Abstract
For years, mammals of the order Pilosa have been considered Leishmania reservoirs. But while most studies have focused on sloth species, anteaters have been overlooked, and in many Leishmania endemic countries like Mexico, no studies have been carried out. The aims of this work were to identify the presence of Leishmania spp. in tissue samples from road-killed northern tamanduas (Tamandua mexicana), using PCR amplification and sequencing of ITS1 DNA, and to discuss the role of Pilosa mammals as reservoirs of Leishmania based on available scientific records. This is the first study that identifies Leishmania in T. mexicana, from 1 of 16 individuals analyzed, so the estimated prevalence (CI 95%) of infection was 6.3% (0.3–27.2). Amplified sequence exhibited a 98.9% (727/735) similarity with L. mexicana, and phylogenetic analysis grouped the species in the L. mexicana-amazonensis cluster. The literature review revealed 241 cases of Leishmania spp. infection among 1219 Pilosa mammals evaluated, with prevalence between studies ranging from 3.5% in the brown-throated three-toed sloth (Bradypus variegatus) to 78% in the Hoffman’s two-toed sloth (Choloepus hoffmanni). Current scientific information indicates that C. hoffmanni sloths are reservoirs of Leishmania, and further studies are needed in order to clarify if other Pilosa species play a role in Leishmania transmission.
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References
Ballados-González GG, Sánchez-Montes S, Romero-Salas D, Colunga-Salas P, Gutiérrez-Molina R, León-Paniagua L, Becker I, Méndez-Ojeda ML, Barrientos-Salcedo C, Serna-Lagunes R, Cruz-Romero A (2018) Detection of pathogenic Leptospira species associated with phyllostomid bats (Mammalia: Chiroptera) from Veracruz, Mexico. Transbound Emerg Dis 65:773–781. https://doi.org/10.1111/tbed.12802
Berzunza-Cruz M, Rodríguez-Moreno Á, Gutiérrez-Granados G, González-Salazar C, Stephens CR, Hidalgo-Mihart M, Marina CF, Rebollar-Téllez EA, Bailón-Martínez D, Domingo-Balcells C, Ibarra-Cerdeña CN, Sánchez-Cordero V (2015) Leishmania (L.) mexicana infected bats in Mexico: novel potential reservoirs. PLoS Negl Trop Dis 9:e0003438. https://doi.org/10.1371/journal.pntd.0003438
Christensen HA, Herrer A (1979) Susceptibility of sand flies (Diptera: Psychodidae) to Trypanosomatidae from two-toed sloths (Edentata: Bradypodidae). J Med Entomol 16:424–427. https://doi.org/10.1093/jmedent/16.5.424
Cupolillo E, Grimaldi JG, Momen H, Beverley SM (1995) Intergenic region typing (IRT): a rapid molecular approach to the characterization and evolution of Leishmania. Mol Biochem Parasitol 73:145–155. https://doi.org/10.1016/0166-6851(95)00108-D
De Aráujo VAL, Boité MC, Cupolillo E, Jansen AM, Roque ALR (2013) Mixed infection in the anteater Tamandua tetradactyla (Mammalia: Pilosa) from Pará State, Brazil: Trypanosoma cruzi, T. rangeli and Leishmania infantum. Parasitology 140:455–460. https://doi.org/10.1017/S0031182012001886
Dedet JP, Gay F, Chatenay G (1989) Isolation of Leishmania species from wild mammals in French Guiana. Trans R Soc Trop Med Hyg 83:613–615. https://doi.org/10.1016/0035-9203(89)90374-X
Espinosa-Martínez DV, Sánchez-Montes DS, León-Paniagua L, Ríos-Muñoz CA, Berzunza-Cruz M, Becker I (2015) New wildlife hosts of Leptospira interrogans in Campeche, Mexico. Rev Inst Med Trop São Paulo 57:181–183. https://doi.org/10.1590/S0036-46652015000200015
Gentile B, Le Pont F, Pajot FX, Besnard R (1981) Dermal leishmaniasis in French Guiana: the sloth (Choloepus didactylus) as a reservoir host. Trans R Soc Trop Med Hyg 75:612–613
