Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T02:05:44.104Z Has data issue: false hasContentIssue false
  • English
  • Français

The invasive giant African land snail, Achatina fulica (Gastropoda: Pulmonata): global geographical distribution of this species as host of nematodes of medical and veterinary importance

Published online by Cambridge University Press:  01 December 2022

G. M. Silva Open the ORCID record for G. M. Silva [Opens in a new window] ,
S. C. Thiengo Open the ORCID record for S. C. Thiengo [Opens in a new window] ,
V. L. Sierpe Jeraldo Open the ORCID record for V. L. Sierpe Jeraldo [Opens in a new window] ,
M. I. F. Rego Open the ORCID record for M. I. F. Rego [Opens in a new window] ,
A. B. P. Silva Open the ORCID record for A. B. P. Silva [Opens in a new window] ,
P. S. Rodrigues Open the ORCID record for P. S. Rodrigues [Opens in a new window]  and
S. R. Gomes Open the ORCID record for S. R. Gomes [Opens in a new window]
G. M. Silva
Affiliation:
Tiradentes University – UNIT, Graduate Program in Health and the Environment, Avenida Murilo Dantas, 300, Bairro Farolândia, 49032-490 Aracaju, SE, Brazil National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
S. C. Thiengo*
Affiliation:
National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
V. L. Sierpe Jeraldo
Affiliation:
Tiradentes University – UNIT, Graduate Program in Health and the Environment, Avenida Murilo Dantas, 300, Bairro Farolândia, 49032-490 Aracaju, SE, Brazil Laboratory of Infecious and Parasitic Diseases, Institute for Technology and Research – ITP, Avenida Murilo Dantas, 300, Prédio do ITP, Bairro Farolândia, 49032-490 Aracaju, SE, Brazil
M. I. F. Rego
Affiliation:
National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
A. B. P. Silva
Affiliation:
National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
P. S. Rodrigues
Affiliation:
National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
S. R. Gomes
Affiliation:
National Reference Laboratory for Schistosomiasis-Malacology: Oswaldo Cruz Institute – FIOCRUZ, Avenida Brazil 4365, Manguinhos, Rio de Janeiro 21.040-900, RJ, Brazil
*
Author for correspondence: S.C. Thiengo, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The giant African land snail, Achatina fulica, is an important invasive species in many countries, where it causes losses in biodiversity and agriculture, as well as impacting the health of both humans and animals, as the intermediate host of medically important nematodes. The present study is based on a comprehensive review of the literature on the nematodes that have been found in association with A. fulica, worldwide. We searched a number of different databases and used the findings to investigate the methods used to extract and identify the nematodes, their larval stages, and environment and collecting procedures of the infected molluscs. Between 1965 and 2021, 11 nematode species were recorded in association with A. fulica in 21 countries. Most of the studies recorded associations between A. fulica and Angiostrongylus cantonensis, which causes cerebral angiostrongyliasis in humans and Aelurostrongylus abstrusus, which provokes pneumonia in felines. The nematodes were extracted primarily by artificial digestion with hydrochloric acid or pepsin, and identified based on their morphology or through experimental infection to obtain the adult. In most cases, the nematodes were at larval stage L3, and the infected A. fulica were collected from anthropogenic environments. The results demonstrate the importance of A. fulica as a host of nematodes of medical and veterinary importance, as well the contribution of anthropogenic environments to the occurrence of the parasites, and give information about the different methods used to collect and identify the nematodes found associated with this species.

