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The helminth community of a population of Rattus norvegicus from an urban Brazilian slum and the threat of zoonotic diseases

Published online by Cambridge University Press:  08 November 2017

Ticiana Carvalho-Pereira ,
Fábio N. Souza ,
Luana R. N. Santos ,
Ruth Walker ,
Arsinoê C. Pertile ,
Daiana S. de Oliveira ,
Gabriel G. Pedra ,
Amanda Minter ,
Maria Gorete Rodrigues  and
Thiago C. Bahiense
...Show all authors
Ticiana Carvalho-Pereira*
Affiliation:
Federal University of Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Fábio N. Souza
Affiliation:
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Luana R. N. Santos
Affiliation:
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Ruth Walker
Affiliation:
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Arsinoê C. Pertile
Affiliation:
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Daiana S. de Oliveira
Affiliation:
Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Gabriel G. Pedra
Affiliation:
Institute of Integrative Biology, University of Liverpool, Liverpool, UK
Amanda Minter
Affiliation:
Institute of Integrative Biology, University of Liverpool, Liverpool, UK
Maria Gorete Rodrigues
Affiliation:
Centro de Controle de Zoonoses, Secretaria Municipal de Saúde, Ministério da Saúde, Salvador, Brazil
Thiago C. Bahiense
Affiliation:
Federal University of Bahia, UFBA, Salvador, Brazil
Mitermayer G. Reis
Affiliation:
Federal University of Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil Department of Epidemiology of Microbial Disease, Yale School of Public Health, New Haven, USA
Peter J. Diggle
Affiliation:
Lancaster Medical School, Lancaster University, Lancaster, UK
Albert I. Ko
Affiliation:
Department of Epidemiology of Microbial Disease, Yale School of Public Health, New Haven, USA
James E. Childs
Affiliation:
Department of Epidemiology of Microbial Disease, Yale School of Public Health, New Haven, USA
Eduardo M. da Silva
Affiliation:
Federal University of Bahia, UFBA, Salvador, Brazil
Mike Begon
Affiliation:
Institute of Integrative Biology, University of Liverpool, Liverpool, UK
Federico Costa
Affiliation:
Federal University of Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil Institute of Integrative Biology, University of Liverpool, Liverpool, UK Department of Epidemiology of Microbial Disease, Yale School of Public Health, New Haven, USA
*
Author for correspondence: Ticiana Carvalho-Pereira, E-mail: [email protected]
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Abstract

Urban slums provide suitable conditions for infestation by rats, which harbour and shed a wide diversity of zoonotic pathogens including helminths. We aimed to identify risk factors associated with the probability and intensity of infection of helminths of the digestive tract in an urban slum population of Rattus norvegicus. Among 299 rats, eleven species/groups of helminths were identified, of which Strongyloides sp., Nippostrongylus brasiliensis and, the human pathogen, Angiostrongylus cantonensis were the most frequent (97, 41 and 39%, respectively). Sex interactions highlighted behavioural differences between males and females, as eg males were more likely to be infected with N. brasiliensis where rat signs were present, and males presented more intense infections of Strongyloides sp. Moreover, rats in poor body condition had higher intensities of N. brasiliensis. We describe a high global richness of parasites in R. norvegicus, including five species known to cause disease in humans. Among these, A. cantonensis was found in high prevalence and it was ubiquitous in the study area – knowledge which is of public health importance. A variety of environmental, demographic and body condition variables were associated with helminth species infection of rats, suggesting a comparable variety of risk factors for humans.

