia. Thesestrains have been isolated from humans, dogs or wild ani-mals, namely Cerdocyon thous and Didelphis marsupialis.The results indicate that L. infantum was introduced in theNew World by multiple waves of immigration from Euro-pean countries and the strains from wild animals did notdiffer from those isolated from humans or domestic ani-mals (Kuhls et al., 2011).
VL has been documented in several mammalian species,including carnivores (Beck et al., 2008; Luppi et al.,2008), primates (Malta et al., 2010), marsupials (Santiagoet al., 2007), edentates (Araújo et al., 2013), lagomorphs(Molina et al., 2012), bats (Lima et al., 2008), rodents(Papadogiannakis et al., 2010), and horses (Rolão et al.,2005). Although the domestic dog is the most importantvertebrate host and the main reservoir for human VL,several wild mammal species are susceptible to L. infan-tum infection. Wild animals are subjected to challengesimposed directly or indirectly by anthropic influencethat impacts ecosystems and may exposure wildlife topathogens, which under some circumstances may lead toor increase the risk of extinction of a given species. Impor-tantly, wild animal health reflects environmental healthand may serve as an indicator of human risk of exposureto zoonosis in that environment (Aguirre, 2009). There-fore, the importance of wild animals as “sentinels” mustbe considered, although analytical methods for linking ani-mal and human data, thus predicting human risk are stillunderdeveloped (Scotch et al., 2009). Zoo animals main-tained in captivity in endemic urban environments areunder high risk of infection, and therefore diagnostic testsare advised for prevention and control of the disease inzoo populations, especially when exchanging or introduc-ing susceptible animals (Malta et al., 2010; Jusi et al., 2011;Libert et al., 2012).
2. Visceral leishmaniasis in zoo and wild animals —diagnostic methods and pathology
As occurs in man and domestic dogs, infected wild mam-mals may be symptomatic or asymptomatic. The diseasedevelops similarly in domestic and wild mammals. Com-mon necropsy findings in wild animals with VL includegross changes that are commonly seen in domestic dogssuch as emaciation, pale mucous membranes, liver enlarge-ment and discoloration, splenomegaly, lymphadenopathy.
Additionally, less specific changes may also be observedincluding pulmonary congestion and edema, hemorrhagesin skin, lung, heart, and intestines (Beck et al., 2008; Luppiet al., 2008; Malta et al., 2010). Cutaneous crusts, ulcers andology 200 (2014) 233– 241
alopecia may be observed particularly in canids (Beck et al.,2008; Luppi et al., 2008; Souza et al., 2010).
Microscopically, a macrophage infiltrate containingintracytoplasmic amastigotes is usually present in manyorgans (lymph nodes, spleen, liver, kidney, lung, and smallintestine) along with plasma cells and lymphocytes (Becket al., 2008; Luppi et al., 2008; Malta et al., 2010) (Fig. 1).As frequently observed in domestic canids, membrano-proliferative glomerulonephritis has been described in abush dog (S. venaticus) with VL (Luppi et al., 2008) (Fig. 1).
Diagnostic methods currently applied to wild animalsinclude serological assays such as indirect immuno-fluorescence (IFA), enzyme-linked immunosorbent assay(ELISA) (Luppi et al., 2008), fucose–mannose ligant-ELISA (FML-ELISA) (Santiago et al., 2007), immunochro-matographic strip assays (ICT) (Molina et al., 2012;Rosypal et al., 2010), direct agglutination test (DAT)(Mohebali et al., 2005), and Western blot (WB) (Sobrinoet al., 2008). In addition, molecular assays have beenemployed for the diagnosis of Leishmania infection,including in situ hybridization (Oliveira et al., 2005),polymerase chain reaction—PCR (Luppi et al., 2008),real-time quantitative PCR—qPCR (Sastre et al., 2008),PCR-restriction fragment length polymorphism—PCR-RFLP(Souza et al., 2010), among other methods including cul-ture (Figueiredo et al., 2008), direct parasitological analysis(Lima et al., 2009), histopathology and immunohistochem-istry (Malta et al., 2010).