Keywords

Achatina fulicaLissachatinanematodesparasiteszoonoses
Type
Review Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e86
Copyright
Copyright © The Author(s), 2022. 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

Alicata, JE (1966) The presence of Angiostrongylus cantonensis in islands of the Indian Ocean and probable role of the giant African snail, Achatina fulica, in dispersal of the parasite to the Pacific islands. Canadian Journal of Zoology 44(6), 1041–1049.CrossRefGoogle ScholarPubMed
Almeida, MN, Pereira, TM and Lima, LHC (2016) Comportamento de Achatina fulica (Bowdich, 1822) (Mollusca, Achatinidae) em ambiente urbano [Behaviour of Achatina fulica (Bowdich, 1822) (Mollusca, Achatinidae) in an urban environment]. Revista Biociências 22(2), 1–17. [In Portuguese.]Google Scholar
Amaya, I, Fajardo, M, Morel, C, Blanco, Y and Devera, R (2014) Enteroparasites of medical interest in specimens of Achatina fulica captured in Ciudad Bolívar, Bolívar State, Venezuela. VITAE Academia Biomédica Digital 57(1), 1–13.Google Scholar
Anderson, RC (2000) Nematode parasites of vertebrates: their development and transmission. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Andrade-Porto, SMD, Souza, KCPD, Cárdenas, MQ, Roque, RA, Pimpão, DM, Araújo, CS and Malta, JCDO (2012) Occurrence of Aelurostrongylus abstrusus (Railliet, 1898) larvae (Nematoda: Metastrongylidae) infecting Achatina (Lissachatina) fulica Bowdich, 1822 (Mollusca: Gastropoda) in the Amazon region. Acta Amazonica 42(2), 245–250.CrossRefGoogle Scholar
Arruda, JO and Santos, L (2022) First record of Achatina fulica Bowdich, 1822 (Mollusca, Achatinidae), for the state of Rio Grande do Sul, Brazil. Biotemas 35(1), 1–6.CrossRefGoogle Scholar
Barbosa, TA, Thiengo, SC, Fernandez, MA, et al. (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. Memórias do Instituto Oswaldo Cruz 115(1), e200115.CrossRefGoogle ScholarPubMed
Beaver, PC and Rosen, L (1964) Memorandum on the first report of Angiostrongylus in Man, by Nomura and Lin, 1945. American Journal of Tropical Medicine and Hygiene 13(4), 589–590.CrossRefGoogle Scholar
Bechara, AH, Simões, RO, Faro, MJ and Garcia, JS (2018) Achatina fulica infected by Angiostrongylus cantonensis on beaches, in the west zone of Rio de Janeiro, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 60(1), e4.CrossRefGoogle ScholarPubMed
Bhaibulaya, M (1979) Morphology and taxonomy of major Angiostrongylus species of Eastern Asia and Australia. pp. 4–13. In Cross JH (Ed.) Studies on Angiostrongylus in Eastern Asia and Australia, vol. 2. Taipei, Taiwan, US Naval Medical Research Unit.Google Scholar
Bisseru, B (1971) The prevalence of Angiostrongylus cantonensis larvae collected from the giant African snail, Achatina fulica in west Malaysia and Singapore. Southeast Asian Journal of Tropical Medicine and Public Health 2(4), 523–526.Google ScholarPubMed
Caldeira, RL, Mendonça, CL, Goveia, CO, et al. (2007) First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Memórias do Instituto Oswaldo Cruz 102(7), 887–889.CrossRefGoogle ScholarPubMed
Carvalho, ODS, Scholte, RGC, Mendonça, CLFD, Passos, LKJ and Caldeira, RL (2012) Angiostrongylus cantonensis (Nematode: Metastrongyloidea) in molluscs from harbour areas in Brazil. Memórias do Instituto Oswaldo Cruz 107(6), 740–746.CrossRefGoogle ScholarPubMed
Civeyrel, L and Simberloff, D (1996) A tale of two snails: is the cure worse than the disease? Biodiversity & Conservation 5(10), 1231–1252.CrossRefGoogle Scholar
Coaglio, AL, Mozzer, LR, Corrêa, DN, de Jesus Pereira, CA and dos Santos Lima, W (2016) Evaluation of techniques for recovery of Angiostrongylus vasorum from Achatina fulica, a potential intermediate host. Journal of Tropical Pathology 45(1), 87–97.Google Scholar
