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Patterns of helminth infections in Rattus rattus and Mus musculus from two Mayan communities in Mexico

Published online by Cambridge University Press:  04 February 2019

J.A. Panti-May Open the ORCID record for J.A. Panti-May [Opens in a new window] ,
E.E. Palomo-Arjona ,
Y.M. Gurubel-González ,
R.C. Barrientos-Medina ,
M.C. Digiani ,
M.R. Robles ,
S.F. Hernández-Betancourt  and
C. Machain-Williams
J.A. Panti-May*
Affiliation:
Doctorado en Ciencias Agropecuarias, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Mexico
E.E. Palomo-Arjona
Affiliation:
Departamento de Zoología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Mexico
Y.M. Gurubel-González
Affiliation:
Departamento de Zoología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Mexico
R.C. Barrientos-Medina
Affiliation:
Departamento de Ecología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Mexico
M.C. Digiani
Affiliation:
CONICET, División Zoología Invertebrados, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina
M.R. Robles
Affiliation:
Centro de Estudios Parasitológicos y de Vectores, CONICET-Universidad Nacional de La Plata, La Plata, Argentina
S.F. Hernández-Betancourt
Affiliation:
Departamento de Zoología, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Mexico
C. Machain-Williams
Affiliation:
Laboratorio de Arbovirología, Centro de Investigaciones Regionales ‘Dr. Hideyo Noguchi’, Universidad Autónoma de Yucatán, Mérida, Mexico
*
Author for correspondence: J.A. Panti-May E-mail: panti.alonso@gmail.com
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Abstract

The black rat Rattus rattus and the house mouse Mus musculus are two commensal rodent species that harbour and shed zoonotic pathogens, including helminths. The aim of this survey was to study the helminth community and the patterns of infections in R. rattus and M. musculus from two Mayan communities in Mexico. Gastrointestinal helminths were isolated from 322 M. musculus and 124 R. rattus, including Gongylonema neoplasticum, Hassalstrongylus aduncus, Hassalstrongylus musculi, Hydatigera taeniaeformis metacestode, Hymenolepis diminuta, Nippostrongylus brasiliensis, Oligacanthorhynchidae gen. sp., Syphacia muris, Syphacia obvelata, Rodentolepis microstoma and Trichuris muris. The overall richness of helminths was seven in R. rattus and six in M. musculus. The results of generalized linear models showed that juvenile rodents had lower probabilities of being infected with G. neoplasticum, H. taeniaeformis and H. musculi than adult rodents. A positive association between the prevalence of S. muris and rat abundance was found. The intensity of infection with S. muris was higher in the rainy season than in the dry season; the opposite result was found for H. musculi infection. Male R. rattus harboured more S. muris specimens. The intensity of infection with T. muris was inversely associated with mouse abundance. The presence of the zoonotic H. diminuta, as well as H. taeniaeformis and R. microstoma in rodent populations indicates that there is risk of transmission, and that their entire life cycle occurs in the study area.

Keywords

Black rathelminth communitieshouse mousepublic health risktropical rural areas
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e30
Copyright
Copyright © Cambridge University Press 2019 