3. Leishmania infection in zoo and wild carnivores
The Carnivora order includes many wild species thatare susceptible to VL. Serological and molecular surveysof L. infantum in wild animals from different parts of theworld have been published, and natural disease has beendescribed in free-ranging and captive wild canids (Sastreet al., 2008; Beck et al., 2008; Luppi et al., 2008; Souza et al.,2010; Libert et al., 2012). Table 1 summarizes reports ofLeishmania infection in wild animal from several regionsin the world.
There are several reports of Leishmania infections inwild canids in Europe. Gray wolves (Canis lupus), whichare considered a wild reservoir host for L. infantum, redfoxes (Vulpes vulpes), Egyptian mongooses (Herpestes ich-neumon), genets (Genetta genetta), and Iberian lynxes (Lynxpardinus), pine martens (Martes martes), and beech martens(Martes foina) have been diagnosed as asymptomatic car-riers in Spain and Portugal (Sastre et al., 2008; Sobrinoet al., 2008; Millán et al., 2011; Munoz-Madrid et al., 2013;Criado-Fornelio et al., 2000). Diagnosis of Leishmania sp.infection in red foxes (V. vulpes) has also been reportedin Italy and France (Mancianti et al., 1994; Dipineto et al.,2007; Davoust et al., 2014), as well as a report of aLeishmania-infected gray wolf (C. lupus) from Croatia (Becket al., 2008).
There has also been a few reports of Leishmania infec-tion in wild canids in the Middle East and North Africa,
including jackals (Canis aureus) from Iran, Israel, and Alge-ria (Shamir et al., 2001; Mohebali et al., 2005; Bessad et al.,2012), and foxes (V. vulpes) and wolves (C. lupus) from Iran(Mohebali et al., 2005).
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Table 1Reported Leishmania infantum infection in wild and zoo animals.
Order/Family Species Positive/total tested (%) Method1 Sample2 Country References
Carnivora/Canidae Bush dog (Speothos venaticus) 1/1 (100.0%) Culture/histopathology Skin Brazil Figueiredo et al. (2008)Bush dog (Speothos venaticus) 1/1 (100.0%) PCR, IHC, histopathology Several tissues Brazil Luppi et al. (2008)Bush dog (Speothos venaticus) 2/2 (100.0%) ELISA Serum Brazil Lima et al. (2009)
2/2 (100.0%) Cytology LN1/1 (100.0%) PCR Liver/LN
Bush dog (Speothos venaticus) 1/1 (100.0%) PCR-RFLP LN/skin/BM Brazil Souza et al. (2010)Bush dog* (Speothos venaticus) 1/2 (50.0%) IFA/ELISA Serum Brazil Jusi et al. (2011)
0/2 (0.0%) PCR/culture Tissues/blood/BMCrab-eating fox (Cerdocyon thous) 29/37 (78.4%) ELISA Serum Brazil Courtenay et al. (2002)
8/35 (22.9%) PCR BM8/21 (38.1%) Culture BM
Crab-eating fox (Cerdocyon thous) 2/12 (16.6%) IFA, ELISA Serum Brazil Curi et al. (2006)Crab-eating fox (Cerdocyon thous) 1/1 (100.0%) IFA, ELISA Serum Brazil Luppi et al. (2008)Crab-eating fox (Cerdocyon thous) 6/6 (100.0%) PCR-RFLP LN, BM, skin Brazil Souza et al. (2010)Crab-eating fox (Cerdocyon thous) 1/3 (33.3%) IFA/ELISA Serum Brazil Jusi et al. (2011)
1/3 (33.3%) PCR Tissues0/3 (0.0%) PCR/culture Blood/BM
Gray wolf (Canis lupus) 2/33 (6.0%) Serology Blood Spain and Portugal Sastre et al. (2008)3/33 (9.0%) PCR Blood
Gray wolf (Canis lupus) 8/39 (20.5%) PCR Spleen or blood Spain Sobrino et al. (2008)Gray wolf (Canis lupus) 1/1 (100.0%) PCR LN Croatia Beck et al. (2008)