Constantino-Santos, DMA, Basiao, ZU, Wade, CM, Santos, BS and Fontanilla, IKC (2014a) Identification of Angiostrongylus cantonensis and other nematodes using the SSU rDNA in Achatina fulica populations of Metro Manila. Tropical Biomedicine 31(2), 327–335.Google ScholarPubMed
Constantino-Santos, DMA, Santos, BS, Soriano, JME, Dy, JSH and Fontanilla, IKC (2014b) Philippine survey of nematode parasite infection and load in the giant African snail Achatina fulica indicate Angiostrongylus cantonensis infection in Mindanao. Science Diliman 26(2), 72–84.Google Scholar
Córdoba-R, D, Patiño-Montoya A, and Giraldo, A (2017) Prevalence of Strongylida nematodes associated with African snail, Achatina fulica, in Valle del Cauca, Colombia. Revista MVZ Córdoba 22(3), 6276–6286.CrossRefGoogle Scholar
Cuasapaz-Sarabia, J (2016) Endoparásitos de Achatina fulica Bowdich, 1822 (Gastropoda: Achatinidae), en el recinto Mata de Cacao, cantón Babahoyo, Provincia de Los Ríos, Ecuador [Endoparasites of Achatina fulica Bowdich, 1822 (Gastropoda: Achatinidae), in the Mata de Cacao enclosure, Babahoyo canton, Los Ríos Province, Ecuador]. Revista Científica Ciencias Naturales y Ambientales 10(1), 12–18. [In Spanish.]Google Scholar
Cunha, MCR (2017) Meningite eosinofílica: Relato de caso [Eosinophilic meningitis: a case report]. Revista Brasileira de Análises Clínicas 49(2), 213–215. [In Portuguese.]Google Scholar
Dard, C, Piloquet, JE, Qvarnstrom, Y, Fox, LM, M'kada, H, Hebert, JC, Mattera, D and Harrois, D (2017) First evidence of angiostrongyliasis caused by Angiostrongylus cantonensis in Guadeloupe, Lesser Antilles. The American Journal of Tropical Medicine and Hygiene 96(3), 692–697.Google Scholar
Darrigran, G, Agudo-Padrón, I, Baez, P, et al. (2020) Non-native mollusks throughout South America: emergent patterns in an understudied continent. Biological Invasions 22(3), 853–871.CrossRefGoogle Scholar
Deng, ZH, Zhang, QM, Huang, SY and Jones, JL (2012) First provincial survey of Angiostrongylus cantonensis in Guangdong Province, China. Tropical Medicine & International Health 17(1), 119–122.CrossRefGoogle ScholarPubMed
Dickens, KL, Capinera, JL and Smith, TR (2018) Effects of density and food deprivation on growth, reproduction, and survival of Lissachatina fulica. American Malacological Bulletin 36(1), 57–61.CrossRefGoogle Scholar
d'Ovidio, D, Nermut, J, Adami, C and Santoro, M (2019) Occurrence of rhabditid nematodes in the pet giant African land snails (Achatina fulica). Frontiers in Veterinary Science 6(1), 88.CrossRefGoogle ScholarPubMed
Dumidae, A, Janthu, P, Subkrasae, C, Dekumyoy, P, Thanwisai, A and Vitta, A (2019) Genetic characterization of Angiostrongylus larvae and their intermediate host, Achatina fulica, in Thailand. PLoS One 14(9), e0223257.CrossRefGoogle ScholarPubMed
Epelboin, L, Blondé, R, Chamouine, A, et al. (2016) Angiostrongylus cantonensis infection on Mayotte Island, Indian Ocean, 2007–2012. PLoS Neglected Tropical Diseases 10(5), e0004635.CrossRefGoogle ScholarPubMed
Espírito-Santo, MCCD, Pinto, PLS, Mota, DJGD and Gryschek, RCB (2013) The first case of Angiostrongylus cantonensis eosinophilic meningitis diagnosed in the city of São Paulo, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 55(2), 129–132.CrossRefGoogle ScholarPubMed
Eston, MRD, Menezes, GV, Antunes, AZ, Santos, ASRD and Santos, AMRD (2006) Espécie invasora em unidade de conservação: Achatina fulica (Bowdich, 1822) no Parque Estadual Carlos Botelho Sete Barras, SP, Brasil [Invasive species in a conservation unit: Achatina fulica (Bowdich, 1822) in Carlos Botelho Sete Barras State Park, SP, Brazil]. Revista do Instituto Florestal 18(1), 173–179. [In Portuguese.]Google Scholar
