Factors associated with endoparasites and ectoparasites in domiciled dogs in the metropolitan area of Toluca, México
Abstract
Introduction: Endoparasites and ectoparasites in dogs are of global distribution. The close relationship between dogs and man implies a risk for the transmission of zoonotic parasites. Therefore, it is necessary to determine the parasites hosted by dogs in specific areas and the factors associated with their presence.
Objectives: To identify and to estimate the prevalence of endoparasites and ectoparasites in domiciled dogs in the Metropolitan area of Toluca, México, and the prevalence of D. caninum in fleas of the genus Ctenocephalides spp.
Materials and methods: We collected samples from 402 domiciled dogs in four reference hospitals in the area in Toluca. We diagnosed endoparasites using direct smear, flotation, and sedimentation techniques and we performed the taxonomic identification of ectoparasites. Finally, the molecular diagnosis of D. caninum in fleas was made using the polymerase chain reaction technique (PCR).
Results: A total of 37.2% of dogs were positive for endoparasites; the genera or species identified were Toxocara spp., Giardia spp., Ancylostoma spp., Cystoisospora spp., D. caninum, Taenia spp., and Trichuris vulpis; the prevalence of ectoparasites was 13.13%. We identified fleas of the species Ctenocephalides felis, Ctenocephalides canis; only one animal was parasitized with Rhipicephalus sanguineus and another one with Trichodectes canis; the prevalence of D. caninum in fleas was 9.5%.
Conclusion: The prevalence of endoparasites was 37.2% while that of ectoparasites was 13.1%; this is the first analysis of endoparasites and ectoparasites conducted in the same population of dogs in México together with the molecular diagnosis of D. caninum in fleas.
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Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors. 2014;7:22. https://doi.org/10.1186/1756-3305-7-22
Rodríguez-Vivas RI, Gutiérrez-Ruiz E, Bolio-González ME, Ruiz-Piña H, Ortega-Pacheco A, Reyes-Novelo E, et al. An epidemiological study of intestinal parasites of dogs from Yucatán, México, and their risk to public health. Vector Borne Zoonotic Dis. 2011;11:1141-4. https://doi.org/10.1089/vbz.2010.0232
Baneth G, Thamsborg SM, Otranto D, Guillot J, Blaga R, Deplazes P, et al. Major parasitic zoonoses associated with dogs and cats in Europe. J Comp Pathol. 2016;155(Suppl.1):S54-74. https://doi.org/10.1016/j.jcpa.2015.10.179
Linardi PM, Santos JLC. Ctenocephalides felis felis vs. Ctenocephalides canis (Siphonaptera: Pulicidae): Some issues in correctly identify these species. Rev Bras Parasitol Vet. 2012;21:345-54. https://doi.org/10.1590/S1984-29612012000400002
Little SE, Johnson EM, Lewis D, Jaklitsch RP, Payton ME, Blagburn BL, et al. Prevalence of intestinal parasites in pet dogs in the United States. Vet Parasitol. 2009;166:144-52. https://doi.org/10.1016/j.vetpar.2009.07.044
Hinney B, Gottwald M, Moser J, Reicher B, Schäfer BJ, Schaper R, et al. Examination of anonymous canine faecal samples provides data on endoparasite prevalence rates in dogs for comparative studies. Vet Parasitol. 2017;245:106-15. https://doi.org/10.1016/j.vetpar.2017.08.016
Katagiri S, Oliveira-Sequeira TCG. Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in São Paulo State, Brazil. Zoonoses Public Health. 2008;55:406-13. https://doi.org/10.1111/j.1863-2378.2008.01163.x
Torres-Chablé OM, García-Herrera RA, Hernández-Hernández M, Peralta-Torres JA, Ojeda-Robertos NF, Blitvich BJ, et al. Prevalence of gastrointestinal parasites in domestic dogs in Tabasco, southeastern México. Rev Bras Parasitol Vet. 2015;24:432-7. https://doi.org/10.1590/S1984-29612015077
Martínez-Barbabosa I, Gutiérrez M, Ruiz LA, Fernández AM, Gutiérrez EM, Aguilar JM, et al. Detección de Cryptosporidium spp. y otros parásitos zoonóticos entéricos en perros domiciliados de la Ciudad de México. Arch Med Vet. 2015;47:347-53. https://doi.org/10.4067/S0301-732X2015000300012
Ortega-Pacheco A, Torres-Acosta JFJ, Alzina-López A, Gutiérrez-Blanco E, Bolio-González ME, Aguilar-Caballero AJ, et al. Parasitic zoonoses in humans and their dogs from a rural community of tropical Mexico. J Trop Med. 2015;2015:481086. https://doi.org/10.1155/2015/481086