1/1 (100.0%) Histology/cytology Several tissuesGray wolf (Canis lupus) 1/10 (10.0%) Culture/PCR-RFLP Spleen Iran Mohebali et al. (2005)
1/10 (10.0%) DAT, ELISA, IFA SerumGray wolf (Canis lupus) 2/49 (4.1%) PCR Hair Spain Munoz-Madrid et al. (2013)Hoary zorros (Lycalopex vetulus) 2/6 (33.3%) IFA, ELISA Serum Brazil Luppi et al. (2008)
2/2 (100.0%) PCR BM1/1 (100.0%) Cytology LN
Jackals (Canis aureus) 3/46 (6.4%) ELISA Serum Israel Shamir et al. (2001)Jackals (Canis aureus) 1/10 (10.0%) Culture/PCR-RFLP Spleen Iran Mohebali et al. (2005)
1/10 (10.0%) DAT, ELISA, IFA SerumJackals (Canis aureus) 1/2 (50.0%) IFA Serum Algeria Bessad et al. (2012)
1/2 (50.0%) PCR and culture Spleen, BMManed wolf (Chrysocyon brachyurus) 2/7 (28.6%) IFA, ELISA Serum Brazil Curi et al. (2006)Maned wolf (Chrysocyon brachyurus) 1/7 (14.3%) IFA, ELISA Serum Brazil Luppi et al. (2008)
1/1 (100.0%) PCR BMManed wolf (Chrysocyon brachyurus) 1/2 (50.0%) IFA/ELISA Serum Brazil Jusi et al. (2011)
1/2 (50.0%) PCR Skin0/2 (0.0%) PCR/Culture Blood/BM
Maned wolf (Chrysocyon brachyurus) 1/10 (10.0%) IFA, ELISA Serum Brazil Curi et al. (2012)Red fox (Vulpes vulpes) 9/50 (18.0%) IFA and ELISA Serum Italy Mancianti et al. (1994)Red fox (Vulpes vulpes) 50/67 (74.6%) PCR Spleen Spain Criado-Fornelio et al. (2000)Red fox (Vulpes vulpes) 1/10 (10.0%) Culture/PCR-RFLP Spleen Iran Mohebali et al. (2005)
1/10 (10.0%) DAT and ELISA Serum0/10 (0.0%) IFA Serum
Red fox (Vulpes vulpes) 50/20 (40%) PCR BM, LN, skin Italy Dipineto et al. (2007)Red fox (Vulpes vulpes) 23/162 (14.1%) PCR Spleen or blood Spain Sobrino et al. (2008)
1/47 (2.1%) WB Serum
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Table 1 (Continued)
Order/Family Species Positive/total tested (%) Method1 Sample2 Country References
Red fox (Vulpes vulpes) 6/9 (66.6%) PCR Hair Spain Munoz-Madrid et al. (2013)Red fox (Vulpes vulpes) 8/92 (8.7%) PCR Spleen, liver France Davoust et al. (2014)Fennec fox (Vulpes zerda) 1/1 (100.0%) Histopathology Several tissues USA Conroy et al. (1970)
Carnivora/Felidae Barbary lions (Panthera leo leo) 2/5 (40.0%) IFA Serum France Libert et al. (2012)2/5 (40.0%) PCR Blood
Feral cats (Felis catus) 13/83 (15.7%) WB Serum Spain Millán et al. (2011)19/73 (26.0%) PCR Spleen
Iberian lynx (Lynx pardinus) 1/4 (25.0%) PCR Spleen or blood Spain Sobrino et al. (2008)Jaguar (Panthera onca) 1/5 (20.0%) PCR-RFLP Blood and LN Brazil Dahroug et al. (2010)Puma (Puma concolor) 5/7 (71.4%) PCR-RFLP Blood and LN Brazil Dahroug et al. (2010)
Carnivora/Herpestidae Egyptian mongoose (Herpestes ichneumon) 2/7 (28.6%) PCR Blood or spleen Spain Sobrino et al. (2008)
Carnivora/Mustelidae Pine martens (Martes martes) 9/23 (39.1%) PCR Blood or spleen Spain Millán et al. (2011)Beech martens (Martes foina) 3/3 (100.0%) PCR Hair Spain Munoz-Madrid et al. (2013)
Carnivora/Viverridae Genets (Genetta genetta) 1/4 (25.0%) PCR Blood or spleen Spain Sobrino et al. (2008)Genets (Genetta genetta) 1/10 (10.0%) PCR Blood or spleen Spain Millán et al. (2011)
Chiroptera/Phillostomidae Bat (Carollia perspicillata) 1/8 (12.5%) Culture/PCR Blood Venezuela Lima et al. (2008)
Chiroptera/(4 families) Bats (28 species) 3/659 (0.4%) PCR Spleen and liver Brazil Savani et al. (2010)