Ferreira, LF, Chieffi, PP and Araujo, A (2012) Parasitismo não é doença parasitária [Parasitism is not a parasitic disease]. Norte Ciência 3(1), 200–221. [In Portuguese.]Google Scholar
Fischer, ML and Colley, E (2005) Espécie invasora em reservas naturais: caracterização da população de Achatina fulica Bowdich, 1822 (Mollusca–Achatinidae) na Ilha Rasa, Guaraqueçaba, Paraná, Brasil [Invasive species in natural reserves: characterization of the population of Achatina fulica Bowdich, 1822 (Mollusca–Achatinidae) on Ilha Rasa, Guaraqueçaba, Paraná, Brazil]. Biota Neotropica 5(1), 127–144. [In Portuguese.]CrossRefGoogle Scholar
Fischer, ML and Costa, LCM (2010) O caramujo gigante africano Achatina fulica no Brasil [The giant African snail Achatina fulica in Brazil]. Curitiba, Champagnat. [In Portuguese.]Google Scholar
Fontanilla, IKC and Wade, C (2012) Research Note: First report of Angiostrongylus cantonensis in the giant African land snail Achatina fulica in French Polynesia detected using the SSU rRNA gene. Tropical Biomedicine 29, 642–645.Google Scholar
Fontanilla, IKC, Sta Maria, IMP, Garcia, JRM, Ghate, H, Naggs, F and Wade, CM (2014) Restricted genetic variation in populations of Achatina (Lissachatina) fulica outside of East Africa and the Indian Ocean Islands points to the Indian Ocean Islands as the earliest known common source. PLoS One 9(9), e105151.CrossRefGoogle Scholar
Franco-Acuña, DO, Pinheiro, J, Torres, EJL, Lanfredi, RM and Brandolini, SVPB (2009) Nematode cysts and larvae found in Achatina fulica Bowdich, 1822. Journal of Invertebrate Pathology 100(2), 106–110.CrossRefGoogle ScholarPubMed
Giraldo, A, Garzón, C, Castillo, A and Córdoba-Rojas, DF (2019) Confirmation of the presence of Angiostrongylus cantonensis in lung tissue of the African giant snail (Lissachatina fulica) in Colombia. Infectio 23(2), 129–132.CrossRefGoogle Scholar
Graeff-Teixeira, C and Morera, P (1995) Método de digestão de moluscos em ácido clorídrico para isolamento de larvas de metastrongilídeos [Hydrochloric acid digestion of molluscs for isolation of metastrongylid larvae]. Biociências 3(1), 85–89. [In Portuguese.]Google Scholar
Graeff-Teixeira, C, da Silva, ACA and Yoshimura, K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22(2), 322–348.CrossRefGoogle ScholarPubMed
Grewal, PS, Grewal, SK, Tan, L and Adams, B (2003) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 35(2), 146–156.Google ScholarPubMed
Guerino, LR, Pecora, IL, Miranda, MS, Aguiar-Silva, C, Carvalho, ODS, Caldeira, RL and Silva, RJD (2017) Prevalence and distribution of Angiostrongylus cantonensis (Nematoda, Angiostrongylidae) in Achatina fulica (Mollusca, Gastropoda) in Baixada Santista, São Paulo, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 50(1), 92–98.CrossRefGoogle ScholarPubMed
Guerrero, R, Rincon-Orozco, B and Delgado, NU (2018) Achatina fulica (Mollusca: Achatinidae) Naturally Infected with Caenorhabditis briggsae (Dougherty and Nigon, 1949) (Nematoda: Rhabditidae). Journal of Parasitology 104(6), 679–684.CrossRefGoogle ScholarPubMed
Hicklenton, L and Betson, M (2019) Molecular detection of Angiostrongylus vasorum in gastropods in Surrey, UK. Parasitology Research 118(3), 1051–1054.CrossRefGoogle ScholarPubMed
Hu, X, Du, J, Tong, C, Wang, S, Liu, J, Li, Y and He, C (2011) Epidemic status of Angiostrongylus cantonensis in Hainan island, China. Asian Pacific Journal of Tropical Medicine 4(4), 275–277.CrossRefGoogle ScholarPubMed
Igbinosa, IB, Isaac, C, Adamu, HO and Adeleke, G (2016) Parasites of edible land snails in Edo State, Nigeria. Helminthologia 53(4), 331–335.CrossRefGoogle Scholar