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References

Amin, OM (1987) Key to the families and subfamilies of Acanthocephala, with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida). Journal of Parasitology 73, 1216–1219.Google Scholar
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Tranmission, 2nd edn. Wallingford: CAB International.Google Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Oxfordshire: CAB International.Google Scholar
Balčiauskienė, L et al. (2015) Indoor small mammals in Lithuania: some morphometrical, body condition, and reproductive characteristics. Zoology and Ecology 25, 305–313.Google Scholar
Battersby, S, Hirschhorn, RB and Amman, BR (2008) Commensal rodents. In Bonnefoy, X, Kampen, H and Sweeney, K (eds), Public Health Significance of Urban Pests. Copenhagen: World Health Organization, pp. 387–419.Google Scholar
Behnke, JM (1975) Aspiculuris tetraptera in wild Mus musculus. The prevalence of infection in male and female mice. Journal of Helminthology 49, 85–90.Google Scholar
Behnke, JM and Wakelin, D (1973) The survival of Trichuris muris in wild populations of its natural hosts. Parasitology 67, 157–164.Google Scholar
Behnke, JM et al. (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
Berdoy, M and Drickamer, LC (2007) Comparative social organization and life history of Rattus and Mus. In Sherman, PW and Wolff, JO (eds), Rodent Societies: An Ecological & Evolutionary Perspective. Chicago, IL: The University of Chicago Press, pp. 380–392.Google Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-theoretic Approach, 2nd edn. New York, NY: Springer.Google Scholar
Bush, AO et al. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Carvalho-Pereira, T et al. (2017) The helminth community of a population of Rattus norvegicus from an urban Brazilian slum and the threat of zoonotic diseases. Parasitology 145, 797–806.Google Scholar
Cattadori, IM et al. (2006) Transmission ecology and the structure of parasite communities in small mammals. In Morand, S, Krasnov, BR and Poulin, R (eds), Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo: Springer-Verlag, pp. 349–369.Google Scholar
Cavia, R, Cueto, GR and Suárez, OV (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape and Urban Planning 90, 11–19.Google Scholar
Colwell, RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. Available at http://viceroy.eeb.uconn.edu/estimates/index.html.Google Scholar
Diagne, C et al. (2016) Parasites and invasions: changes in gastrointestinal helminth assemblages in invasive and native rodents in Senegal. International Journal for Parasitology 46, 857–869.Google Scholar
Doran, DJ (1955) A catalogue of the protozoa and helminths of North American rodents. III. Nematoda. American Midland Naturalist 53, 162–175.Google Scholar
Galán-Puchades, MT et al. (2018) First survey on zoonotic helminthosis in urban brown rats (Rattus norvegicus) in Spain and associated public health considerations. Veterinary Parasitology 259, 49–52.Google Scholar
Gales, RP (1982) Age- and sex-related differences in diet selection by Rattus rattus on Stewart Island, New Zealand. New Zealand Journal of Zoology 9, 463–466.Google Scholar
García-Prieto, L, Falcón-Ordaz, J and Guzmán-Cornejo, C (2012) Helminth parasites of wild Mexican mammals: list of species, hosts and geographical distribution. Zootaxa 92, 1–92.Google Scholar
Gupta, N, Khan, DK and Santra, SC (2009) Prevalence of intestinal helminth eggs on vegetables grown in wastewater-irrigated areas of Titagarh, West Bengal, India. Food Control 20, 942–945.Google Scholar
Hall, JE, Sonnenberg, B and Hodes, JR (1955) Some helminth parasites of rodents from localities in Maryland and Kentucky. Journal of Parasitology 41, 640–641.Google Scholar
Hancke, D, Navone, GT and Suarez, OV (2011) Endoparasite community of Rattus norvegicus captured in a shantytown of Buenos Aires city, Argentina. Helminthologia 48, 167–173.Google Scholar
Himsworth, CG et al. (2014) The characteristics of wild rat (Rattus spp.) populations from an inner-city neighborhood with a focus on factors critical to the understanding of rat-associated zoonoses. PLoS ONE 9, e91654.Google Scholar
Instituto Nacional de Estadística y Geografía (2012) Inventario nacional de viviendas. Available at: http://www3.inegi.org.mx/sistemas/mapa/inv/Default.aspx?bi=1 (accessed 25 May 2013).Google Scholar
International Fund for Agricultural Development (2016) Rural Development Report 2016. Rome: International Fund for Agricultural Development.Google Scholar
Jarrett, EEE, Jarrett, WFH and Urquhart, GM (1966) Immunological unresponsiveness in adult rats to the nematode Nippostrongylus brasiliensis induced by infection in early life. Nature 211, 1310–1311.Google Scholar
Jones, A and Pybus, MJ (2001) Taeniasis and echinococcosis. In Samuel, WM, Pybus, MJ and Kocan, AA (eds), Parasitic Diseases of Wild Mammals. Ames, IA: Iowa State University Press, pp. 150–192.Google Scholar
Julius, RS, Schwan, EV and Chimimba, CT (2018) Helminth composition and prevalence of indigenous and invasive synanthropic murid rodents in urban areas of Gauteng Province, South Africa. Journal of Helminthology 92, 445–454.Google Scholar
Khalil, LF, Jones, A and Bray, RA (1994) Key to the Cestode Parasites of Vertebrates. Wallingford: CAB International.Google Scholar