Didelphimorphia/Didelphidae Opossum (Didelphis albiventris/Didelphis aurita) 21/112 (18.8%) Culture BM Brazil Santiago et al. (2007)18/112 (16.1%) Cytology BM103/112 (91.6%) PCR BM76/107 (71.0%) ELISA Serum18/72 (25.0%) FML-ELISA Serum
Didelphimorphia/Didelphidae Opossum (Didelphis sp.) 24/111 (21.6%) IFA Serum Brazil Schallig et al. (2007)10/111 (9.0%) DAT Serum1/20 (5.0%) PCR Blood
Erinaceomorpha/Erinaceidae Hedgehog (Erinaceus europaeus) 1/1 (100.0%) PCR Hair Spain Munoz-Madrid et al. (2013)
Lagomorpha/Leporidae Iberian hare (Lepus granatensis) 4/4 (100.0%) ICT Blood Spain Molina et al. (2012)Iberian hare (Lepus granatensis) 32/76 (42.1%) PCR Spleen Spain Ruiz-Fons et al. (2013)European brown hare (Lepus europaeus) 9/16 (56.2%) PCR Spleen Spain Ruiz-Fons et al. (2013)Wild rabbits 1/162 (0.6%) PCR Spleen Spain Chitimia et al. (2011)
Pilosa/Myrmecophagidae Anteater (Tamandua tetradactyla) 1/1 (100.0%) Culture/PCR Blood/BM Brazil Araújo et al. (2013)
Primates/Cebidae Black-fronted titi monkey (Callicebus nigrifrons) 7/9 (77.7%) PCR Blood/tissues Brazil Malta et al. (2010)1/1 (100.0%) IHC Several tissues
Black head owl monkey (Aotus nigriceps) 1/1 (100.0%) PCR Blood Brazil Malta et al. (2010)Emperor tamarins (Saguinus imperator) 3/3 (100.0%) PCR Blood Brazil Malta et al. (2010)Golden-bellied capuchins (Cebusxanthosternos)
3/5 (60.0%) PCR Blood Brazil Malta et al. (2010)
Golden head lion tamarins (Leontopithecuscrysomelas)
1/5 (20.0%) PCR Blood Brazil Malta et al. (2010)
Howler monkeys (Alouatta guariba) 1/8 (12.5%) PCR Blood Brazil Malta et al. (2010)Rio Tapajo’ sakis (Pithecia irrorata) 2/4 (50.0%) PCR Blood Brazil Malta et al. (2010)
T.D. Souza et al. / Veterinary Parasit
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VL has been also diagnosed in wildlife in South Amer-ica, particularly in Brazil, where VL is an important publichealth issue, as it is an emerging disease in some regions,whereas it is endemic in others. Wild animals kept in zooslocated at endemic regions have been shown to harborthe parasite, and in some cases they can even progressto fatal VL (Luppi et al., 2008; Malta et al., 2010; Souzaet al., 2010; Jusi et al., 2011). Therefore, Leishmania sp.should be screened for before any susceptible animal entera zoo collection (Figueiredo et al., 2008). Reports fromBrazil involve bush dogs (S. venaticus), crab-eating foxes(C. thous), hoary zorros (Lycalopex vetulus), and manedwolves (Chrysocyon brachyurus) (Courtenay et al., 2002;Curi et al., 2006; Luppi et al., 2008; Figueiredo et al., 2008;Lima et al., 2009; Souza et al., 2010; Jusi et al., 2011; Curiet al., 2012). In a well documented case, a captive adultfemale bush dog (S. venaticus) developed emaciation, vom-iting, diarrhea, anemia, azotemia, polyuria, polydipsia, anddied in spite of treatment. Gross and histopathologicalfindings were characteristic of VL and diagnosis was con-firmed by immunohistochemistry and PCR (Luppi et al.,2008).