Iwanowicz, DD, Sanders, LR, Schill, WB, Xayavong, MV, da Silva, AJ, Qvarnstrom, Y and Smith, T (2015) Spread of the rat lungworm (Angiostrongylus cantonensis) in giant African land snails (Lissachatina fulica) in Florida, USA. Journal of Wildlife Diseases 51(3), 749–753.CrossRefGoogle Scholar
Jakkul, W, Chaisiri, K, Saralamba, N, Limpanont, Y, Dusitsittipon, S, Charoennitiwat, V, Chan, AHE and Thaenkham, U (2021) Newly developed SYBR Green-based quantitative real-time PCRs revealed coinfection evidence of Angiostrongylus cantonensis and A. malaysiensis in Achatina fulica existing in Bangkok Metropolitan, Thailand. Food and Waterborne Parasitology 23(1), e00119. doi:10.1016/j.fawpar.2021.e00119CrossRefGoogle 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(5), e94969.CrossRefGoogle ScholarPubMed
Kwon, E, Ferguson, TM, Park, SY, Manuzak, A, Qvarnstrom, Y, Morgan, S, Ciminera, P and Murphy, GS (2013) A severe case of Angiostrongylus eosinophilic meningitis with encephalitis and neurologic sequelae in Hawai ‘i. Hawai'i Journal of Medicine & Public Health 72(6), 41–45.Google Scholar
Lange, MK, Penagos-Tabares, F, Vélez, J, Gutiérrez, J, Hirzmann, J, Chaparro-Gutiérrez, JJ, Piedrahita, D, Taubert, A and Hermosilla, C (2018) Regional report on Angiostrongylus vasorum in Colombia: genetic similarity to European lineage. Veterinary Parasitology: Regional Studies and Reports 13(1), 21–23.Google ScholarPubMed
Lerner, H and Berg, C (2015) The concept of health in one health and some practical implications for research and education: what is one health? Infection Ecology & Epidemiology 5(1), 1–7.CrossRefGoogle ScholarPubMed
Lim, BL and Heyneman, D (1965) Host–parasite studies of Angiostrongylus cantonensis (Nematoda, Metastrongylidae) in Malaysian rodents: natural infection of rodents and molluscs in urban and rural areas of central Malaya. Annals of Tropical Medicine & Parasitology 59(4), 425–433.CrossRefGoogle Scholar
Lim, BL, Lim, TW, Cheah, W and Yap, LF (1976) Angiostrongylus malaysiensis from Tuaran, Sabah, with reference to the distribution of the parasite in Malaysia. The Southeast Asian Journal of Tropical Medicine and Public Health 7(3), 384–389.Google Scholar
Lima, MSD and Guilherme, E (2018) Diagnosis, presence of endoparasites, and local knowledge on the infestation of the exotic giant African snail (Gastropoda: Pulmonata: Achatinidae), in the urban zone of Rio Branco, Acre, Brazil. Biota Neotropica 18(3), 1–10.CrossRefGoogle Scholar
Lima, ARMC, Mesquita, SD, Santos, SS, Aquino, ERPD, Rosa, LRS, Duarte, FS, Teixeira, AO, Costa, ZRS and Ferreira, MLB (2009) Alicata disease: neuroinfestation by Angiostrongylus cantonensis in Recife, Pernambuco, Brazil. Arquivos de Neuro-Psiquiatria 67(4), 1093–1096.CrossRefGoogle ScholarPubMed
Lima, WS, Cruz, ACL, Samasquini, SJJ, Mesquita, MN, Medeiros, LS, Pacheco, AD and Souza, SF (2020) Aspectos epidemiológicos de Aelurostrongylus abstrusus no Brasil [Epidemiological aspects of Aelurostrongylus abstrusus in Brazil]. Scientia Naturalis 2(2), 920–933. [In Portuguese.]Google Scholar
Lv, S, Zhang, Y, Liu, HX, et al. (2009) Invasive snails and an emerging infectious disease: results from the first national survey on Angiostrongylus cantonensis in China. PLoS Neglected Tropical Diseases 3(2), e368. doi:10.1371/journal.pntd.0000368CrossRefGoogle Scholar
Maldonado, A Jr, Simões, RO, Oliveira, APM, Motta, EM, Fernandez, MA, Pereira, Z, Monteiro, SS, Torres, EJL and Thiengo, SC (2010) First report of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Achatina fulica (Mollusca: Gastropoda) from Southeast and South Brazil. Memórias do Instituto Oswaldo Cruz 105(7), 938–941.CrossRefGoogle ScholarPubMed
