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01-09-2019 | Flea | Original Contribution

Zoonotic Trypanosomes in Rats and Fleas of Venezuelan Slums

Authors: Herakles A. Garcia, Carlos J. Rangel, Paola A. Ortíz, Carlos O. Calzadilla, Raul A. Coronado, Arturo J. Silva, Arlett M. Pérez, Jesmil C. Lecuna, Maria E. García, Aixa M. Aguirre, Marta M. G. Teixeira

Published in: EcoHealth | Issue 3/2019

Abstract

Rattus spp. are reservoirs of many human zoonoses, but their role in domestic transmission cycles of human trypanosomiasis is underestimated. In this study, we report trypanosome-infected Rattus norvegicus and Rattus rattus in human dwellings in slums neighboring Maracay, a large city near Caracas, the capital of Venezuela. Blood samples of R. norvegicus and R. rattus examined by PCR and FFLB (fluorescent fragment length barcoding) revealed a prevalence of 6.3% / 31.1% for Trypanosoma lewisi (agent of rat- and flea-borne human emergent zoonosis), and 10.5% / 24.6% for Trypanosoma cruzi (agent of Chagas disease). Detection in flea guts of T. lewisi (76%) and, unexpectedly, T. cruzi (21.3%) highlighted the role of fleas as carriers and vectors of these trypanosomes. A high prevalence of rats infected with T. lewisi and T. cruzi and respective flea and triatomine vectors poses a serious risk of human trypanosomiasis in Venezuelan slums. Anthropogenic activities responsible for growing rat and triatomine populations within human dwellings drastically increased human exposure to trypanosomes. This scenario has allowed for the reemergence of Chagas disease as an urban zoonosis in Venezuela and can propitiate the emergence of atypical T. lewisi infection in humans.

Añez N, Crisante G, Maia da Silva F, Rojas A, Carrasco H, Umezawa ES, Stolf AM, Ramírez JL, Teixeira MMG (2004) Predominance of lineage I among Trypanosoma cruzi isolates from Venezuelan patients with different clinical profiles of acute Chagas’ disease. Tropical Medicine & International Health 9:1319–1326CrossRef

Añez N, Martens ML, Romero M, Crisante G (2011) Trypanosoma cruzi primary infection prevents severe re-infection in mice. Boletín de Malariología y Salud Ambiental 51:177–185

Archer CE, Schoeman MC, Appleton CC, Mukaratirwa S, Hope KJ, Matthews GB (2018) Predictors of Trypanosoma lewisi in Rattus norvegicus from Durban, South Africa. Journal of Parasitology 104:187–195. https://doi.org/10.1645/17-92 CrossRefPubMed

Averis S, Thompson RC, Lymbery AJ, Wayne AF, Morris KD, Smith A (2009) The diversity, distribution and host-parasite associations of trypanosomes in Western Australian wildlife. Parasitology 136:1269–1279. https://doi.org/10.1017/s0031182009990801 CrossRefPubMed

Bharodiya D, Singhal T, Kasodariya GS, Banerjee PS, Garg R (2018) Trypanosomiasis in a young infant from rural Gujarat, India. Indian Pediatrics 55:69–70CrossRef

Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D (2010) Fleas and flea-borne diseases. International Journal of Infectious Diseases 14:e667–676. https://doi.org/10.1016/j.ijid.2009.11.011 CrossRefPubMed

Bonwitt J, Sáez AM, Lamin J, Ansumana R, Dawson M, Buanie J, Lamin J, Sondufu D, Borchert M, Sahr F, Fichet-Calvet E, Brown H (2017) At home with Mastomys and Rattus: Human-rodent interactions and potential for primary transmission of Lassa virus in domestic spaces. The American Journal of Tropical Medicine and Hygiene 96:935–943. https://doi.org/10.4269/ajtmh.16-0675 CrossRefPubMedPubMedCentral

Bordes F, Blasdell K, Morand S (2015) Transmission ecology of rodent-borne diseases: New frontiers. Integrative Zoology 10:424–435. https://doi.org/10.1111/1749-4877.12149 CrossRefPubMed

Brigada AM, Doña R, Caviedes-Vidal E, Moretti E, Basso B (2010) American tripanosomiasis: a study on the prevalence of Trypanosoma cruzi and Trypanosoma cruzi-like organisms in wild rodents in San Luis province, Argentina. Revista da Sociedade Brasileira de Medicina Tropical 43:249–253CrossRef