In North America, foxes and coyotes trapped at dif-ferent areas in Southeastern United States were testedfor antibodies against Leishmania spp. Among 286 wildcanids sampled, all of them were negative for Leishmaniasp. Importantly, canine leishmaniasis has been well docu-mented in that country, although it is almost completelyrestricted to one hunting dog breed, the American Fox-hound. Indigenous sand flies may become adapted to L.infantum if the vector becomes continually exposed to theprotozoa (Duprey et al., 2006). Therefore, Foxhounds withleishmaniasis may represent a threat to local L. infantumnegative wild canids and therefore control of the diseasein this particular breed of dogs should be considered fromthe conservation and public health perspective (Petersen,2009).
Wild felids are occasionally diagnosed with VL. Twobarbary lions (Panthera leo leo) were diagnosed with L.infantum in a zoo in France. One was asymptomatic andthe other had colitis, epistaxis, and pad ulcers, success-fully treated with marbofloxacine and allopurinol (Libertet al., 2012). Felids were also reported positive from azoo in Brazil, where five pumas (Puma concolor) andone jaguar (Panthera onca) – out of 16 captive wildfelids – had positive blood samples by PCR-RFLP. Allthese infected felids were asymptomatic (Dahroug et al.,2010).
Clinical signs of VL in wild carnivores and other animalspecies are summarized in Table 2.
4. Visceral leishmaniasis in other wild mammalianspecies
In primates, a fatal natural case of VL have beendescribed in a captive black-fronted titi monkey (Callicebusnigrifrons) that was kept in captivity at a zoo in the State
of Minas Gerais (Brazil). This animal developed clinicalsigns and lesions that were typical of VL. Microscopically,amastigotes were not observed in the skin, but the presenceof Leishmania sp. was confirmed by immunohistochemistry
238 T.D. Souza et al. / Veterinary Parasitology 200 (2014) 233– 241
Fig. 1. (A) Liver; bush dog (Speothos venaticus). Multifocal hepatitis. Portal infiltration of lymphocytes, plasma cells, and macrophages containingintracytoplasmic amastigotes (arrows and inset). (B) Kidney; bush dog (Speothos venaticus). Membranoproliferative glomerulonephritis. Multifocal lym-
y mesan
phoplasmacytic infiltrate associated to glomerulopathy characterized baccumulation. Hematoxylin and eosin. 400×.and PCR in other tissue samples. All five black-fronted titisliving in the same premises were positive by PCR, althoughnone of them developed clinical signs of the disease(Malta et al., 2010). Frozen blood samples from 36 other
non-human primates from the same zoo were tested foramplification of Leishmania kDNA by PCR and 12 turned outpositive, including one howler monkey (Alouatta guariba),three golden bellied capuchins (Cebus xanthosternos),gial cell proliferation, thickening of the basal membrane, and protein
one golden-headed lion tamarin (Leontopithecus crysome-las), one black-headed owl monkey (Aotus nigriceps),two Rio Tapajo’ sakis (Pithecia irrorata), three emperortamarins (Saguinus imperator), and one black-fronted
titi (C. nigrifrons). This later was a free-ranging animal(Malta et al., 2010).Experimental infection of marmosets (Callithrix jac-chus jacchus) by intraperitoneal injection of L. infantum
T.D. Souza et al. / Veterinary Parasitology 200 (2014) 233– 241 239
Table 2Clinical manifestation of Leishmania infantum infection in wild and zoo animals.