Gradoni LA (2018) Brief introduction to leishmaniasis epidemiology. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical diseases. Springer, Cham, pp 1–13. https://doi.org/10.1007/978-3-72386-0_1
Grimaldi Júnior G, Kreutzer RD, Hashiguchi Y, Gomez EA, Mimory T, Tesh RB (1992) Description of Leishmania equatorensis sp. n.(Kinetoplastida: Trypanosomatidae), a new parasite infecting arboreal mammals in Ecuador. Mem Inst Oswaldo Cruz 87:221–228. https://doi.org/10.1590/S0074-02761992000200009
Herrer A, Christensen HA (1980) Leishmania braziliensis in the Panamanian two-toed sloth, Choloepus hoffmanni. Am J Trop Med Hyg 29:1196–1200. https://doi.org/10.4269/ajtmh.1980.29.1196
Herrer A, Telford SR (1969) Leishmania braziliensis isolated from sloths in Panama. Science 164:1419–1420. https://doi.org/10.1126/science.164.3886.1419
Kreutzer RD, Corredor A, Grimaldi G Jr, Grogl M, Rowton ED, Young DG, Morales A, McMahon-Pratt D, Guzman H, Tesh RB (1991) Characterization of Leishmania colombiensis sp. n (Kinetoplastida: Trypanosomatidae), a new parasite infecting humans, animals, and phlebotomine sand flies in Colombia and Panama. Am J Trop Med Hyg 44:662–675. https://doi.org/10.4269/ajtmh.1991.44.662
Lainson R, Shaw JJ, Póvoa M (1981a) The importance of edentates (sloth and anteaters) as primary reservoirs of Leishmania braziliensis guyanensis, causative agent of “pian-bois” in north Brazil. Trans R Soc Trop Med Hyg 75:611–612
Lainson R, Shaw JJ, Ready PD, Miles MA, Póvoa M (1981b) Leishmaniasis in Brazil: XVI. Isolation and identification of, Leishmania species from sandflies, wild mammals and man in north Pará State, with particular reference to L. braziliensis guyanensis causative agent of “pian-bois”. Trans R Soc Trop Med Hyg 75:530–536. https://doi.org/10.1016/0035-9203(81)90192-9
Lainson R, Braga RR, De Souza AAA, Povoa MM, Ishikawa EAY, Silveira FT (1989) Leishmania (Viannia) shawi sp. n., a parasite of monkeys, sloths and procyonids in Amazonian Brazil. Ann Parasitol Hum Comp 64:200–207. https://doi.org/10.1051/parasite/1989643200
Loyola EG, Alzate A, Sánchez A, González A (1988) Epidemiology of a natural focus of Leishmania braziliensis in the Pacific lowlands of Colombia. III. Natural infections in wild mammals. Trans R Soc Trop Med Hyg 82:406–407. https://doi.org/10.1016/0035-9203(88)90136-8
Maia C, Dantas-Torres F, Campino L (2018) Parasite biology: the reservoir hosts. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical diseases. Springer, Cham, pp 79–106. https://doi.org/10.1007/978-3-319-72386-0_4
Marco JD, Barroso PA, Locatelli FM, Cajal SP, Hoyos CL, Nevot MC, Lauthier JJ, Tomasini N, Juarez M, Estévez JO, Korenaga M, Nasser JR, Hashiguchi Y, Ruybal P (2015) Multilocus sequence typing approach for a broader range of species of Leishmania genus: describing parasite diversity in Argentina. Infect Genet Evol 30:308–317. https://doi.org/10.1016/j.meegid.2014.12.031
Mimori T, Grimaldi G Jr, Kreutzer RD, Gomez EA, McMahon-Pratt D, Tesh RB, Hashiguchi Y (1989) Identification, using isoenzyme electrophoresis and monoclonal antibodies, of Leishmania isolated from humans and wild animals of Ecuador. Am J Trop Med Hyg 40:154–158. https://doi.org/10.4269/ajtmh.1989.40.154
Moraes-Barros N, Arteaga MC (2015) Genetic diversity in Xenarthra and its relevance to patterns of neotropical biodiversity. J Mammal 96:690–702. https://doi.org/10.1093/jmammal/gyv077
Muñoz-García CI, Berriatua E, Martínez-Carrasco C (2018) What do we known about parasites of wildlife in high biodiversity areas with anthropogenic disturbance? The special case of Mexico. Anim Health Res Rev 19:155–161. https://doi.org/10.1017/S1466252318000087