Otranto D, Dantas-Torres F, Mihalca AD, Traub RJ, Lappin M, Baneth G. Zoonotic parasites of sheltered and stray dogs in the era of the global economic and political crisis. Trends Parasitol. 2017;33:813-25. https://doi.org/10.1016/j.pt.2017.05.013
Rinaldi L, Spera G, Musella V, Carbone S, Veneziano V, Iori A, et al. A survey of fleas on dogs in southern Italy. Vet Parasitol. 2007;148:375-8. https://doi.org/10.1016/j.vetpar.2007.06.036
Gracia MJ, Calvete C, Estrada R, Castillo JA, Peribáñez MA, Lucientes J. Fleas parasitizing domestic dogs in Spain. Vet Parasitol. 2008;151:312-9. https://doi.org/10.1016/j.vetpar.2007.10.006
Costa-Junior LM, Rembeck K, Mendonça FL de M, Azevedo SC, Passos LMF, Ribeiro MFB. Occurrence of ectoparasites on dogs in rural regions of the state of Minas Gerais, Brazil. Rev Bras Parasitol Vet. 2012;21:237-42. https://doi.org/10.1590/S1984-29612012000300011
Bolio-González ME, Rodríguez-Vivas RI, Sauri-Arceo CH, Gutiérrez-Blanco E, Morales-Puerto F, Gutiérrez-Ruiz EJ, et al. Prevalencia de lesiones cutáneas de Ctenocephalides felis y Ctenocephalides canis en perros del estado de Yucatán, México. Bioagrociencias. 2012;5:15-9.
Cruz-Vázquez C, García-Vázquez Z, Morales-Soto M. Prevalence of Rhipicephalus sanguineus infestation in dogs in Cuernavaca, Morelos, México. Parasitol Día. 1998;22:29-32. https://doi.org/10.4067/S0716-07201998000100005
Tinoco-Gracia L, Quiroz-Romero H, Quintero-Martínez MT, Rentería-Evangelista TB, González-Medina Y, Barreras-Serrano A, et al. Prevalence of Rhipicephalus sanguineus ticks on dogs in a region on the Mexico-USA border. Vet Rec. 2009;164:59-61. https://doi.org/10.1136/vr.164.2.59
Rodríguez-Vivas RI, Apanaskevich DA, Ojeda-Chi MM, Trinidad-Martínez I, Reyes-Novelo E, Esteve-Gassent MD, et al. Ticks collected from humans, domestic animals, and wildlife in Yucatán, México. Vet Parasitol. 2016;215:106-13. https://doi.org/10.1016/j.vetpar.2015.11.010
INEGI, CONAPO. Delimitación de las zonas metropolitanas de México. Fecha de consulta: 28 de noviembre de 2017. Disponible en: http://internet.contenidos.inegi.org.mx/contenidos/productos/prod_serv/contenidos/espanol/bvinegi/productos/historicos/1329/702825010048/702825010048_1.pdf
World Health Organization (WHO). Sample size determination in health studies: A practical manual. Genève: World Health Organization; 1991.
Bögel K, Frucht K, Drysdale G, Remfry J, World Health Organization, Veterinary Public Health Unit, et al. Guidelines for dog population management/preparation. Genève: World Health Organization; 1990. https://apps.who.int/iris/handle/10665/61417
Laflamme D. Development and validation of a body condition score system for dogs. Canine Practice. 1997;22:10-5.
Sirois M. Laboratory manual for laboratory procedures for veterinary technicians. 7th edition. San Luis: Mosby; 2019.
Rodríguez-Vivas RI, Cob-Galera LA. Técnicas diagnósticas de parasitología veterinaria, Mérida, México. Mérida: Universidad Autónoma de Yucatán; 2005.
De Oliveira PR, Bechara GH, Denardi SE, Saito KC, Nunes ET, Szabó MPJ, et al. Comparison of the external morphology of Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) ticks from Brazil and Argentina. Vet Parasitol. 2005;129:139-47. https://doi.org/10.1016/j.vetpar.2005.01.001
Beugnet F, Labuschagne M, Fourie J, Jacques G, Farkas R, Cozma V, et al. Occurrence of Dipylidium caninum in fleas from client-owned cats and dogs in Europe using a new PCR detection assay. Vet Parasitol. 2014;205:300-6. https://doi.org/10.1016/j.vetpar.2014.06.008
Boubaker G, Marinova I, Gori F, Hizem A, Müller N, Casulli A, et al. A dual PCR-based sequencing approach for the identification and discrimination of Echinococcus and Taenia taxa. Mol Cell Probes. 2016;30:211-7. https://doi.org/10.1016/j.mcp.2016.05.004
Fontanarrosa MF, Vezzani D, Basabe J, Eiras DF. An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Vet Parasitol. 2006;136:283-95. https://doi.org/10.1016/j.vetpar.2005.11.012
Martínez-Barbabosa I, Gutiérrez-Cárdenas EM, Aguilar-Venegas J, Pimienta-Lastra R de J, Shea M. Frecuencia de geohelmintos en canes domiciliados en siete delegaciones de la Ciudad de México. Vet Mex. 2011;42:83-91.
