Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T03:42:10.343Z Has data issue: false hasContentIssue false

Predictors of parasite and pathogen infections in urban rodents of central Argentina

Published online by Cambridge University Press:  09 December 2021

B. Fitte
Affiliation:
Centro de Estudios Parasitológicos y de Vectores, CEPAVE (CCT La Plata CONICET UNLP), La Plata, Argentina
R. Cavia*
Affiliation:
Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA), UBA-CONICET, Buenos Aires, Argentina
M. del Rosario Robles
Affiliation:
Centro de Estudios Parasitológicos y de Vectores, CEPAVE (CCT La Plata CONICET UNLP), La Plata, Argentina
A. Dellarupe
Affiliation:
Laboratorio de Inmunoparasitología, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, La Plata, Argentina
J.M. Unzaga
Affiliation:
Laboratorio de Inmunoparasitología, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, La Plata, Argentina
G.T. Navone
Affiliation:
Centro de Estudios Parasitológicos y de Vectores, CEPAVE (CCT La Plata CONICET UNLP), La Plata, Argentina
*
Author for correspondence: Regino Cavia, E-mail: [email protected]

Abstract

Urban rodents are associated with parasites and pathogens, which present health risks for humans, but information on factors related to parasite and pathogen infection in rodents in cities of Latin America is scarce. This study analyzes the hosts, host community structure and environmental characteristics of parasite and pathogen fauna present in the three species of urban rodents in an urban area of South America. Rodents were captured seasonally in seven different neighborhoods. Digestive tracts were dissected under stereoscopic microscopy and feces were processed using a sedimentation technique. Protozoa and bacteria were detected through polymerase chain reaction and indirect immunofluorescence techniques. In Rattus norvegicus, Rattus rattus and Mus musculus, ten helminths, three protozoa and two bacteria were found. Six were zoonotic: Toxoplasma gondii; Hymenolepis diminuta; Rodentolepis nana; Strobilocercus fasciolaris; Leptospira borgpetersenii; and Leptospira interrogans. The parasite and pathogen infections were influenced by the host species, the host community structure, the season, and the presence of streams in the neighborhood. Urban rodents may be the infection source of many zoonotic diseases and it is important to generate public policies for this problem. This study is one example of the situation of many cities of Latin America, where peripheral neighborhoods are growing dramatically.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agudelo-Flórez, P, Londoño, AF, Quiroz, VH, Ángel, JC, Moreno, N, Loaiza, ET and Rodas, JD (2009) Prevalence of Leptospira spp. in urban rodents from a groceries trade center of Medellin, Colombia. American Journal of Tropical Medicine and Hygiene 81(5), 906910.CrossRefGoogle ScholarPubMed
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates: Archival volume. Wallingford, CAB International.CrossRefGoogle Scholar
Arneberg, P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25(1), 8894.CrossRefGoogle Scholar
Battersby, S, Parsons, R and Webster, J (2002) Urban rat infestations and the risk to public health. International Journal of Environmental Health Research 1, 5765.Google Scholar
Behnke, JM, Harris, PD, Bajer, A, Barnard, CJ, Sherif, N and Cliffe, L (2004) Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St Katherine region of the Sinai Peninsula in Egypt. Parasitology 129(3), 379398.CrossRefGoogle ScholarPubMed
Bonnefoy, X, Kampen, H and Sweeney, K (2008) Public health significance of urban pests. Copenhaguen, World Health Organization.Google Scholar
Bordes, F, Blasdell, K and Morand, S (2015) Transmission ecology of rodent-borne diseases: new frontiers. Integrative Zoology 10(5), 424435.CrossRefGoogle ScholarPubMed
Bradley, CA and Altizer, S (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22(2), 95102.CrossRefGoogle ScholarPubMed