Keywords

Rattus norvegicushelminth communityslum settlementshuman pathogensAngiostrongylus cantonensisrisk factorsspillover riskurban
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 797 - 806
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Copyright
Copyright © Cambridge University Press 2017 

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References

Adejinmi, JO and Emikpe, GE (2011) Helminth parasites of some wildlife in Asejire Game Reserve, Nigeria. South African Journal of Wildlife Research 41, 214–217.CrossRefGoogle Scholar
Alicata, JE (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Advances in Parasitology 3, 223–248.CrossRefGoogle ScholarPubMed
Almeida, A, Corrigan, R and Sarno, R (2013) The economic impact of commensal rodents on small businesses in Manhattan's Chinatown: trends and possible causes. Suburban Sustainability 1, 1–12.CrossRefGoogle Scholar
Alruzug, IM, Khormi, MM and Alhanoo, IK (2016) Hymenolepis nana human diagnosed through colonoscopy: a case report. Bacteriology & Parasitology 7, 265.Google Scholar
Araújo, P (1967) Helmintos de Rattus norvegicus (Berkenhout, 1769) da cidade de São Paulo. Revista da Faculdade de Farmácia e Bioquímica da Universidade de São Paulo 5, 141–159.Google Scholar
Bartlett, MS, Harper, K, Smith, N, Verbanac, P and Smith, JW (1978) Comparative evaluation of a modified zinc sulfate flotation technique. Journal of Clinical Microbiology 7, 524–528.Google Scholar
Beldomenico, PM and Begon, M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology & Evolution 25, 21–27.CrossRefGoogle ScholarPubMed
Calhoun, JB (1962) The Ecology and Sociology of the Norway Rat. US Department of Health Education and Welfare, Public Health Service Publication No. 1008, USA.Google Scholar
Carvalho, OS, Scholte, RGC, Mendonça, CLF, Passos, LKJ and Caldeira, RL (2012) Angiostrongylus cantonensis (Nematode: Metastrongyloidea) in molluscs from harbour areas in Brazil. Memórias do Instituto Oswaldo Cruz 107, 740–746.Google Scholar
Childs, JE, McLafferty, SL, Sadek, R, Miller, GL, Khan, AS, DuPree, ER, Advani, R, Mills, JN and Glass, GE (1998) Epidemiology of rodent bites and prediction of rat infestation in New York city. American Journal of Epidemiology 148, 78–87.CrossRefGoogle ScholarPubMed
Costa, F, Ribeiro, GS, Felzemburgh, RDM, Santos, N, Reis, RB, Santos, AC, Fragal, DBM, Araujo, WN, Santana, C, Childs, JE, Reis, MG and Ko, AI (2014 a) Influence of household rat infestation on Leptospira transmission in the urban slum environment. PLoS Neglected Tropical Diseases 8, e3338.CrossRefGoogle ScholarPubMed
Costa, F, Porter, FH, Rodrigues, G, Farias, H, de Faria, MT, Wunder, EA, Osikowicz, LM, Kosoy, MY, Reis, MG, Ko, AI and Childs, JE (2014 b) Infections by Leptospira interrogans, seoul virus, and Bartonella spp. Among Norway rats (Rattus norvegicus) from the Urban Slum Environment in Brazil. Vector-Borne and Zoonotic Diseases 14, 33–40.CrossRefGoogle ScholarPubMed
Costa, F, Hagan, JE, Calcagno, J, Kane, M, Torgerson, P, Martinez-Silveira, MS, Stein, C, Abela-Ridder, B and Ko, AI (2015 a) Global morbidity and mortality of leptospirosis: a systematic review. PLoS Neglected Tropical Diseases 9, e0003898.Google Scholar
Costa, F, Wunder, EA Jr., De Oliveira, D, Bisht, V, Rodrigues, G, Reis, MG, Ko, AI, Begon, M and Childs, JE (2015 b) Patterns in Leptospira Shedding in Norway rats (Rattus norvegicus) from Brazilian Slum Communities at high risk of disease transmission. PLoS Neglected Tropical Diseases 9, e0003819.Google Scholar
Crawley, MJ (2007) The R Book. 1st edn. Chichester, UK: John Wiley & Sons, Ltd.Google Scholar