Species Clinical signs Diagnostic method Reference
Bush dog (Speothos venaticus) Anemia, vomiting, diarrhea, renalfailure, hemorrhage
IHC and PCR Luppi et al. (2008)
Bush dog (Speothos venaticus) Dermatitis, alopecia, renal failure,cachexia, onychogryphosis
ELISA and PCR Lima et al. (2009)
Bush dog (Speothos venaticus) Death with typical signs IFA and ELISA Jusi et al. (2011)Crab-eating fox (Cerdocyon thous) Death with typical signs IFA and ELISA Jusi et al. (2011)Crab-eating fox (Cerdocyon thous) Cutaneous and ocular lesions PCR-RFLP Souza et al. (2010)Gray wolf (Canis lupus) Typical, mainly cutaneous Several, including HE and PCR Beck et al. (2008)Hoary zorros (Lycalopex vetulus) Cutaneous lesions IFA, ELISA and PCR Luppi et al. (2008)Maned wolf (Chrysocyon brachyurus) Typical, including onychogryphosis IFA and ELISA Jusi et al. (2011)Maned wolf (Chrysocyon brachyurus) Cutaneous lesions IFA, ELISA and PCR Luppi et al. (2008)Barbary lion (Panthera leo leo) Colitis, epistaxis and pad ulcers PCR/IFA Libert et al. (2012)
omegalrrhages
aiw1
iwshwcsr(pLqh(2
(L(Mhae
TrpS
dtpc
lsdi(
Black-fronted titi monkey (Callicebusnigrifrons)
Emaciation, hepatosplenlymphadenopathy, hemo
mastigotes resulted in mild clinical signs at 120 days afternoculation, whereas marked spleen and liver enlargement
ere observed at 601 days post infection (Marsden et al.,981).
Wild rabbits were investigated for the presence of L.nfantum in Spain (Chitimia et al., 2011), but the prevalence
as very low (Table 1). Importantly, hares (Lepus granaten-is) captured from an area where there was an ongoinguman outbreak of VL in Southwestern Madrid (Spain)ere submitted to xenodiagnosis, and four hares were
apable of infecting 4.7% (0–10.6%) Phlebotomus perniciosaand flies. These results suggest that this species may rep-esent a reservoir in the sylvatic cycle of VL in that regionMolina et al., 2012). A retrospective survey analyzed sam-les from three different hare species (Lepus granatensis,. europaeus, L. castroviejoi) from Spain with a high fre-uency of positive samples (Ruiz-Fons et al., 2013). Thereas been also a report of a Leishmania-infected hedgehogErinaceus europaeus) from Spain (Munoz-Madrid et al.,013).
Rodents are considered reservoirs for L. infantumPapadogiannakis et al., 2010). Variable frequencies ofeishmania-positive Rattus norvegicus have been reportedPapadogiannakis et al., 2010; Helhazar et al., 2013;
unoz-Madrid et al., 2013). In Brazil, Leishmania infectionas been reported in Thrichomys apereoides, Rattus rattus,nd Rhipidomys mastacalis (Oliveira et al., 2005; Quaresmat al., 2011).