Burnham, KP and Anderson, DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. vol. 65, no 1, p. 23-35. Fort Collins, Springer Science & Business Media.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83(4), 575583.CrossRefGoogle Scholar
Calero, C, Ortiz, O and Souza, L (1950) Helminths in rats from Panama city and suburbs. Journal of Parasitology 36(5), 426.Google ScholarPubMed
Cavia, R, Cueto, G and Suárez, O (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape and Urban Planning 90(1–2), 1119.CrossRefGoogle Scholar
Cavia, R, Cueto, GR and Suárez, OV (2012) Techniques to estimate abundance and monitoring rodent pests in urban environments. pp. 147172 in Larramendy, Marcelo L., Soloneski, Sonia (Eds) Integrated pest management and pest control—current and future tactics. Rijeka, InTech.Google Scholar
Cavia, R, Gómez Villafañe, I, Suárez, OV, Gómez, MD, Sánchez, J and León, V (2019a) Mus musculus Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina: SAREM. Available at http://cma.sarem.org.ar (accessed 30 November 2021).Google Scholar
Cavia, R, Gómez Villafañe, I, Suárez, OV, Piudo, L, Sánchez, J and Monteverde, M (2019b) Rattus norvegicus Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina: SAREM. Available at http://cma.sarem.org.ar (accessed 30 November 2021).Google Scholar
Cavia, R, Gómez Villafañe, I, Suárez, OV, Piudo, L, Sánchez, J and Monteverde, M. (2019c) Rattus rattus. Categorización 2019 de los mamíferos de Argentina según su riesgo de extinción. Lista Roja de los mamíferos de Argentina: SAREM. Available at http://cma.sarem.org.ar (accessed 30 November 2021).Google Scholar
Chace, JF and Walsh, JJ (2006) Urban effects on native avifauna: a review. Landscape and Urban Planning 74(1), 4669.CrossRefGoogle Scholar
Chaiblich, JV, Lima, MLDS, Oliveira, RFD, Monken, M and Penna, MLF (2017) Spatial study of risks to leptospirosis in the municipality of Rio de Janeiro (RJ). Saúde em Debate 41(SPE2), 225240.CrossRefGoogle Scholar
Childs, JE, McLafferty, SL, Sadek, R, Miller, GL, Khan, AS, DuPree, ER and Glass, GE (1998) Epidemiology of rodent bites and prediction of rat infestation in New York city. American Journal of Epidemiology 148(1), 7887.CrossRefGoogle ScholarPubMed
Costa, F, Porter, FH, Rodrigues, G, Farias, H and de Faria, MT (2014) Infections by Leptospira interrogans, Seoul virus, and Bartonella spp. among Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Vector-Borne Zoonotic Diseases 14(1), 3340.CrossRefGoogle ScholarPubMed
Coto, H (2015) Protocolos para la vigilancia y control de roedores sinantrópicos. Washington, D.C., Organización Panamericana de la Salud.Google Scholar
De León, D (1964) Helminth parasites of rats in San Juan, Puerto Rico. J Parasitol 50(3), 478479.CrossRefGoogle Scholar
Dellarupe, A, Fitte, B, Pardini, L and Campero, LM (2019) Toxoplasma gondii and Neospora caninum infections in synanthropic rodents from Argentina. Revista Brasilera de Parasitologia Veterinaria 28(1), 113118.CrossRefGoogle ScholarPubMed
de Masi, E, Vilaça, P and Razzolini, MTP (2009) Environmental conditions and rodent infestation in Campo Limpo district, Sao Paulo municipality, Brazil. International Journal of Environmental Health Research 19(1), 116.CrossRefGoogle Scholar
Deter, J, Chaval, Y, Galan, M, Berthier, K, Salvador, AR and Garcia, JCC (2007) Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species. International Journal of Parasitology 37(7), 813824.CrossRefGoogle Scholar
Dubey, J and Frenkel, J (1998) Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Veterinary Parasitology 77(1), 132.CrossRefGoogle ScholarPubMed
Easterbrook, JD, Kaplan, J, Vanasco, N, Reeves, W, Purcell, R and Kosoy, M (2007) A survey of zoonotic pathogens carried by Norway rats in Baltimore, Maryland, USA. Epidemiological Infection 135(7), 11921199.CrossRefGoogle ScholarPubMed