Carhuallanqui A, Chávez A, Pinedo R (2017) Trypanosoma spp. en ratas (Rattus rattus y Rattus norvegicus) de dos medioambientes: mercados de abasto y granjas porcinas. Revista de Investigaciones Veterinarias del Perú 28:958–968. https://doi.org/10.15381/rivep.v28i4.13880 CrossRef

Carrasco HJ, Segovia M, Llewellyn MS, Morocoima A, Urdaneta-Morales S, Martínez C, Martínez CE, Garcia C, Rodríguez M, Espinosa R, de Noya BA, Díaz-Bello Z, Herrera L, Fitzpatrick S, Yeo M, Miles MA, Feliciangeli MD (2012) Geographical distribution of Trypanosoma cruzi genotypes in Venezuela. PLOS Neglected Tropical Diseases 6:1707. https://doi.org/10.1371/journal.pntd.0001707 CrossRef

Carrasco HJ, Segovia M, Londoño JC, Ortegoza J, Rodríguez M, Martínez CE (2014) Panstrongylus geniculatus and four other species of triatomine bug involved in the Trypanosoma cruzi enzootic cycle: high risk factors for Chagas’ disease transmission in the Metropolitan District of Caracas, Venezuela. Parasites & Vectors 7:602. https://doi.org/10.1186/s13071-014-0602-7 CrossRef

Carrasco HJ, Torrellas A, García C, Segovia M, Feliciangeli MD (2005) Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (Metropolitan District) and neighboring States, Venezuela. International Journal for Parasitology 35:1379–1384CrossRef

Cassan C, Diagne CA, Tatard C, Gauthier P, Dalecky A, Bâ K, Kane M, Niang Y, Diallo M, Sow A, Brouat C, Bañuls AL (2018) Leishmania major and Trypanosoma lewisi infection in invasive and native rodents in Senegal. PLOS Neglected Tropical Diseases 12:0006615. https://doi.org/10.1371/journal.pntd.0006615 CrossRef

D’Alessandro PA, Behr MA (1991) Trypanosoma lewisi and its relatives. In: Parasitic Protozoa, Kreier J, Baker JR (editors), New York, NY: Academic Press, pp 225–263

Dahesh SM, Mikhail MW (2016) Surveillance of Trypanosoma spp. of rodents and studies in their transmission probability by fleas in some rural Egyptian areas. Journal of the Egyptian Society of Parasitology 46:157–166CrossRef

de Lima H, Carrero J, Rodríguez A, de Guglielmo Z, Rodríguez N (2006) Trypanosomatidae of public health importance occurring in wild and synanthropic animals of rural Venezuela. Biomedica 26:42–50CrossRef

de Lima H, Rodriguez N, Borges R, Convit J (2003) Trypanosoma (Herpetosoma) lewisi in Rattus spp. from La Matica, Lara State, Venezuela and the possible relationship with zoonotic diseases. Boletín de malariología y salud ambiental 43:37–43

de Noya BA, González ON (2015) An ecological overview on the factors that drives to Trypanosoma cruzi oral transmission. Acta Tropica 151:94–102. https://doi.org/10.1016/j.actatropica.2015.06.004 CrossRefPubMed

Desquesnes M, Holzmuller P, Lai DH, Dargantes A, Lun ZR, Jittaplapong S (2013) Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects. BioMed Research International 194176. https://doi.org/10.1155/2013/194176 CrossRefPubMedPubMedCentral

Desquesnes M, Kamyingkird K, Yangtara S, Milocco C, Ravel S, Wang MH, Lun ZR, Morand S, Jittapalapong S (2011) Specific primers for PCR amplification of the ITS1 (ribosomal DNA) of Trypanosoma lewisi. Infection, Genetics and Evolution 11:1361–1367. https://doi.org/10.1016/j.meegid.2011.04.030 CrossRefPubMed

Díaz-Bello Z, Thomas MC, López MC, Zavala-Jaspe R, Noya O, de Noya BA, Abate T (2014) Trypanosoma cruzi genotyping supports a common source of infection in a school-related oral outbreak of acute Chagas disease in Venezuela. Epidemiology & Infection 142:156–162. https://doi.org/10.1017/s0950268813000757 CrossRef

Dobigny G, Poirier P, Hima K, Cabaret O, Gauthier P, Tatard C, Costa JM, Bretagne S (2011) Molecular survey of rodent-borne Trypanosoma in Niger with special emphasis on T. lewisi imported by invasive black rats. Acta Tropica 117:183–188. https://doi.org/10.1016/j.actatropica.2010.11.004 CrossRefPubMed