Navarrete D, Ortega J (2011) Tamandua mexicana (Pilosa: Myrmecophagidae). Mamm Species 43:56–63. https://doi.org/10.1644/874.1
Nuñez-Perez R, Corona-Corona E, Torres-Villanueva J, Anguiano-Méndez C, Tornez M, Solorio I, Torres A (2011) Nuevos registros del oso hormiguero, Tamandua mexicana, en el occidente de México. Edentata 12:58–62. https://doi.org/10.5537/020.012.0109
Paternina LE, Verbel-Vergara D, Romero-Ricardo L, Pérez-Doria A, Paternina-Gómez M, Martínez L, Bejarano EE (2016) Evidence for anthropophily in five species of phlebotomine sand flies (Diptera: Psychodidae) from northern Colombia, revealed by molecular identification of bloodmeals. Acta Trop 153:86–92. https://doi.org/10.1016/j.actatropica.2015.10.005
Quinnell RJ, Courtenay O (2009) Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology 136:1915–1193. https://doi.org/10.1017/S0031182009991156
Reibe S, Madea B (2010) How promptly do blowflies colonise fresh carcasses? A study comparing indoor with outdoor locations. Forensic Sci Int 195:52–57. https://doi.org/10.1016/j.forsciint.2009.11.009
Richini-Pereira VB, Marson PM, Hayasaka EY, Victoria C, da Silva RC, Langoni H (2014) Molecular detection of Leishmania spp. in road-killed wild mammals in the Central Western area of the State of São Paulo, Brazil. J Venom Anim Toxins Incl Trop Dis 20:27. https://doi.org/10.1186/1678-9199-20-27
Roque ALR, Jansen AM (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. Int J Parasitol Parasites Wildl 3:251–262. https://doi.org/10.1016/j.ijppaw.2014.08.004
Semarnat (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010: Protección ambiental-especies nativas de México de flora y fauna silvestres-categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-lista de especies en riesgo. URL: http://dof.gob.mx/nota_detalle_popup.php?codigo=5173091. Accessed 1 Nov 2018
Stephens CR, Heau JG, González C, Ibarra-Cerdeña CN, Sánchez-Cordero V, González-Salazar C (2009) Using biotic interaction networks for prediction in biodiversity and emerging diseases. PLoS One 4:e5725. https://doi.org/10.1371/journal.pone.0005725
Superina M, Loughry WJ (2015) Why do Xenarthrans matter? J Mammal 96:617–621. https://doi.org/10.1093/jmammal/gyv099
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Van Wynsberghe NR, Canto-Lara SB, Sosa-Bibiano EI, Rivero-Cárdenas NA, Andrade-Narváez FJ (2009) Comparison of small mammal prevalence of Leishmania (Leishmania) mexicana in five foci of cutaneous leishmaniasis in the state of Campeche, Mexico. Rev Inst Med Trop São Paulo 51:87–94. https://doi.org/10.1590/S0036-46652009000200006
Woodburne MO (2010) The Great American Biotic Interchange: dispersals, tectonics, climate, sea level and holding pens. J Mamm Evol 17:245–264. https://doi.org/10.1007/s10914-010-9144-8
Zeledón R, Ponce C, De Ponce E (1975) The isolation of Leishmania braziliensis from sloths in Costa Rica. Am J Trop Med Hyg 24:706–707. https://doi.org/10.4269/ajtmh.1975.24.706
Zeledón R, Ponce C, Murillo J (1979) Leishmania herreri sp. n from sloths and sandflies of Costa Rica. J Parasitol 65:275–279. https://doi.org/10.2307/3280164
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Muñoz-García, C.I., Sánchez-Montes, S., Villanueva-García, C. et al. The role of sloths and anteaters as Leishmania spp. reservoirs: a review and a newly described natural infection of Leishmania mexicana in the northern anteater. Parasitol Res 118, 1095–1101 (2019). https://doi.org/10.1007/s00436-019-06253-6
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DOI: https://doi.org/10.1007/s00436-019-06253-6