Fitte, B and Kosoy, M (2021) Presence of Leptospira spp. and absence of Bartonella spp. in urban rodents of Buenos Aires province, Argentina. Pathogens and Global Health, 18.CrossRefGoogle Scholar
Fitte, B, Robles, M, Dellarupe, A, Unzaga, JM and Navone, GT (2017) Taenia taeniformis larvae (Strobilocercus fasciolaris) (Cestoda: Cyclophyllidea) from commensal rodents in Argentina: potential sanitary risk. Mastozoología Neotropical 24(1), 227233.Google Scholar
Franjola, T, Soto, G and Montefusco, A (1995) Prevalencia de infección por protozoos en roedores sinantrópicos de la ciudad de Valdivia en Chile. Boletín Chileno de Parasitología 50(3/4), 6672.Google Scholar
Gibbons, LM (2010) Keys to the nematode parasites of vertebrates: Supplementary volume (Vol. 10). Wallingford, CAB International.Google Scholar
Gómez Villafañe, IE, Robles, MR and Busch, M (2008) Helminth communities and host–parasite relationships in Argentine brown rat (Rattus norvegicus). Helminthologia 45(3), 127130.CrossRefGoogle Scholar
Gómez Villafañe, IE, Cavia, R, Vadell, MV, Suárez, OV and Busch, M (2012) Differences in population parameters of Rattus norvegicus in urban and rural habitats of central Argentina. Mammalia 77(2), 187–193.Google Scholar
Guerreiro Martins, NB, Robles, MdR and Navone, GT (2014) Distribución geográfica de cestodes Hymenolepididae de Oxymycterus rufus (rodentia - cricetidae) en Argentina. Revista Argentina de Parasitología 2, 1624.Google Scholar
Haley, AJ (1962) Biology of the rat nematode, Nippostrongylus brasiliensis (Travassos, 1914). II. Preparasitic stages and development in the laboratory rat. Journal of Parasitology 48(1), 1323.CrossRefGoogle Scholar
Hancke, D and Suárez, OV (2017) Helminth diversity in synanthropic rodents from an urban ecosystem. EcoHealth 14(3), 603613. doi: 10.1007/s10393-017-1239-8CrossRefGoogle ScholarPubMed
Hancke, D, Navone, GT and Suarez, OV (2011) Endoparasite community of Rattus norvegicus captured in a shantytown of Buenos Aires city, Argentina. Helminthologia 48(3), 167173.CrossRefGoogle Scholar
Hassell, JM, Begon, M, Ward, MJ and Fèvre, EM (2017) Urbanization and disease emergence: dynamics at the wildlife–livestock–human interface. Trends in Ecology and Evolution 32(1), 5567.CrossRefGoogle Scholar
Himsworth, CG, Parsons, KL, Jardine, C and 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 Zoonotic Diseases 13(6), 349359.CrossRefGoogle ScholarPubMed
Jittapalapong, S, Herbreteau, V, Hugot, JP, Arreesrisom, P, Karnchanabanthoeng, A, Rerkamnuaychoke, W and Morand, S (2009) Relationship of parasites and pathogens diversity to rodents in Thailand. Kasetsart Journal of Natural Science 43, 106117.Google Scholar
Johnson, PT, De Roode, JC and Fenton, A (2015) Why infectious disease research needs community ecology. Science 349(6252), 1259504.CrossRefGoogle ScholarPubMed
Kataranovski, M, Mirkov, I, Belij, S, Popov, A, Petrović, Z, Gačić, Z and Kataranovski, D (2011) Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat. Parasite 18(2), 189196.CrossRefGoogle ScholarPubMed
Khalil, LF, Jones, A and Bray, RA (1994) Keys to the cestode parasites of vertebrates. Wallingford, CAB International.Google Scholar
Kosoy, M, Khlyap, L, Cosson, JF and Morand, S (2015) Aboriginal and invasive rats of genus Rattus as hosts of infectious agents. Vector-Borne Zoonotic Diseases 15(1), 312.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA x: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6), 15471549..CrossRefGoogle ScholarPubMed
Landaeta-Aqueveque, CA, Robles, MD and Cattan, PE (2007) Helmintofauna del roedor Abrothrix olivaceus (Sigmodontinae) en áreas sub-urbanas de Santiago de Chile. Parasitología Latinoamericana 62(3-4), 134141.CrossRefGoogle Scholar
Lavikainen, A, Iwaki, T, Haukisalmi, V, Konyaev, SV, Casiraghi, M, Dokuchaev, NE and Nakao, M (2016) Reappraisal of Hydatigera taeniaeformis (Batsch, 1786) (Cestoda: Taeniidae) sensu lato with description of Hydatigera kamiyai n. sp. International Journal for Parasitology 46(5-6), 361374.CrossRefGoogle ScholarPubMed
