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Angiostrongylus cantonensis in urban populations of terrestrial gastropods and rats in an impoverished region of Brazil

Published online by Cambridge University Press:  12 April 2021

Fábio N. Souza Open the ORCID record for Fábio N. Souza [Opens in a new window] ,
Maísa Aguiar Santos Open the ORCID record for Maísa Aguiar Santos [Opens in a new window] ,
Daniele Almeida Alves Open the ORCID record for Daniele Almeida Alves [Opens in a new window] ,
Leyva Cecília Vieira de Melo ,
Dan Jessé Gonçalves da Mota ,
Arsinoê Cristina Pertile ,
Ricardo Gava ,
Pedro Luiz Silva Pinto Open the ORCID record for Pedro Luiz Silva Pinto [Opens in a new window] ,
Max T. Eyre Open the ORCID record for Max T. Eyre [Opens in a new window]  and
Caio Graco Zeppelini Open the ORCID record for Caio Graco Zeppelini [Opens in a new window]
...Show all authors
Fábio N. Souza*
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Maísa Aguiar Santos
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Daniele Almeida Alves
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Leyva Cecília Vieira de Melo
Affiliation:
Instituto Adolfo Lutz, São Paulo, Brazil
Dan Jessé Gonçalves da Mota
Affiliation:
Instituto Adolfo Lutz, São Paulo, Brazil
Arsinoê Cristina Pertile
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
Ricardo Gava
Affiliation:
Instituto Adolfo Lutz, São Paulo, Brazil
Pedro Luiz Silva Pinto
Affiliation:
Instituto Adolfo Lutz, São Paulo, Brazil
Max T. Eyre
Affiliation:
Centre for Health Informatics, Computing, and Statistics, Lancaster University Medical School, Lancaster, UK
Caio Graco Zeppelini
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil
Mitermayer G. Reis
Affiliation:
Universidade Federal da 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
Albert I. Ko
Affiliation:
Department of Epidemiology of Microbial Disease, Yale School of Public Health, New Haven, USA
Mike Begon
Affiliation:
Institute of Integrative Biology, University of Liverpool, Liverpool, UK
Thiago C. Bahiense
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil
Federico Costa
Affiliation:
Universidade Federal da 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 Institute of Integrative Biology, University of Liverpool, Liverpool, UK
Ticiana Carvalho-Pereira
Affiliation:
Universidade Federal da Bahia, UFBA, Salvador, Brazil Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Ministério da Saúde, Salvador, Brazil
*
Author for correspondence: Fábio N. Souza, E-mail: [email protected]
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Abstract

The nematode Angiostrongylus cantonensis is the most common cause of neuroangiostrongyliasis (manifested as eosinophilic meningitis) in humans. Gastropod molluscs are used as intermediate hosts and rats of various species are definitive hosts of this parasite. In this study, we identified several environmental factors associated with the presence and abundance of terrestrial gastropods in an impoverished urban region in Brazil. We also found that body condition, age and presence of co-infection with other parasite species in urban Rattus norvegicus, as well as environmental factors were associated with the probability and intensity of A. cantonensis infection. The study area was also found to have a moderate prevalence of the nematode in rodents (33% of 168 individuals). Eight species of molluscs (577 individuals) were identified, four of which were positive for A. cantonensis. Our study indicates that the environmental conditions of poor urban areas (presence of running and standing water, sewage, humidity and accumulated rain and accumulation of construction materials) influenced both the distribution and abundance of terrestrial gastropods, as well as infected rats, contributing to the maintenance of the A. cantonensis transmission cycle in the area. Besides neuroangiostrongyliasis, the presence of these hosts may also contribute to susceptibility to other zoonoses.