Feliciangeli MD, Campbell-Lendrum D, Martinez C, Gonzalez D, Coleman P, Davies C (2003) Chagas disease control in Venezuela: lessons for the Andean region and beyond. Trends in Parasitology 19:44–49CrossRef

Franjola R, Soto G, Montefusco A (1995) Prevalencia de infección por protozoos en roedores sinantrópicos de la ciudad de Valdivia, Chile. Boletín chileno de parasitología 50:66–72PubMed

Garcia HA, Rodrigues CMF, Rodrigues AC, Pereira DL, Pereira CL, Camargo EP, Hamilton PB, Teixeira MMG (2018) Remarkable richness of trypanosomes in tsetse flies (Glossina morsitans morsitans and Glossina pallidipes) from the Gorongosa National Park and Niassa National Reserve of Mozambique revealed by fluorescent fragment length barcoding (FFLB). Infection, Genetics and Evolution 63:370–379. https://doi.org/10.1016/j.meegid.2017.07.005 CrossRefPubMed

Hamilton PB, Adams ER, Malele II, Gibson WC (2008) A novel, high-throughput technique for species identification reveals a new species of tsetse-transmitted trypanosome related to the Trypanosoma brucei subgenus Trypanozoon. Infection, Genetics and Evolution 8:26–33CrossRef

Hamilton PB, Lewis MD, Cruickshank C, Gaunt MW, Yeo M, Llewellyn MS, Valente SA, Maia da Silva F, Stevens JR, Miles MA, Teixeira MMG (2011) Identification and lineage genotyping of South American trypanosomes using fluorescent fragment length barcoding. Infection, Genetics and Evolution 11:44–51. https://doi.org/10.1016/j.meegid.2010.10.012 CrossRefPubMed

Herrera L, Urdaneta-Morales S (1997) Synanthropic rodent reservoirs of Trypanosoma (Schizotrypanum) cruzi in the valley of Caracas, Venezuela. Revista do Instituto de Medicina Tropical de São Paulo 39:279–282. https://doi.org/10.1590/s0036-4665199700050000637 CrossRefPubMed

Himsworth CG, Parsons KL, Jardine C, Patrick DM (2013) Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector-Borne and Zoonotic Diseases 13:349–359. https://doi.org/10.1089/vbz.2012.1195 CrossRefPubMed

Hoare CA (1972) The Trypanosomes of Mammals: A Zoological Monograph. Blackwell Scientific Publications, Oxford

Hong XK, Zhang X, Fusco OA, Lan YG, Lun ZR, Lai DH (2017) PCR-based identification of Trypanosoma lewisi and Trypanosoma musculi using maxicircle kinetoplast DNA. Acta Tropica 171:207–212. https://doi.org/10.1016/j.actatropica.2017.04.007 CrossRefPubMed

Jittapalapong S, Inpankaew T, Sarataphan N, Herbreteau V, Hugot JP, Morand S, Stich RW (2008) Molecular detection of divergent trypanosomes among rodents of Thailand. Infection, Genetics and Evolution 8:445–449CrossRef

Kosoy M, Khlyap L, Cosson JF, Morand S (2015) Aboriginal and invasive rats of genus Rattus as hosts of infectious agents. Vector-Borne and Zoonotic Diseases 15:3–12. https://doi.org/10.1089/vbz.2014.1629 CrossRefPubMed

Lima L, Ortiz PA, Maia da Silva F, Alves JM, Serrano MG, Cortez AP, Alfieri SC, Buck GA, Teixeira MMG (2012) Repertoire, genealogy and genomic organization of cruzipain and homologous genes in Trypanosoma cruzi, T. cruzi-like and other trypanosome species. PLoS One 7:e38385. https://doi.org/10.1371/journal.pone.0038385 CrossRefPubMedPubMedCentral

Linardi PM, Botelho JR (2002) Prevalence of Trypanosoma lewisi in Rattus norvegicus from Belo Horizonte, State of Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 97:411–414CrossRef

Lizundia R, Newman C, Buesching CD, Ngugi D, Blake D, Sin YW, Macdonald DW, Wilson A, McKeever D (2011) Evidence for a role of the host-specific flea (Paraceras melis) in the transmission of Trypanosoma (Megatrypanum) pestanai to the European badger. PLoS One 6:e16977. https://doi.org/10.1371/journal.pone.0016977 CrossRefPubMedPubMedCentral