Legendre, P and Legendre, L (2012) Numerical Ecology. 990 pages. Amsterdam, Elsevier.Google Scholar
Lobos, G, Ferres, M and Palma, RE (2005) Presencia de los géneros invasores Mus y Rattus en áreas naturales de Chile: un riesgo ambiental y epidemiológico. Revista Chilena de Historia Natural 78(1), 113124.CrossRefGoogle Scholar
Lovera, R, Fernández, MS, Jacob, J, Lucero, N, Morici, G, Brihuega, B and Cavia, R (2017) Intrinsic and extrinsic factors related to pathogen infection in wild small mammals in intensive milk cattle and swine production systems. PLoS Neglected Tropical Diseases 11(6), e0005722. https://doi.org/10.1371/journal.pntd.0005722.CrossRefGoogle ScholarPubMed
Lykins, J, Wang, K, Wheeler, K, Clouser, F, Dixon, A, El Bissati, K and McLeod, R (2016) Understanding toxoplasmosis in the United States through “large data” analyses. Reviews of Infectious Diseases 63(4), 468475.CrossRefGoogle ScholarPubMed
Meerburg, BG, Singleton, GR and Kijlstra, A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35(3), 221270.CrossRefGoogle ScholarPubMed
Milazzo, C, de Bellocq, JG, Cagnin, M, Casanova, JC, Di Bella, C, Feliu, C and Santalla, F (2003) Helminths and ectoparasites of Rattus rattus and Mus musculus from Sicily, Italy. Comparative Parasitology 70(2), 199205.CrossRefGoogle Scholar
Mills, JN, Ellis, BA, Mckee, KT, Maiztegui, JI and Childs, JE (1991) Habitat associations and relative densities of rodent populations in cultivated areas of central Argentina. Journal of Mammalogy 72(3), 470479.CrossRefGoogle Scholar
Ministerio de Salud de la Nación (MSAL) (2014) Dirección de Epidemiología. Leptospirosis. Guia para el Equipo de Salud. Cdad. Autónoma de Bs. As., Argentina: Dirección de Epidemiologıa—Ministerio de Salud de la Nación; ISSN 1852-1819 / ISSN 1852-219X (online).Google Scholar
Morand, S and Poulin, R (1998) Density, body mass and parasite species richness of terrestrial mammals. Ecology and Evolution 12(6), 717727.CrossRefGoogle Scholar
Moré, G, Pardini, L, Basso, W, Machuca, M, Bacigalupe, D, Villanueva, M and Venturini, L (2010) Toxoplasmosis and genotyping of Toxoplasma gondii in Macropus rufus and Macropus giganteus in Argentina. Veterinary Parasitology 169(1–2), 5761.CrossRefGoogle ScholarPubMed
Muradian, V, Ferreira, LR, Lopes, EG, de Oliveira Esmerini, P, de Jesus Pena, HF, Soares, RM and Gennari, SM (2012) A survey of Neospora caninum and Toxoplasma gondii infection in urban rodents from Brazil. Journal of Parasitology 98(1), 128134.CrossRefGoogle ScholarPubMed
Nagorsen, D (2005) Rodents and lagomorphs of British Columbia (Vol. 4). British Columbia Royal BC Museum Victoria.Google Scholar
Oksanen, J, Blanchet, FG, Kindt, R, Oksanen, MJ and Suggests, M (2013) Package ‘vegan’. Community Ecology Package Version, 2, 0-0.Google Scholar
Panti-May, J, Hernández-Betancourt, S, Rodríguez-Vivas, R and Robles, MR (2015) Infection levels of intestinal helminths in two commensal rodent species from rural households in Yucatan, Mexico. Journal of Helminthology 89(1), 4248.CrossRefGoogle ScholarPubMed
Panti-May, J, Digiani, MC, Palomo-Arjona, EE, Gurubel-González, YM, Navone, GT, Williams, C and Robles, M (2018) A checklist of the helminth parasites of sympatric rodents from two Mayan villages in Yucatán, México. Zootaxa 4403(3), 495512.CrossRefGoogle ScholarPubMed
Poulin, R (2004) Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5(5), 423434.CrossRefGoogle Scholar
Poulin, R (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal of Parasitology 44(9), 581589.CrossRefGoogle ScholarPubMed
Poulin, R and George-Nascimento, M (2007) The scaling of total parasite biomass with host body mass. International Journal of Parasitology 37(3-4), 359364.CrossRefGoogle ScholarPubMed