Keywords

Angiostrongyliasishelminthone healthpublic healthRattus norvegicusrisk factorsslugsnailzoonoses
Type
Research Article
Information
Parasitology , Volume 148 , Issue 8 , July 2021 , pp. 994 - 1002
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Anderson, RC (1978) Keys to genera of the superfamily Metastrongyloidea, CIH keys to the nematode parasites of vertebrates, No. 5. Commonwealth Agricultural Bureau, Farnham Royal, Bucks, UK.Google Scholar
Ash, LR (1970) Diagnostic morphology of the third-stage larvae of Angiostrongylus cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, and Anafilaroides rostratus (Nematoda: Metastrongyloidea). The Journal of Parasitology 56, 249–253.10.2307/3277651CrossRefGoogle Scholar
Astor, T, Proschwitz, T, Strengbom, J, Berg, MP and Bengtsson, J (2017) Importance of environmental and spatial components for species and trait composition in terrestrial snail communities. Journal of Biogeography 44, 1362–1372.10.1111/jbi.12946CrossRefGoogle Scholar
Au, ACS and Ko, RC (1979) Changes in worm burden, haematological and serological response in rats after single and multiple Angiostrongylus cantonensis infections. Zeitschrift für Parasitenkunde 58, 233–242.10.1007/BF00933930CrossRefGoogle ScholarPubMed
Barbosa, TA, Thiengo, SC, Fernandez, MA, Graeff-Teixeira, C, Morassutti, AL, Mourão, FRP, Miranda, COS, Jorge, MM, Costa, LF and Gomes, SR (2020) Infection by Angiostrongylus cantonensis in both humans and the snail Achatina (Lissachatina) fulica in the city of Macapá, in the Amazon Region of Brazil. Memorias do Instituto Oswaldo Cruz 115, e200115.10.1590/0074-02760200115CrossRefGoogle ScholarPubMed
Barratt, J, Chan, D, Sandaradura, I, Malik, R, Spielman, D, Lee, R, Marriott, D, Harkness, J, Ellis, J and Stark, D (2016) Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology 143, 1087–1118.10.1017/S0031182016000652CrossRefGoogle ScholarPubMed
Bartón, K (2013) Model selection and model averaging based on information criteria (AICc and alike). The Comprehensive R Archive Network 1, 13.Google Scholar
Breure, ASH and Ablett, JD (2014) Annotated type catalogue of the Bulimulidae (Mollusca, Gastropoda, Orthalicoidea) in the Natural History Museum, London. ZooKeys 392, 1–367. doi: 10.3897/zookeys.392.6328CrossRefGoogle Scholar
Caldeira, RL, Carvalho, OS, Mendonça, CL, Graeff-Teixeira, C, Silva, MCF, Ben, R, Maurer, R, Lima, WS and Lenzi, HL (2003) Molecular differentiation of Angiostrongylus costaricensis, A. cantonensis, and A. vasorum by polymerase chain reaction-restriction fragment length polymorphism. Memorias do Instituto Oswaldo Cruz 98, 1039–1043.10.1590/S0074-02762003000800011CrossRefGoogle Scholar
Caldeira, RL, Mendonça, CL, Goveia, CO, Lenzi, HL, Graeff-Teixeira, C, Lima, WS, Mota, EM, Pecora, IL, de Medeiros, AMZ and Carvalho, OS (2007) First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Memorias do Instituto Oswaldo Cruz 102, 887–889.CrossRefGoogle ScholarPubMed
Carvalho-Pereira, T, Souza, FN, Santos, LRN, Walker, R, Pertile, AC, de Oliveira, DS, Pedra, GG, Minter, A, Rodrigues, MG, Bahiense, TC, Reis, MG, Diggle, PJ, Ko, AI, Childs, JE, da Silva, EM, Begon, M and Costa, F (2018) The helminth community of a population of Rattus norvegicus from an urban Brazilian slum and the threat of zoonotic diseases. Parasitology 145, 797–806.10.1017/S0031182017001755CrossRefGoogle ScholarPubMed
Carvalho-Pereira, TSA, Souza, FN, Santos, LRN, Pedra, GG, Minter, A, Bahiense, TC, Reis, MG, Ko, AI, Childs, JE, Silva, EM, Costa, F and Begon, M (2019) Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum. Ecosphere (Washington, D.C.) 10(10), 1–14. doi: 10.1002/ecs2.2887Google Scholar
Carvalho, ODS, Scholte, RGC, de Mendonça, CLF, Passos, LKJ and Caldeira, RL (2012) Angiostrongylus cantonensis (Nematode: Metastrongyloidea) in molluscs from harbour areas in Brazil. Memorias do Instituto Oswaldo Cruz 107, 740–746.10.1590/S0074-02762012000600006CrossRefGoogle Scholar
Castillo, DSC and Paller, VGV (2018) Occurrence of Angiostrongylus cantonensis in rodents from the rice granary of the Philippines and associated risk factors for zoonotic transmission. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology 42, 350–356.10.1007/s12639-018-1005-zCrossRefGoogle ScholarPubMed
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, 11–19.10.1016/j.landurbplan.2008.10.017CrossRefGoogle Scholar