Cringoli, G, Rinaldi, L, Veneziano, V, Capelli, G and Scala, A (2004) The influence of flotation solution, sample dilution and the choice of McMaster slide area (volume) on the reliability of the McMaster technique in estimating the faecal egg counts of gastrointestinal strongyles and Dicrocoelium dendriticum in sheep. Veterinary Parasitology 123, 121–131.Google Scholar
De Faria, MT, Calderwood, MS, Athanazio, DA, McBride, AJA, Hartskeerl, RA, Pereira, MM, Ko, AI and Reis, MG (2008) Carriage of Leptospira interrogans among domestic rats from an urban setting highly endemic for leptospirosis in Brazil. Acta Tropica 108, 1–5.Google Scholar
Dineen, JK and Kelly, JD (1973) Immunological unresponsiveness of neonatal rats to infection with Nippostrongylus brasiliensis the competence of neonatal lymphoid cells in worm expulsion. Immunology 25, 141–150.Google Scholar
Falcón-Ordaz, J, Pulido-Flores, G and Monks, S (2010) New species of Aspiculuris (Nematoda: Heteroxynematidae), parasite of Mus musculus (Rodentia: Muridae), from Hidalgo, Mexico. Revista Mexicana de Biodiversidad 81, 669–676.Google Scholar
Faust, EC, D'Antoni, JS, Odom, V, Miller, MJ, Peres, C, Sawitz, W, Thomen, LF, Tobie, J and Walker, JH (1938) A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces I. Preliminary communication. American Journal of Tropical Medicine 18, 169–183.Google Scholar
Felzemburgh, RDM, Ribeiro, GS, Costa, F, Reis, RB, Hagan, JE, Melendez, AXTO, Fraga, D, Santana, FS, Mohr, S, dos Santos, BL, Silva, AQ, Santos, AC, Ravines, RR, Tassinari, WS, Carvalho, MS, Reis, MG and Ko, AI (2014) Prospective study of leptospirosis transmission in an Urban Slum Community: role of poor environment in repeated exposures to the Leptospira agent. PLoS Neglected Tropical Diseases 8, e2927.CrossRefGoogle Scholar
Garcia, MHO, Moraes, C, Almada, GL and Araújo, WN (2008) Investigação de casos de meningite eosinofílica causada pela infecção por angiostrongylus cantonensis no Espírito Santo, Brasil. Secretaria de Vigilância em Saúde – Boletim Eletrônico Epidemiológico, 8, 1–5.Google Scholar
Gillespie, TR and Chapman, CA (2006) Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 20, 441–448.CrossRefGoogle ScholarPubMed
Glass, GE, Childs, JE, Korch, GW and LeDuc, JW (1988) Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiology & Infection 101, 459–472.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, 126–129.CrossRefGoogle Scholar
Gordon, H Mcl. and Whitlock, HV (1939) A new technique four counting nematode eggs in sheep faeces. Journal of Scientific & Industrial Research 12, 50–52.Google Scholar
Hacker, KP, Minter, A, Begon, M, Diggle, PJ, Serrano, S, Reis, MG, Childs, JE, Ko, AI and Costa, F (2016) A comparative assessment of track plates to quantify fine scale variations in the relative abundance of Norway rats in urban slums. Urban Ecosystems 19, 561–575.Google Scholar
Hagan, JE, Moraga, P, Costa, F, Capian, N, Ribeiro, GS, Wunder, EA Jr., Felzemburgh, RDM, Reis, RB, Nery, N, Santana, FS, Fraga, D, dos Santos, BL, Santos, AC, Queiroz, A, Tassinari, W, Carvalho, MS, Reis, MG, Diggle, PJ and Ko, AI (2016) Spatiotemporal determinants of urban leptospirosis transmission: four-year prospective Cohort study of slum residents in Brazil. PLoS Neglected Tropical Diseases 10, e0004275.Google Scholar
Hancke, D, Navone, GT and Suarez, OV (2011) Endoparasite community of Rattus norvegicus captured in a shantytown of Buenos Aires City. Helminthologia 48, 167–173.Google Scholar
Himsworth, CG, Jardine, CM, Parsons, KL, Feng, AYT and Patrick, DM (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
Hoffman, WA, Pons, JA and Janer, JL (1934) Sedimentation concentration method in schistosomiasis mansoni. Puerto Rico Journal of Public Health and Tropical Medicine 9, 283–298.Google Scholar