Matayoshi, S, Noda, S and Sato, A (1987) Observations on the life history of Achatina fulica, an intermediate host of Angiostrongylus cantonensis, in the Amami Islands. Medical Entomology and Zoology 38, 297–301.CrossRefGoogle Scholar
Mead, AR (1961) Dispersal of the giant African snail. 257 pp. in The giant African snail: a problem in economic malacology, vol. Xvii. Chicago, USA, University of Chicago Press.Google Scholar
Meffowoet, CP, Kouam, KM, Tchakounte, FM and Kana, JR (2020) Parasites diversity of edible African giant snails (Achatina fulica and Archachatina marginata) in the Lekie, Wouri and Santchou localities of Cameroon during the dry season. Scientific Journal of Animal Science 9(7), 644–653.Google Scholar
Meijides-Mejías, C and Robledo, AR (2019) Primer reporte de larvas de estrongylidios Metastrongyloidea (Strongyluris larvae) en Achatina (Lissachatina) fulica (Mollusca, Achatinidae) en el municipio de Regla, La Habana, Cuba [First report of larvae of strongylids Metastrongyloidea (Strongyluris larvae) in Achatina (Lissachatina) fulica (Mollusca, Achatinidae) in the municipality of Regla, Havana, Cuba]. Revista estudantil 16 de abril 58(273), 90–93. [In Spanish.]Google Scholar
Morassutti, AL, Thiengo, SC, Fernandez, M, Sawanyawisuth, K and Graeff-Teixeira, C (2014) Eosinophilic meningitis caused by Angiotrongylus cantonensis: an emergent disease in Brazil. Memórias do Instituto Oswaldo Cruz 109(4), 399–407.CrossRefGoogle Scholar
Moreira, VL, Giese, EG, Melo, FT, 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(1), 90–97.CrossRefGoogle Scholar
Morocoima, A, Rodríguez, V, Rivas, R, Coriano, H, Rivero, S, Errante, R, Mitchell, M, Herrera, L and Urdaneta-Morales, S (2014) Achatina fulica Bowdich, 1822 (Mollusca, Gastropoda, Achatinidae) hospedador de helmintos, protozoarios y bacterias en el noreste de Venezuela [Achatina fulica Bowdich, 1822 (Mollusca, Gastropoda, Achatinidae) host of helminths, protozoa and bacteria in northeastern Venezuela]. Malariología y Salud Ambiental 54(2), 174–185. [In Spanish.]Google Scholar
Neuhauss, E, Fitarelli, M, Romanzini, J and Graeff-Teixeira, C (2007) Low susceptibility of Achatina fulica from Brazil to infection with Angiostrongylus costaricensis and A. cantonensis. Memórias do Instituto Oswaldo Cruz 102(1), 49–52.CrossRefGoogle ScholarPubMed
Noda, S, Uchikawa, R, Matayoshi, S, Watanabe, Y and Sato, A (1987) Observations on the transmission of Angiostrongylus cantonensis from snail to rodent. Journal of Helminthology 61(3), 241–246.CrossRefGoogle ScholarPubMed
Oda, FH, da Graça, RJ, Lima, FS, Alvarenga, FS and Takemoto, RM (2020) Cysts and larvae of Strongyluris: a parasite of amphibians and reptiles found in an urban population of Lissachatina fulica (Férussac, 1821) in southern Brazil. Veterinary Parasitology: Regional Studies and Reports 20(1), 100386.Google Scholar
Ohlweiler, FP, Guimarães, MCA, Takahashi, FY and Eduardo, JM (2010) Current distribution of Achatina fulica, in the state of São Paulo including records of Aelurostrongylus abstrusus (nematoda) larvae infestation. Revista do Instituto de Medicina Tropical de São Paulo 52(4), 211–214.CrossRefGoogle Scholar
Oliveira, JL and Santos, SB (2018) Distribution of cysts of Strongyluris sp. (Nematoda) in the pallial system of Achatina fulica Bowdich, 1822 from Vila Dois Rios and Vila do Abraão, Ilha Grande, Angra dos Reis, Rio de Janeiro. Brazilian Journal of Biology 79(1), 38–44.CrossRefGoogle Scholar
Oliveira, APM, Torres, EJL, Maldonado, A Jr, Araujo, JLB, Fernandez, MA and Thiengo, SC (2010) Achatina fulica como hospedeiro intermediário de nematóideos de interesse médico-veterinário em Goiás, Brasil [Achatina fulica as an intermediate host of nematodes of veterinary medical interest in Goiás, Brazil]. Revista de Patologia Tropical 39(3), 199–210. [In Portuguese.]Google Scholar