Červená, B, Modrý, D, Fecková, B, Hrazdilová, K, Foronda, P, Alonso, AM, Lee, R, Walker, J, Niebuhr, CN and Malik, R (2019) Low diversity of Angiostrongylus cantonensis complete mitochondrial DNA sequences from Australia, Hawaii, French Polynesia and the Canary Islands revealed using whole genome next-generation sequencing. Parasites & Vectors 12, 241.10.1186/s13071-019-3491-yCrossRefGoogle ScholarPubMed
Climate-Data.org. Salvador: Temperatura, Tempo e Dados climatológicos Salvador. Temperatura da água Salvador. Available at https://pt.climate-data.org/america-do-sul/brasil/bahia/salvador-854/ (Accessed 19 June 2020).Google Scholar
Colley, E (2012) Moluscos terrestres e a malacologia paranaense: histórico e importância no cenário nacional. Estudos de Biologia 34, 1–34. doi: 10.7213/estud.biol.6127CrossRefGoogle Scholar
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) 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, 33–40.10.1089/vbz.2013.1378CrossRefGoogle ScholarPubMed
Cowie, RH (2013) Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai'i Journal of Medicine & Public Health, 72(6 suppl. 2), 6.Google ScholarPubMed
Dias, RJP, Bessa, ECA and D’Ávila, S (2007) Influence of substrate humidity on desiccation resistance capacity in Subulina octona (Mollusca, Subulinidae). Brazilian Archives of Biology and Technology 50, 137–139.10.1590/S1516-89132007000100016CrossRefGoogle Scholar
Faust, EC, D'Antoni, JS, Odom, V, Miller, MJ, Peres, C, Sawitz, W, Thomen, LF, Tobie, J and Walker, HJ (1938) A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces. The American Journal of Tropical Medicine and Hygiene s1–18, 169–183.10.4269/ajtmh.1938.s1-18.169CrossRefGoogle Scholar
Feng, AYT and Himsworth, CG (2014) The secret life of the city rat: a review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus). Urban Ecosystems 17, 149–162.10.1007/s11252-013-0305-4CrossRefGoogle Scholar
Gordon, HM and Whitlock, HV (1939) A new technique for counting nematode eggs in sheep faeces. Journal of the Council for Scientific and Industrial Research 12, 50–52.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, e0004275.10.1371/journal.pntd.0004275CrossRefGoogle ScholarPubMed
Hoffman, WA, Pons, JA and Janer, JL (1934) The sedimentation-concentration method in Schistosomiasis mansoni. Puerto Rico Journal of Public Health and Tropical Medicine 9, 283–298.Google Scholar
Hylander, K, Nilsson, C, Jonsson, GB and Göthner, T (2005) Differences in habitat quality explain nestedness in a land snail meta-community. Oikos 108, 351–361.10.1111/j.0030-1299.2005.13400.xCrossRefGoogle Scholar
Kikuti, M, Cunha, GM, Paploski, IAD, Kasper, AM, Silva, MMO, Tavares, AS, Cruz, JS, Queiroz, TL, Rodrigues, MS, Santana, PM, Lima, HCAV, Calcagno, J, Takahashi, D, Gonçalves, AHO, Araújo, JMG, Gauthier, K, Diuk-Wasser, MA, Kitron, U, Ko, AI, Reis, MG and Ribeiro, GS (2015) Spatial distribution of dengue in a Brazilian urban slum setting: role of socioeconomic gradient in disease risk. PLoS Neglected Tropical Diseases 9, e0003937.10.1371/journal.pntd.0003937CrossRefGoogle Scholar
Kim, JR, Hayes, KA, Yeung, NW and Cowie, RH (2014) Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS ONE 9, e94969.10.1371/journal.pone.0094969CrossRefGoogle ScholarPubMed
Loeys, T, Moerkerke, B, De Smet, O and Buysse, A (2012) The analysis of zero-inflated count data: beyond zero-inflated Poisson regression. The British Journal of Mathematical and Statistical Psychology 65, 163–180.CrossRefGoogle ScholarPubMed
Masi, E, Pino, FA, Santos, MGS, Genehr, L, Albuquerque, JOM, Bancher, AM and Alves, JCM (2010) Socioeconomic and environmental risk factors for urban rodent infestation in Sao Paulo, Brazil. Journal of Pest Science 83, 231–241.10.1007/s10340-010-0290-9CrossRefGoogle Scholar
Ministério da Saúde (2008) Vigilância e Controle de Moluscos de Importância Epidemiológica: Diretrizes Técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE). Ministério da Saúde-Brasil.Google Scholar
Miranda, MS, Fontenelle, JH and Pecora, IL (2015) Population structure of a native and an alien species of snail in an urban area of the Atlantic Rainforest. Journal of Natural History 49, 19–35.10.1080/00222933.2014.930756CrossRefGoogle Scholar
Morassutti, AL, Thiengo, SC, Fernandez, M, Sawanyawisuth, K and Graeff-Teixeira, C (2014) Eosinophilic meningitis caused by Angiostrongylus cantonensis: an emergent disease in Brazil. Memorias do Instituto Oswaldo Cruz 109, 399–407.10.1590/0074-0276140023CrossRefGoogle ScholarPubMed