Estrada-Peña A, Roura X, Sainz A, Miró G, Solano-Gallego L. Species of ticks and carried pathogens in owned dogs in Spain: Results of a one-year national survey. Ticks Tick Borne Dis. 2017;8:443-52. https://doi.org/10.1016/j.ttbdis.2017.02.001
Coelho WMD, Gomes JF, Amarante AFT do, Bresciani KDS, Lumina G, Koshino-Shimizu S, et al. A new laboratorial method for the diagnosis of gastrointestinal parasites in dogs. Rev Bras Parasitol Vet. 2013;22:1-5. https://doi.org/10.1590/S1984-29612013000100002
Klimpel S, Heukelbach J, Pothmann D, Rückert S. Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): High infection risk for humans? Parasitol Res. 2010;107:713-9. https://doi.org/10.1007/s00436-010-1926-7
Romero-Núñez C, Yáñez-Arteaga S, Mendoza-Martínez GD, Bustamante-Montes LP, Ramírez-Durán N. Contaminación y viabilidad de huevos de Toxocara spp. en suelo y heces colectadas en parques públicos, calles y perros en Toluca, México. Rev Cient (Maracaibo). 2013;XXIII:475-9.
ESCCAP. Worm control in dogs and cats, Esccap.org. 2017. Fecha de consulta: 28 de noviembre de 2017. Disponible en: https://www.esccap.org/uploads/docs/ms7v1icy_0778_ESCCAP_GL1_v14_1p.pdf
Bajer A, Bednarska M, Rodo A. Risk factors and control of intestinal parasite infections in sled dogs in Poland. Vet Parasitol. 2011;175:343-50. https://doi.org/10.1016/j.vetpar.2010.10.029
Mircean V, Dumitrache MO, Mircean M, Colosi HA, Györke A. Prevalence and risk factors associated with endoparasitic infection in dogs from Transylvania (Romania): A retrospective study. Vet Parasitol. 2017;243:157-61. https://doi.org/10.1016/j.vetpar.2017.06.028
Alvarado-Esquivel C, Romero-Salas D, Aguilar-Domínguez M, Cruz-Romero A, Ibarra-Priego N, Pérez-de León AA. Epidemiological assessment of intestinal parasitic infections in dogs at animal shelter in Veracruz, México. Asian Pac J Trop Biomed. 2015;5:34-9. https://doi.org/10.1016/S2221-1691(15)30167-2
Martínez-Carrasco C, Berriatua E, Garijo M, Martínez J, Alonso FD, De Ybáñez RR. Epidemiological study of non-systemic parasitism in dogs in southeast Mediterranean Spain assessed by coprological and post-mortem examination. Zoonoses Public Health. 2007;54:195-203. https://doi.org/10.1111/j.1863-2378.2007.01047.x
Robertson ID, Irwin PJ, Lymbery AJ, Thompson RC. The role of companion animals in the emergence of parasitic zoonoses. Int J Parasitol. 2000;30:1369-77. https://doi.org/10.1016/S0020-7519(00)00134-X
Epe C. Intestinal nematodes: Biology and control. Vet Clin North Am Small Anim Pract. 2009;39:1091-107. https://doi.org/10.1016/j.cvsm.2009.07.002
Macpherson CNL. The epidemiology and public health importance of toxocariasis: A zoonosis of global importance. Int J Parasitol. 2013;43:999-1008. https://doi.org/10.1016/j.ijpara.2013.07.004
Ponce-Macotela M, Peralta-Abarca GE, Martínez-Gordillo MN. Giardia intestinalis and other zoonotic parasites: Prevalence in adult dogs from the southern part of Mexico City. Vet Parasitol. 2005;131:1-4. https://doi.org/10.1016/j.vetpar.2005.03.027
Payne PA, Artzer M. The biology and control of Giardia spp. and Tritrichomonas foetus. Vet Clin North Am Small Anim Pract. 2009;39:993-1007. https://doi.org/10.1016/j.cvsm.2009.06.007
Bouzid M, Halai K, Jeffreys D, Hunter PR. The prevalence of Giardia infection in dogs and cats, a systematic review and meta-analysis of prevalence studies from stool samples. Vet Parasitol. 2015;207:181-202. https://doi.org/10.1016/j.vetpar.2014.12.011
Traversa D, Frangipane di Regalbono A, Di Cesare A, La Torre F, Drake J, Pietrobelli M. Environmental contamination by canine geohelminths. Parasit Vectors. 2014;7:67. https://doi.org/10.1186/1756-3305-7-67
Georgi JR, Georgi ME. Parasitología en clínica canina. Madrid, España, PA: Interamericana-McGraw-Hill; 1994.