Oliveira, APM, Gentile, R, Maldonado, A Jr, 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. Memórias do Instituto Oswaldo Cruz 110(6), 739–744.CrossRefGoogle Scholar
Oliveira, KL, Simões, RS and Decanine, D (2021) First report of Achatina fulica (Bowdich, 1822) naturally infected with nematodes from the families Angiostrongylidae and Rhabditidae in the city of Campo Grande, Mato Grosso do Sul. Revista de Biologia Neotropical 18(1), 83–89.Google Scholar
Orico, LD, Barbosa, CM, Luca, LR, Soares, RM and Gregori, F (2019) Angistrongylus cantonensis and Ancylostoma caninum detection in snails of São Paulo city (2016–2017), Brazil. Ars Veterinaria 35(3), 115–121.CrossRefGoogle Scholar
Penagos-Tabares, F, Lange, MK, Vélez, J, Hirzmann, J, Gutiérrez-Arboleda, J, Taubert, A, Hermosilla, C and Chaparro Gutiérrez, JJ (2019) The invasive giant African snail Lissachatina fulica as natural intermediate host of Aelurostrongylus abstrusus, Angiostrongylus vasorum, Troglostrongylus brevior, and Crenosoma vulpis in Colombia. PLoS Neglected Tropical Diseases 13(4), e0007277.CrossRefGoogle Scholar
Peng, J, He, ZP, Zhang, S, et al. (2017) Phylogeography of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae) in southern China and some surrounding areas. PLoS Neglected Tropical Diseases 11(8), e0005776.CrossRefGoogle ScholarPubMed
Pereira, CADJ, Coaglio, AL, Capettini, LS, Becattini, R, Ferreira, APPN, Costa, A and Lima, WDS (2020) New approaches to studying morphological details of intramolluscan stages of Angiostrongylus vasorum. Revista Brasileira de Parasitologia Veterinária 29(2), e000420.CrossRefGoogle ScholarPubMed
Pérez, JAR, Mejías, CM, Robledo, AR, del Vallín, VP, Viel, AM, Pérez, DG, González, WC, Contreras, AJD and Robles, LM (2019) Strongylides in Achatina (Lissachatina) fulica (Mollusca, Achatinidae) in Havana, Cuba. Revista Cubana de Investigaciones Biomédicas 38(1), 1–7.Google Scholar
Picot, H, Lavarde, V and Grillot, ML (1976) Presence of Angiostrongylus cantonensis in the Réunion Island. Isolation of the strain. Bulletin de la Societe de Pathologie Exotique et de ses Filiales 69(4), 329–331.Google ScholarPubMed
Qvarnstrom, Y, da Silva, ACA, Teem, JL, Hollingsworth, R, Bishop, H, Graeff-Teixeira, C and da Silva, AJ (2010) Improved molecular detection of Angiostrongylus cantonensis in mollusks and other environmental samples with a species-specific internal transcribed spacer 1-based TaqMan assay. Applied and Environmental Microbiology 76(15), 5287–5289.CrossRefGoogle ScholarPubMed
Ramos-de-Souza, J, Maldonado, A Jr, Vilela, RV, Andrade-Silva, BE, Barbosa, HS, Gomes, SR and Thiengo, SC (2021) First report of the nematode Cruzia tentaculata using molluscs as natural intermediate hosts, based on morphology and genetic markers. International Journal for Parasitology: Parasites and Wildlife 15(1), 105–111.Google ScholarPubMed
Ramos-de-Souza, J, Thiengo, SC, Fernandez, MA, et al. (2018) First records of molluscs naturally infected with Angiostrongylus cantonensis (Nematoda: Metastrongyloidea) in Sergipe State, Northeastern Brazil, including new global records of natural intermediate hosts. Revista do Instituto de Medicina Tropical de São Paulo 60(1), e1.CrossRefGoogle ScholarPubMed
Raut, SK and Barker, GM (2002) Achatina fulica Bowdich and other Achatinidae pests in tropical agriculture. pp. 55–114. In Barker, GM (Ed.) Molluscs as crop pests, vol. 55. New Zealand, CAB Publishing.Google Scholar
Robinson, DG (2000) Public health concern: mollusk vectored angiostrongyliasis. USDA APHIS PPO R 8, 1–4.Google Scholar