Moreira, VLC, Giese, EG, Melo, FTV, Simões, RO, Thiengo, SC, Maldonado, A and Santos, JN (2013) Endemic angiostrongyliasis in the Brazilian Amazon: Natural parasitism of Angiostrongylus cantonensis in Rattus rattus and Rattus norvegicus, and sympatric giant African land snails, Achatina fulica. Acta Tropica 125, 90–97.10.1016/j.actatropica.2012.10.001CrossRefGoogle ScholarPubMed
Nunes, GKM and Santos, SB (2012) Environmental factors affecting the distribution of land snails in the Atlantic Rain Forest of Ilha Grande, Angra dos Reis, RJ, Brazil. Brazilian Journal of Biology 72, 79–86.CrossRefGoogle Scholar
Oliveira, AP, Gentile, R, Maldonado Júnior, A, Lopes Torres, EJ and Thiengo, SC (2015) Angiostrongylus cantonensis infection in molluscs in the municipality of São Gonçalo, a metropolitan area of Rio de Janeiro, Brazil: role of the invasive species Achatina fulica in parasite transmission dynamics. Memorias do Instituto Oswaldo Cruz 110, 739–744.CrossRefGoogle Scholar
Onyishi, GC, Aguzie, IO, Okoro, JO, Nwani, CD, Ezenwaji, N, Oluah, NS and Okafor, FC (2018) Terrestrial snail fauna and associated helminth parasites in a tropical semi-urban zone, Enugu State, Nigeria. Pakistan Journal of Zoology 50, 1080–1085.10.17582/journal.pjz/2018.50.3.1079.1085CrossRefGoogle 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.CrossRefGoogle 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, 1883–1891.10.1111/j.1600-0706.2009.17643.xCrossRefGoogle Scholar
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.Google Scholar
Rugai, E, Mattos, T and Brisola, AP (1954) Nova técnica para isolar larvas de nematóides das fezes-modificação do método de Baermann. Revista do Instituto Adolfo Lutz 14, 5–8.Google Scholar
Salgado, NC and dos Santos Coelho, AC (2003) Moluscos terrestres do Brasil (Gastrópodes operculados ou não, exclusive Veronicellidae, Milacidae e Limacidae). Revista de Biología Tropical 51, 149–189.Google Scholar
Simões, RO, Júnior, A, Olifiers, N, Garcia, JS, Bertolino, AVFA and Luque, JL (2014) A longitudinal study of Angiostrongylus cantonensis in an urban population of Rattus norvegicus in Brazil: the influences of seasonality and host features on the pattern of infection. Parasites & Vectors 7, 100.10.1186/1756-3305-7-100CrossRefGoogle Scholar
Simone, LRL (2006) Land and Freshwater Molluscs of Brazil: An Illustrated Inventory on the Brazilian Malacofauna, Including Neighbor Regions of the South America, Respect to the Terrestrial and Freshwater Ecosystems. Museu de Zoologia, Universidade de São Paulo.Google Scholar
Sólymos, P, Farkas, R, Kemencei, Z, Páll-Gergely, B, Vilisics, F, Nagy, A, Kisfali, M and Hornung, E (2009) Micro-habitat scale survey of land snails in dolines of the Alsó-hegy, Aggtelek National Park, Hungary. Mollusca 27, 167–171.Google Scholar
Spickett, A, Junker, K, Krasnov, BR, Haukisalmi, V and Matthee, S (2017) Helminth parasitism in two closely related South African rodents: abundance, prevalence, species richness and impinging factors. Parasitology Research 116, 1395–1409.10.1007/s00436-017-5419-9CrossRefGoogle ScholarPubMed
Thiengo, SC, Maldonado, A, Mota, EM, Torres, EJL, Caldeira, R, Carvalho, OS, Oliveira, APM, Simões, RO, Fernandez, MA and Lanfredi, RM (2010) The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernambuco, northeast Brazil. Acta Tropica 115, 194–199.CrossRefGoogle Scholar
Thiengo, SC, de Oliveira Simões, R, Fernandez, MA and Júnior, AM (2013) Angiostrongylus cantonensis and rat lungworm disease in Brazil. Hawai'i Journal of Medicine & Public Health 72(6 suppl. 2), 18.Google ScholarPubMed
Valente, R, Robles, MDR, Navone, GT and Diaz, JI (2018) Angiostrongylus spp. in the Americas: geographical and chronological distribution of definitive hosts versus disease reports. Memorias do Instituto Oswaldo Cruz 113, 143–152.CrossRefGoogle ScholarPubMed
Vicente, JJ, Rodrigues, HDO, Gomes, DC and Pinto, RM (1997) Nematóides do Brasil. Parte V: nematóides de mamíferos. Revista Brasileira de Zoologia 14, 1–452.CrossRefGoogle Scholar
Wallace, GD and Rosen, L (1969) Techniques for recovering and identifying larvae of Angiostrongylus cantonensis from molluscs. Malacologia 7, 427–438.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.CrossRefGoogle ScholarPubMed
Zuur, AF and Ieno, EN (2016) Beginner's Guide to Zero-Inflated Models with R. United Kingdom: Highland Statistics Limited.Google Scholar
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