Puckett, EE, Park, J, Combs, M, Blum, MJ, Bryant, JE, Caccone, A and Himsworth, CG (2016) Global population divergence and admixture of the brown rat (Rattus norvegicus). Proceedings of the Royal Society B: Biological Sciences 283(1841), 20161762.CrossRefGoogle Scholar
R Core Team (2013) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. ISBN 3-900051-07-0.Google Scholar
Robles, MdR, Navone, GT and Villafañe, IEG (2008) New morphological details and first records of Heterakis spumosa and Syphacia muris from Argentina. Comparative Parasitology 75(1), 145149.CrossRefGoogle Scholar
Rothenburger, JL, Himsworth, CH, Nemeth, NM, Pearl, DL and Jardine, CM (2017) Environmental factors and zoonotic pathogen ecology in urban exploiter species. EcoHealth 14(3), 630641.CrossRefGoogle ScholarPubMed
Schapira, MFP (2001) Fragmentación espacial y social: conceptos y realidades. Revista de la Facultad Latinoamericana de Ciencias Sociales, Sede México 9(19), 3356.Google Scholar
Seifollahi, Z, Sarkari, B, Motazedian, MH, Asgari, Q, Ranjbar, MJ and Abdolahi Khabisi, S (2016) Protozoan parasites of rodents and their zoonotic significance in Boyer–Ahmad District, southwestern Iran. Veterinary Medicine International 2016. doi:10.1155/2016/3263868.CrossRefGoogle ScholarPubMed
Soares, TSM, Latorre, MDRDDO, Laporta, GZ and Buzzar, MR (2010) Spatial and seasonal analysis on leptospirosis in the municipality of São Paulo, Southeastern Brazil, 1998 to 2006. Revista de Saúde Pública 44(2), 283291.CrossRefGoogle Scholar
Swain, K, Routray, A, Panigrahi, S, Rath, AP, Sahoo, S and Ganguly, S (2016) Nippostrongylus brasiliensis, an experimental model: a review. International Journal 2(2), 37.Google Scholar
Telfer, S, Lambin, X, Birtles, R, Beldomenico, P, Burthe, S, Paterson, S and Begon, M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330(6001), 243246.CrossRefGoogle Scholar
Thienpont, D, Rochette, F and Vanparijs, O (1979) Diagnóstico de las helmintiasis por medio del examen coprológico (Vol. V617 THId). Beerse, Janssen Research Foundation.Google Scholar
Titus, K, Mosher, JA and Williams, BK (1984) Chance-corrected classification for use in discriminant analysis: ecological applications. American Midland Naturalist 111(1), 17.CrossRefGoogle Scholar
Travassos, L (1914) Contribuições para o conhecimento da fauna helmintolojica brazileira: III. Memórias Do Instituto Oswaldo Cruz 6, 150162.CrossRefGoogle Scholar
Traweger, D and Slotta-Bachmayr, L (2005) Introducing GIS-modelling into the management of a brown rat (Rattus norvegicus Berk.) (Mamm. Rodentia Muridae) population in an urban habitat. Journal of Pest Science 78(1), 1724.CrossRefGoogle Scholar
Traweger, D, Travnitzky, R, Moser, C, Walzer, C and Bernatzky, G (2006) Habitat preferences and distribution of the brown rat (Rattus norvegicus Berk.) in the city of Salzburg (Austria): implications for an urban rat management. Journal of Pest Science 79(3), 113125.CrossRefGoogle Scholar
Vadell, M, Villafañe, IG and Cavia, R (2014) Are life-history strategies of Norway rats (Rattus norvegicus) and house mice (Mus musculus) dependent on environmental characteristics? Wildlfe Research 41(2), 172184.CrossRefGoogle Scholar
Wardle, MA and Mcleod, JA (1952) The zoology of tapeworms. 780 pp. Minneapolis, University of Minnesota Press.Google Scholar
Waugh, CA, Lindo, JF, Foronda, P, Ángeles-Santana, M, Lorenzo-Morales, J and Robinson, RD (2006) Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. Journal of Parasitology 92(5), 10141019.CrossRefGoogle Scholar
Zain, SNM, Behnke, JM and Lewis, JW (2012) Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasites Vector 5(1), 47.CrossRefGoogle Scholar
Zuur, A, Ieno, EN, Walker, N, Saveliev, AA and Smith, GM (2009) Mixed effects models and extensions in ecology with R. New York, Springer.CrossRefGoogle Scholar
Supplementary material: File

Fitte et al. supplementary material

Fitte et al. supplementary material

Download Fitte et al. supplementary material(File)
File 20 KB