Khanam, S et al. (2017) Population ecology of the house mouse (Mus musculus) in rural human habitations of Pothwar, Pakistan. Zoology and Ecology 27, 106–113.Google Scholar
King, OM (1950) An ecological study of the Norway rat and the house mouse in a city block in Lawrence, Kansas. Transactions of the Kansas Academy of Science 53, 500–528.Google Scholar
Landaeta-Aqueveque, CA, Robles, M and Cattan, PE (2007) The community of gastrointestinal helminths in the house mouse, Mus musculus, in Santiago, Chile. Parasitología Latinoamericana 62, 165–169.Google Scholar
Lloyd, S and Soulsby, EJ (1978) The role of IgA immunoglobulins in the passive transfer of protection to Taenia taeniaeformis in the mouse. Immunology 34, 939–945.Google Scholar
Macnish, MG et al. (2003) Detection of the rodent tapeworm Rodentolepis (=Hymenolepis) microstoma in humans. A new zoonosis? International Journal for Parasitology 33, 1079–1085.Google Scholar
Meerburg, BG, Singleton, GR and Kijlstra, A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221–270.Google Scholar
Mega, JD, Galdos-Cardenas, G and Gilman, RH (2013) Tapeworm infections. In Magill, AJ et al. (eds), Hunter's Tropical Medicine and Emerging Infectious Disease. China: Elsevier, pp. 895–902.Google Scholar
Melo, MC et al. (2014) Spermatogenesis recovery in protein-restricted rats subjected to a normal protein diet after weaning. Reproduction, Fertility and Development 26, 787–796.Google Scholar
Milazzo, C et al. (2003) Helminths and ectoparasites of Rattus rattus and Mus musculus from Sicily, Italy. Comparative Parasitology 70, 199–204.Google Scholar
Mohd Zain, SN, Behnke, JM and Lewis, JW (2012) Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasites & Vectors 5, 47.Google Scholar
Nelson, L and Clark, FW (1973) Correction for sprung traps in catch/effort calculations of trappring results. Journal of Mammalogy 54, 295–298.Google Scholar
Panti-May, JA et al. (2012) Abundance and population parameters of commensal rodents present in rural households in Yucatan, Mexico. International Biodeterioration and Biodegradation 66, 77–81.Google Scholar
Panti-May, JA et al. (2015) Infection levels of intestinal helminths in two commensal rodent species from rural households in Yucatan, Mexico. Journal of Helminthology 89, 42–48.Google Scholar
Panti-May, JA et al. (2016) A two-year ecological study of Norway rats (Rattus norvegicus) in a Brazilian urban slum. PLoS ONE 11, e0152511.Google Scholar
Panti-May, JA et al. (2017) New host, geographical records, and factors affecting the prevalence of helminths infection from synanthropic rodents in Yucatán, Mexico. Helminthologia 54, 231–239.Google Scholar
Price, PW (1990) Host populations as resources defining parasite community organization. In Esch, G, Bush, A and Aho, J (eds), Parasite Communities: Patterns and Processes. New York, NY: Chapman & Hall, pp. 21–40.Google Scholar
Pulido-Flores, G, Moreno-Flores, S and Monks, S (2005) Helminths of rodents (Rodentia: Muridae) from Metztitlán, San Cristobal, and Rancho Santa Elena, Hidalgo, Mexico. Comparative Parasitology 72, 186–192.Google Scholar
R Core Team (2014) R: A Language and Environment for Statistical Computing. Version 3.1. 3. Available at https://www.r-project.org/.Google Scholar
Secretaría de Desarrollo Social (2015) Programa para el desarrollo de zonas prioritarias: Cobertura 2015. Available at http://www.sedesol.gob.mx/en/SEDESOL/Zonas_de_Atencion_Priorita (accessed 16 June 2016).Google Scholar
Simões, RO et al. (2016) Biotic and abiotic effects on the intestinal helminth community of the brown rat Rattus norvegicus from Rio de Janeiro, Brazil. Journal of Helminthology 90, 21–27.Google Scholar
Sterba, J, Blazer, K and Barus, V (1977) Contribution to the pathology of Strobilocercosis (Strobilocercus fasciolaris) in the liver of man and some animals. Folia Parasitologica 24, 41–46.Google Scholar
Swanson, JA and Bone, LW (1983) Host influences on reproduction and establishment of mouse-adapted Nippostrongylus brasiliensis (Nematoda). Journal of Parasitology 69, 890–896.Google Scholar
Taffs, LF (1976) Pinworm infections in laboratory rodents: a review. Laboratory Animals 10, 1–13.Google Scholar
Tay Zavala, J et al. (1999) Zoonosis por helmintos en mamíferos de Morelia, Michoacán, República Mexicana. Revista de la Facultad de Medicina UNAM 42, 64–65.Google Scholar
Theis, JH and Schwab, RG (1992) Seasonal prevalence of Taenia taeniaeformis: relationship to age, sex, reproduction and abundance of an intermediate host (Peromyscus maniculatus). Journal of Wildlife Diseases 28, 42–50.Google Scholar
UN-Habitat (2016) Urbanization and Development: Emerging Futures. Nairobi: United Nations Human Settlements Programme.Google Scholar
Vakis, R, Rigolini, J and Lucchetti, L (2015) Overview: Left Behind: Chronic Poverty in Latin America and the Caribbean. Washington, DC: World Bank.Google Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th edn. New York, NY: Springer.Google Scholar
Waugh, CA et al. (2006) Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. Journal of Parasitology 92, 1014–1018.Google Scholar
Worth, CB (1950) Field and laboratory observations on roof rats, Rattus rattus (Linnaeus), in Florida. Journal of Mammalogy 31, 293–304.Google Scholar