Lun ZR, Wen YZ, Uzureau P, Lecordier L, Lai DH, Lan YG, Desquesnes M, Geng GQ, Yang TB, Zhou WL, Jannin JG, Simarro PP, Truc P, Vincendeau P, Pays E (2015) Resistance to normal human serum reveals Trypanosoma lewisi as an underestimated human pathogen. Molecular and Biochemical Parasitology 199:58–61. https://doi.org/10.1016/j.molbiopara.2015.03.007 CrossRefPubMed

Maia da Silva F, Marcili A, Ortiz PA, Epiphanio S, Campaner M, Catão-Dias JL, Shaw JJ, Camargo EP, Teixeira MMG (2010) Phylogenetic, morphological and behavioural analyses support host switching of Trypanosoma (Herpetosoma) lewisi from domestic rats to primates. Infection, Genetics and Evolution 10:522–529. https://doi.org/10.1016/j.meegid.2010.02.005 CrossRefPubMed

Milocco C, Kamyingkird K, Desquesnes M, Jittapalapong S, Herbreteau V, Chaval Y, Douangboupha B, Morand S (2013) Molecular demonstration of Trypanosoma evansi and Trypanosoma lewisi DNA in wild rodents from Cambodia, Lao PDR and Thailand. Transboundary and Emerging Diseases 60:17–26. https://doi.org/10.1111/j.1865-1682.2012.01314.x CrossRefPubMed

Morand S, Bordes F, Chen HW, Claude J, Cosson JF, Galan M, Czirják GÁ, Greenwood AD, Latinne A, Michaux J, Ribas A (2015) Global parasite and Rattus rodent invasions: The consequences for rodent-borne diseases. Integrative Zoology 10:409–423. https://doi.org/10.1111/1749-4877.12143 CrossRefPubMed

Ortiz PA, Garcia HA, Lima L, Maia da Silva F, Campaner M, Pereira CL, Jittapalapong S, Neves L, Desquesnes M, Camargo EP, Teixeira MMG (2017) Diagnosis and genetic analysis of the worldwide distributed Rattus-borne Trypanosoma (Herpetosoma) lewisi and its allied species in blood and fleas of rodents. Infection, Genetics and Evolution 63:380–390. https://doi.org/10.1016/j.meegid.2017.09.001 CrossRefPubMed

Ortiz PA, Maia da Silva F, Cortez AP, Lima L, Campaner M, Pral EM, Alfieri SC, Teixeira MMG (2009) Genes of cathepsin L-like proteases in Trypanosoma rangeli isolates: markers for diagnosis, genotyping and phylogenetic relationships. Acta Tropica 112:249–259. https://doi.org/10.1016/j.actatropica.2009.07.036 CrossRefPubMed

Panti-May JA, De Andrade RRC, Gurubel-González Y, Palomo-Arjona E, Sodá-Tamayo L, Meza-Sulú J, Ramírez-Sierra M, Dumonteil E, Vidal-Martínez VM, Machaín-Williams C, De Oliveira D, Reis MG, Torres-Castro MA, Robles MR, Hernández-Betancourt SF, Costa F (2017) A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico. Epidemiology & Infection 145:2287–2295. https://doi.org/10.1017/s0950268817001352 CrossRef

Pinto CM, Ocaña-Mayorga S, Lascano MS, Grijalva MJ (2006) Infection by trypanosomes in marsupials and rodents associated with human dwellings in Ecuador. Journal of Parasitology 92:1251–1255CrossRef

Pumhom P, Morand S, Tran A, Jittapalapong S, Desquesnes M (2015) Trypanosoma from rodents as potential source of infection in human-shaped landscapes of South-East Asia. Veterinary Parasitology 208:174–180. https://doi.org/10.1016/j.vetpar.2014.12.027 CrossRefPubMed

Pumhom P, Pognon D, Yangtara S, Thaprathorn N, Milocco C, Douangboupha B, Herder S, Chaval Y, Morand S, Jittapalapong S, Desquesnes M (2014) Molecular prevalence of Trypanosoma spp. in wild rodents of Southeast Asia: influence of human settlement habitat. Epidemiology & Infection 142:1221–1230. https://doi.org/10.1017/s0950268813002161 CrossRef

Roque AL, Jansen AM (2014) Wild and synanthropic reservoirs of Leishmania species in the Americas. International Journal for Parasitology: Parasites and Wildlife 3:251–262. https://doi.org/10.1016/j.ijppaw.2014.08.004 CrossRefPubMed