Hurvich, CM and Tsai, C-L (1989) Regression and time series model selection in small samples. Biometrika 76, 297–307.CrossRefGoogle Scholar
Instituto Brasileiro de Geografia e Estatística (IBGE) (2010) http://www.censo2010.ibge.gov.br/sinopseporsetores/?nivel=st, last accessed in the 11th of February 2017.Google Scholar
Jarret, EEE, Jarret, 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
Jarret, EEE, Jarret, WFH and Urquhart, GM (1968) Immunological unresponsiveness to Helminth parasites: I. The pattern of Nippostrongylus brasiliensis infection in young rats. Experimental Parasitology 23, 151–160.Google Scholar
Kataranovski, D, Kataranovski, M and Deljanin, I (2010) Helminth fauna of Rattus Norvegicus Berkenhout, 1769 from the Belgrade area, Serbia. Archives of Biological Sciences 62, 1091–1099.Google Scholar
Klein, SL (2000) The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience & Biobehavioral Reviews 24, 627–638.Google Scholar
Ko, AI, Reis, MG, Dourado, CMR, Johnson, WD Jr., Riley, LW, Ferrer, SR, Guerreiro, H, Salgado, K, Pereira, MM, Velloso, LF, Carvalho, CC, de Codes, LMG, Orrico, GS, Tavares-Neto, J, Pereira, MM and Lee, S (1999) Urban epidemic of severe leptospirosis in Brazil. The Lancet 354, 820–825.Google Scholar
Kunwar, CB, Subba, B, Shrestha, M, Chapagain, RH, Jha, B, Subedi, J, Blangero, J, Williams Blangero, S and Towne, B (2005) A human case of Hymenolepis diminuta infection in Nepal. Journal of Institute of Medicine 27, 66–67.Google Scholar
Lescano, SZ, Queiroz, ML and Chieffi, PP (2004) Larval recovery of Toxocara canis in organs and tissues of experimentally infected Rattus norvegicus. Memórias do Instituto Oswaldo Cruz 99, 627–628.CrossRefGoogle ScholarPubMed
Levecke, B, Behnke, JM, Ajjampur, SSR, Albonico, M, Ame, SM, Charlier, J, Geiger, SM, Hoa, NTV, Kamwa Ngassam, RI, Kotze, AC, McCarthy, JS, Montresor, A, Periago, MV, Roy, S, Tchuem Tchuenté, L-A, Thach, DTC and Vercruysse, J (2011) A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5, e1201.Google Scholar
Long, JL (2003) Introduced Mammals of the World. Collingwood, Victoria, AU: CSIRO Publishing and Wallingford, UK: CABI Publishing.Google Scholar
Lo Re, V III and Gluckman, SJ (2003) Eosinophilic meningitis. American Journal of Medicine 114, 217–223.Google Scholar
Lynsdale, CL, Franco dos Santos, DJ, Hayward, AD, Mar, KU, Htut, W, Aung, HH, Soe, AT and Lummaa, V (2015) A standardised faecal collection protocol for intestinal helminth egg counts in Asian elephants, Elephas maximus. International Journal for Parasitology: Parasites and Wildlife 4, 307–315.Google Scholar
Martins, AV and Pessôa, SB (1977) Pessôa Parasitologia Médica, 10th edn. Rio de Janeiro, BR: Editora Guanabara-Koogan.Google Scholar
McGarry, JW, Higgins, A, White, NG, Pounder, KC and Hetzel, U (2015) Zoonotic helminths of urban brown rats (Rattus norvegicus) in the UK: neglected public health considerations? Zoonoses and Public Health 62, 44–52.Google Scholar
Mercer, JG, Mitchell, PI, Moar, KM, Bissett, A, Geissler, S, Bruce, K and Chappell, LH (2000) Anorexia in rats infected with the nematode, Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120, 641–647.Google Scholar
Mills, JN, Childs, JE, Ksiazek, TG, Peters, CJ and Velleca, WM (1995) Methods for trapping and sampling small mammals for virologic testing. U.S. Department of Health & Human Services, Edn. Atlanta, USA, 61p.Google Scholar
Mirdha, BR and Samantray, JC (2002) Hymenolepis nana: a common cause of paediatric diarrhoea in Urban Slum Dwellers in India. Journal of Tropical Pediatrics 48, 331–334.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, 1–23.CrossRefGoogle ScholarPubMed