Palmer CS, Thompson RCA, Traub RJ, Rees R, Robertson ID. National study of the gastrointestinal parasites of dogs and cats in Australia. Vet Parasitol. 2008;151:181-90. https://doi.org/10.1016/j.vetpar.2007.10.015
Conboy G. Cestodes of dogs and cats in North America. Vet Clin North Am Small Anim Pract. 2009;39:1075-90. https://doi.org/10.1016/j.cvsm.2009.06.005
Mitchell SM, Zajac AM, Charles S, Duncan RB, Lindsay DS. Cystoisospora canis Nemeséri, 1959 (syn. Isospora canis), infections in dogs: Clinical signs, pathogenesis, and reproducible clinical disease in beagle dogs fed oocysts. J Parasitol. 2007;93:345-52. https://doi.org/10.1645/GE-1024R.1
Robertson ID, Thompson RC. Enteric parasitic zoonoses of domesticated dogs and cats. Microbes Infect. 2002;4:867-73. https://doi.org/10.1016/S1286-4579(02)01607-6
Márquez-Navarro A, García-Bracamontes G, Álvarez-Fernández BE, Ávila-Caballero LP, Santos-Aranda I, Díaz-Chiguer DL, et al. Trichuris vulpis (Froelich, 1789) infection in a child: A case report. Korean J Parasitol. 2012;50:69-71. https://doi.org/10.3347/kjp.2012.50.1.69
Encalada-Mena LA, Duarte-Ubaldo EL, Vargaz-Magaña JJ, García-Ramírez MJ, Medina-Hernández RE. Prevalence of gastroenteric parasites of dogs in the city of Escárcega, Campeche, México. Univ Cienc. 2011;27:209-17.
Kumsa BE, Mekonnen S. Ixodid ticks, fleas and lice infesting dogs and cats in Hawassa, southern Ethiopia. Onderstepoort J Vet Res. 2011;78:326. https://doi.org/10.4102/ojvr.v78i1.326
Cruz-Vázquez C, Castro-Gámez E, Parada-Fernández M, Ramos-Parra M. Seasonal occurrence of Ctenocephalides felis felis and Ctenocephalides canis (Siphonaptera: Pulicidae) infesting dogs and cats in an urban area in Cuernavaca, México. J Med Entomol. 2001;38:111-3. https://doi.org/10.1603/0022-2585-38.1.111
Hernández-Valdivia E, Cruz-Vázquez C, Ortiz-Martínez R, Valdivia-Flores A, Quintero-Martínez MT. Presence of Ctenocephalides canis (Curtis) and Ctenocephalides felis (Bouché) Infesting dogs In the city of Aguascalientes, México. J Parasitol. 2011;97:1017-9. https://doi.org/10.1645/GE-2701.1
Dantas-Torres F. Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors. 2010;3:26. https://doi.org/10.1186/1756-3305-3-26
Torres-Chable OM, Baak-Baak CM, Cigarroa-Toledo N, Zaragoza-Vera CV, Arjona-Jiménez G, Moreno-Pérez LG, et al. First report of chewing lice Heterodoxus spiniger (Enderlein, 1909) and Trichodectes canis (De Geer, 1778) on domestic dogs at Tabasco, México. Southwest Entomol. 2017;42:409-18. https://doi.org/10.3958/059.042.0211
Low VL, Prakash BK, Tan TK, Sofian-Azirun M, Anwar FHK, Vinnie-Siow WY, et al. Pathogens in ectoparasites from free-ranging animals: Infection with Rickettsia asembonensis in ticks, and a potentially new species of Dipylidium in fleas and lice. Vet Parasitol. 2017;245:102-5. https://doi.org/10.1016/j.vetpar.2017.08.015
Traversa D. Fleas infesting pets in the era of emerging extra-intestinal nematodes. Parasit Vectors. 2013;6:59. https://doi.org/10.1186/1756-3305-6-59
Neira O P, Jofré M L, Muñoz S N. Infección por Dipylidium caninum en un preescolar: presentación del caso y revisión de la literatura. Rev Chilena Infectol. 2008;25:465-71. https://doi.org/10.4067/S0716-10182008000600010
Narasimham MV, Panda P, Mohanty I, Sahu S, Padhi S, Dash M. Dipylidium caninum infection in a child: A rare case report. Indian J Med Microbiol. 2013;31:82-4. https://doi.org/10.4103/0255-0857.108738
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