Rosal GG, Nogueda-Torres B, Villagrán ME, de Diego-Cabrera JA, Montañez-Valdez OD, Martínez-Ibarra JA (2018) Chagas disease: Importance of rats as reservoir hosts of Trypanosoma cruzi (Chagas, 1909) in western Mexico. Journal of Infection and Public Health 11:230–233. https://doi.org/10.1016/j.jiph.2017.07.017 CrossRefPubMed

Rossi JP, Kadaouré I, Godefroid M, Dobigny G (2017) Landscape epidemiology in urban environments: The example of rodent-borne Trypanosoma in Niamey, Niger. Infection, Genetics and Evolution 63:307–315. https://doi.org/10.1016/j.meegid.2017.10.006 CrossRefPubMed

Salzer JS, Pinto CM, Grippi DC, Williams-Newkirk AJ, Peterhans JK, Rwego IB, Carroll DS, Gillespie TR (2016) Impact of anthropogenic disturbance on native and invasive trypanosomes of rodents in forested Uganda. EcoHealth 13:698–707. https://doi.org/10.1007/s10393-016-1160-6 CrossRefPubMed

Schwan TG, Lopez JE, Safronetz D, Anderson JM, Fischer RJ, Maïga O, Sogoba N (2016) Fleas and trypanosomes of peridomestic small mammals in sub-Saharan Mali. Parasites & Vectors 9:541CrossRef

Tang HJ, Lan YG, Wen YZ, Zhang XC, Desquesnes M, Yang TB, Hide G, Lun ZR (2012) Detection of Trypanosoma lewisi from wild rats in Southern China and its genetic diversity based on the ITS1 and ITS2 sequences. Infection, Genetics and Evolution 12:1046–1051. https://doi.org/10.1016/j.meegid.2012.02.018 CrossRefPubMed

Tatard C, Garba M, Gauthier P, Hima K, Artige E, Dossou DKHJ., Gagaré S, Genson G, Truc P, Dobigny G (2017) Rodent-borne Trypanosoma from cities and villages of Niger and Nigeria: A special role for the invasive genus Rattus? Acta Tropica 171:151–158. https://doi.org/10.1016/j.actatropica.2017.03.027 CrossRefPubMed

Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, Juyal P, Lun ZR, Mattioli R, Pays E, Simarro PP, Teixeira MMG, Touratier L, Vincendeau P, Desquesnes M (2013) Atypical human infections by animal trypanosomes. PLOS Neglected Tropical Diseases 7:e2256. https://doi.org/10.1371/journal.pntd.0002256 CrossRefPubMedPubMedCentral

Urdaneta-Morales S (2014) Chagas’ disease: an emergent urban zoonosis. The Caracas valley (Venezuela) as an epidemiological model. Frontiers in Public Health 2:265. https://doi.org/10.3389/fpubh.2014.00265

Votýpka J, Suková E, Kraeva N, Ishemgulova A, Duží I, Lukeš J, Yurchenko V (2013) Diversity of trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist 164:763–781. https://doi.org/10.1016/j.protis.2013.08.002 CrossRefPubMed

Woo PT (1970) The haematocrit centrifuge technique for the diagnosis of African trypanosomiasis. Acta Tropica 27:384–386.PubMed

Woods ME, Montenieri JA, Eisen RJ, Zeidner NS, Borchert JN, Laudisoit A, Babi N, Atiku LA, Enscore RE, Gage KL (2009) Identification of flea blood meals using multiplexed real-time polymerase chain reaction targeting mitochondrial gene fragments. The American Journal of Tropical Medicine and Hygiene 80:998–1003.CrossRef

Yefi-Quinteros E, Muñoz-San Martín C, Bacigalupo A, Correa JP, Cattan PE (2018) Trypanosoma cruzi load in synanthropic rodents from rural areas in Chile. Parasites & Vectors 11:171. https://doi.org/10.1186/s13071-018-2771-2 CrossRef

Title: Zoonotic Trypanosomes in Rats and Fleas of Venezuelan Slums
Authors: Herakles A. Garcia
Carlos J. Rangel
Paola A. Ortíz
Carlos O. Calzadilla
Raul A. Coronado
Arturo J. Silva
Arlett M. Pérez
Jesmil C. Lecuna
Maria E. García
Aixa M. Aguirre
Marta M. G. Teixeira
Publication date: 01-09-2019
Publisher: Springer US
Keywords: Flea
Flea
Published in: EcoHealth / Issue 3/2019
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI: https://doi.org/10.1007/s10393-019-01440-4

At a glance: The STEP trials

Springer Medicine

Zoonotic Trypanosomes in Rats and Fleas of Venezuelan Slums

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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