Morassutti, AL, Thiengo, SC, Fernandez, M, Sawanyawisuth, K and Graeff-Teixeira, C (2014) Eosinophilic meningitis caused by Angiostrongylus cantonensis: an emergent disease in Brazil. Memórias do Instituto Oswaldo Cruz 109, 399–407.Google Scholar
Moreira, VLC, Giese, EG, Melo, FTV, Simões, RO, Thiengo, SC, Maldonado, A Jr. and Santos, JN (2013) Endemic angiostrongyliasis in the Brazilian Amazon: Natural parasitism of Angiostrongylus cantonensis in Rattus rattus and R. norvegicus, and sympatric giant African land snails. Achatina fulica, Acta Tropica 125, 90–97.Google Scholar
Nursyazana, MT, Mohdzain, SN and Jeffery, J (2013) Biodiversity and macroparasitic distribution of the wild rat population of Carey Island, Klang. Tropical Biomedicine 30, 199–210.Google Scholar
Ooi, GL and Phua, KH (2007) Urbanization and slum formation. Journal of Urban Health 84, i27–i34.Google Scholar
Panti-May, JA, Carvalho-Pereira, TSA, Serrano, S, Pedra, GG, Taylor, J, Pertile, AC, Minter, A, Airam, V, Carvalho, M, Júnior, NN, Rodrigues, G, Reis, MG, Ko, AI, Childs, JE, Begon, M and Costa, F (2016) A two-year ecological study of Norway rats (Rattus norvegicus) in a Brazilian Urban Slum. PLoS ONE 11, e0152511.Google Scholar
Patamia, I, Cappello, E, Castellano-Chiodo, D, Greco, F, Nigro, L and Cacopardo, B (2010) A human case of Hymenolepis diminuta in a child from Eastern Sicily. The Korean Journal of Parasitology 48, 167–169.Google Scholar
Peig, J and Green, AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883–1891.Google Scholar
Pinto, HA, Mati, VLT and Melo, AL (2014) Toxocara cati (Nematoda: Ascarididae) in Didelphis albiventris (Marsupialia: Didelphidae) from Brazil: a case of pseudoparasitism. Revista Brasileira de Parasitologia Veterinária 23, 522–525.Google Scholar
Puckett, EE, Park, J, Combs, M, Blum, MJ, Bryant, JE, Caccone, A, Costa, F, Deinum, EE, Esther, A, Himsworth, CG, Keightley, PD, Ko, A, Lundkvist, A, McElhinney, LM, Morand, S, Robins, J, Russell, J, Strand, TM, Suarez, O, Yon, L and Munshi-South, J (2016) Global population divergence and admixture of the brown rat (Rattus norvegicus) Proceedings of the Royal Society of London B 283, 20161762.Google Scholar
Rafique, A, Rana, SA, Khan, HA and Sohail, A (2009) Prevalence of some helminths in rodents captured from different city structures including poultry farms and human population of Faisalabad, Pakistan. Pakistan Veterinary Journal 29, 141–144.Google Scholar
R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna, AT: R Foundation for Statistical Computing. http://www.R-project.org. ISBN 3-900051-07-0. Last accessed in the 20th of May 2013.Google Scholar
Reis, RB, Ribeiro, GS, Felzemburgh, RDM, Santana, FS, Mohr, S, Melendez, AXTO, Queiroz, A, Santos, AC, Ravines, RR, Tassinari, WS, Carvalho, MS, Reis, MG and Ko, AI (2008) Impact of environment and social gradient on Leptospira infection in urban slums. PLoS Neglected Tropical Diseases 2, e228.Google Scholar
Riley, LW, Ko, AI, Unger, A and Reis, MG (2007) Slum health: diseases of neglected populations. BMC International Health and Human Rights 7, 1–6.CrossRefGoogle ScholarPubMed
Santos, NJ, Sousa, E, Reis, MG, Ko, AI and Costa, F (2017) Rat infestation associated with environmental deficiencies in an urban slum community with high risk of leptospirosis transmission. Cadernos de Saúde Pública 33, e00132115.Google Scholar
Santos, SV, Lescano, SZ, Castro, JM and Chieffi, PP (2009) Larval recovery of Toxocara cati in experimentally infected Rattus norvegicus and analysis of the rat as potential reservoir for this ascarid. Memórias do Instituto Oswaldo Cruz 104, 933–934.Google Scholar
Schantz, PM (1996) Tapeworms (Cestodiasis). Gastroenterology Clinics of North America 25, 637–653.Google Scholar