Marsupials are also susceptible to L. infantum infection.he opossum (Didelphis sp.) was considered a potentialeservoir host, since serological survey is resulted in a sero-revalence between 9% and 25% (Santiago et al., 2007;challig et al., 2007).
An interesting report from the Brazilian Amazon regionescribed a case of an asymptomatic anteater (Tamanduaetradactyla) concomitantly positive for L. infantum, Try-anosoma cruzi, and Trypanossoma rangeli, identified byulture, PCR and sequencing (Araújo et al., 2013).
In Venezuela, L. infantum was identified in a bat (Carol-ia perspicillata) (Lima et al., 2008). In Brazil, a survey that
ampled spleen and liver from 659 bats, belonging to 28ifferent species, resulted in only one Glossophaga soric-na and two Molossus molossus Leishmania positive batsSavani et al., 2010).
y, IHC and PCR Malta et al. (2010)
5. Epidemio-ecological implications andconcluding remarks
Considering all reports of Leishmania infection inwildlife, the red fox (V. vulpes) apparently is the specieswith the highest frequency of reported cases, although,clinical disease has not been reported in this species(Criado-Fornelio et al., 2000; Dipineto et al., 2007). Bushdogs (S. venaticus) were the most frequently reported wildcanids with clinical signs of VL (Figueiredo et al., 2008;Luppi et al., 2008; Lima et al., 2009; Souza et al., 2010;Jusi et al., 2011). This species is considered by The Ministryof the Environment in Brazil as “threatened of extinction”(Ministério do Meio Ambiente, 2003) and by The Interna-tional Union for Conservation of Nature (IUCN, 2012) as“near threatened”, with an estimated decline in the popu-lation of 20–25% in the last 12 years. The main reasons forthis threat include habitat loss and fragmentation, reduc-tion in pray availability, predation by domestic dogs, anddiseases (IUCN, 2012).
Although VL is an important emerging zoonosis, con-trolling this disease in Latin America is still extremelychallenging (Romero and Boelaert, 2010). Asymptomaticinfected individuals kept in zoos may represent a risk forother susceptible wild and synanthropic animals in theenvironment, as well as for the zookeepers and visitors.Therefore, control measures are extremely important inthese institutions (Jusi et al., 2011).
Many studies have demonstrated the presence of L.infantum in wild and synanthropic animals, but the impor-tance of these species as effective reservoirs for themaintenance of VL remains to be determined. A studybased on xenodiagnosis conducted with C. thous demon-strated that the transmission of L. infantum to Lutzomialongipalpis did not occur over a 15-month period of obser-vation under experimental conditions (Courtenay et al.,2002). In addition, in some cases of VL reported in wild ani-mals, Leishmania sp. was not present in skin samples fromprimates (Marsden et al., 1981; Malta et al., 2010). Thesestudies support the notion that wild canids and primates
very likely do not play a major role as reservoirs in endemicareas.The use of insecticide collars on infected canids has beenimplemented in some zoos to prevent contact with the
y Parasit
240 T.D. Souza et al. / Veterinarvector, and consequent transmission of the parasite. Peri-odic spray of insecticides on the environment has beensuggested in areas where the vector exists (Luppi et al.,2008). Diagnosis and treatment of infected animals, withcontrol of parasitemia (Libert et al., 2012) may also pre-vent L. infantum transmission. Positive wild animals maybe part of endangered species lists, and therefore elimina-tion of these animals may not be considered an effectiveapproach due to ethical and conservational implications(Curi et al., 2006; Figueiredo et al., 2008; Luppi et al., 2008;Sastre et al., 2008; Malta et al., 2010; Souza et al., 2010; Jusiet al., 2011; Libert et al., 2012).
Acknowledgements
Work in RLS lab is supported by CNPq (ConselhoNacional de Desenvolvimento Científico e Tecnológico,Brazil) and FAPEMIG (Fundac ão de Amparo a Pesquisa doEstado de Minas Gerais, Brazil).
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