Schnyder, M, Maurelli, MP, Morgoglione, ME, Kohler, L, Deplazes, P, Torgerson, P, Cringoli, G and Rinaldi, L (2011) Comparison of faecal techniques including FLOTAC for copromicroscopic detection of first stage larvae of Angiostrongylus vasorum. Parasitology Research 109, 63–69.Google Scholar
Simões, RO, Luque, JL, Gentile, R, Rosa, MCS, Costa-Neto, S and Maldonado, A Jr. (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
Singleton, GR, Hinds, LA, Krebs, CJ and Spratt, DM (2003) Rats, Mice and People: Rodent Biology and Management. Australian Centre for International Agricultural Research Monograph no. 96, Canberra, AU, 564p.Google Scholar
Tena, D, Pérez Simón, M, Gimeno, C, Pérez Pomata, MT, Illescas, S, Amondarain, I, González, A, Domínguez, J and Bisquert, J (1998) Human infection with Hymenolepis diminuta: case report from Spain. Journal of Clinical Microbiology 36, 2375–2376.CrossRefGoogle ScholarPubMed
Thiengo, SC, Faraco, FA, Salgado, NC, Cowie, RH and Fernandez, MA (2007) Rapid spread of an invasive snail in South America: the giant African snail, Achatina fulica, in Brasil. Biological Invasions 9, 693–702.Google Scholar
Tiwari, S, Karuna, T and Rautaraya, B (2014) Hymenolepis diminuta infection in a child from a rural area: a rare case report. Journal of Laboratory Physicians 6, 58–59.Google Scholar
United Nations (2003) The Challenge of Slums: Global Report on Human Settlements. London: UN Human Settlements Programme and London, UK: Sterling, Earthscan Publications Ltd., 310 p.Google Scholar
United Nations (2005) Investing in Development: A Practical Plan to Achieve the Millennium Development Goals. New York, USA: UN Millennium Project.Google Scholar
United Nations (2016) Urbanization and Development: Emerging Features. UN-Habitat World Cities Report 2016, UN Human Settlements Programme, Nairobi, Kenya, 262 p.Google Scholar
Vadell, MV, Gómez Villafañe, IE and Cavia, R (2014) Are life-history strategies of Norway rats (Rattus norvegicus) and house mice (Mus musculus) dependent on environmental characteristics? Wildlife Research 41, 172–184.CrossRefGoogle Scholar
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1997) Nematóides do Brasil. Parte V: nematóides de mamíferos. Revista Brasileira de Zoologia 14, 1–452.Google Scholar
Walker, R, Carvalho-Pereira, T, Serrano, S, Pedra, G, Hacker, K, Taylor, J, Minter, A, Pertile, A, Panti-May, A, Carvalho, M, Souza, FN, Nery, N Jr., Rodrigues, G, Bahiense, T, Reis, MG, Ko, AI, Childs, JE, Begon, M and Costa, F (2017) Factors affecting carriage and intensity of infection of Calodium hepaticum within Norway rats (Rattus norvegicus) from an urban slum environment in Salvador, Brazil. Epidemiology & Infection 145, 334–338.Google Scholar
Wang, Q-P, Lai, D-H, Zhu, X-Q, Chen, X-G and Lun, Z-R (2008) Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621–630.Google Scholar
Wang, Q-P, Wu, Z-D, Wei, J, Owen, RL and Lun, Z-R (2012) Human Angiostrongylus cantonensis: an update. European Journal of Clinical Microbiology & Infectious Diseases 31, 389–395.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. Norveg icus from Jamaica. Journal of Parasitology 2, 1014–1018.Google Scholar
Webster, JP and Macdonald, DW (1995) Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 111, 247–255.Google Scholar
Wolff, JO (2003) Density-dependence and the socioecology of space use in rodents. In Singleton, GR, Hinds, LA, Krebs, CJ and Spratt, DM (eds). Rats, Mice and People: Rodent Biology and Management, pp. 124–130. Australian Centre for International Agricultural Research Monograph No. 96. Canberra, AU.Google Scholar
Zuk, M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitology Today 6, 231–233.Google Scholar
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