Roda, A, Nachman, G, Weihman, S, Yong Cong, M and Zimmerman, F (2016) Reproductive ecology of the giant African snail in south Florida: implications for eradication programs. PLoS One 11(11), e0165408.CrossRefGoogle ScholarPubMed
Rodrigues, PS, Gomes, ST, Montresor, LC, Ramos-de-Souza, J, Barros, LA, Fernandez, LC and Thiengo, SC (2022) The giant African snail Achatina (Lissachatina) fulica Bowdich, 1822 as an intermediate host of Aelurostrongylus abstrusus (Railliet, 1898) in the Rio de Janeiro state, Brazil. Veterinary Parasitology: Regional Studies and Reports 30(1), 100712.Google Scholar
Rollins, RL, Cowie, RH, Echaluse, MV and Medeiros, MC (2021) Host snail species exhibit differential Angiostrongylus cantonensis prevalence and infection intensity across an environmental gradient. Acta Tropica 216(1), 105824.CrossRefGoogle ScholarPubMed
Scrimgeour, EM and Welch, JS (1984) Angiostrongylus cantonensis in East New Britain, Papua New Guinea. Transactions of the Royal Society of Tropical Medicine and Hygiene 78(6), 774–775.CrossRefGoogle ScholarPubMed
Silva, GM, Santos, MB, Melo, CM and Jeraldo, VLS (2020) Achatina fulica (Gastropoda: Pulmonata): occurrence, environmental aspects and presence of nematodes in Sergipe, Brazil. Brazilian Journal of Biology 80(2), 245–254.CrossRefGoogle ScholarPubMed
Silva, GM, Thiengo, SC, Menezes, AN, Melo, CMD and Jeraldo, VLS (2022) Relative condition factor and predictive model for the presence of the invasive snail Achatina (Lissachatina) fulica in Sergipe, Northeast Brazil. Biota Neotropica 22(2), 1–15.CrossRefGoogle Scholar
Simião, MS and Fischer, ML (2004) Estimativa e inferências do método de controle do molusco exótico Achatina fulica no Pontal do Paraná, Litoral do Estado do Paraná [Estimation and inferences of the method of control of the exotic mollusk Achatina fulica in Pontal do Paraná, Coast of the State of Paraná]. Cadernos de Biodiversidade 4(1), 1–11. [In Portuguese.]Google Scholar
Smith, TR, Howe, AC, Dickens, K, Stanley, JD, Brito, JA and Inserra, RN (2015) First comprehensive molecular and morphological identification of the rat lungworm, Angiostrongylus cantonensis Chen, 1935 (Nematoda: Strongylida: Metastrongylida) in association with the giant African snail, Lissachatina fulica Bowdich (Gastropoda: Pulmonata: Achtinidae) in Florida. Nematropica 45(1), 20–33.Google Scholar
Soares, CB, Hoga, LAK, Peduzzi, M, Sangaleti, C, Yonekura, T and Silva, DRAD (2014) Revisão integrativa: conceitos e métodos utilizados na enfermagem [Integrative review: concepts and methods used in nursing]. Revista da Escola de Enfermagem da USP 48(2), 335–345. [In Portuguese.]CrossRefGoogle Scholar
Solórzano-Alava, L, Sánchez-Amador, F and Valverde, T (2019) Angiostrongylus (Parastrongylus) cantonensis en huéspedes intermediarios y definitivos en Ecuador, 2014–2017 [Angiostrongylus (Parastrongylus) cantonensis in intermediate and definitive hosts in Ecuador, 2014–2017]. Biomédica 39(2), 370–384. [In Spanish.]CrossRefGoogle ScholarPubMed
Song, L, Wang, X, Yang, Z, Lv, Z and Wu, Z (2016) Angiostrongylus cantonensis in the vector snails Pomacea canaliculata and Achatina fulica in China: a meta-analysis. Parasitology Research 115(3), 913–923.CrossRefGoogle ScholarPubMed
Souza, FN, Santos, MA, Alves, DA, et al. (2021) Angiostrongylus cantonensis in urban populations of terrestrial gastropods and rats in an impoverished region of Brazil. Parasitology 148(8), 994–1002.CrossRefGoogle Scholar
Spratt, DM (2015) Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal of Parasitology: Parasites and Wildlife 4(2), 178–189.Google ScholarPubMed
Stafford, EE, Sukeri, S and Sutanti, T (1976) The bandicoot rat, a new host record for Angiostrongylus cantonensis in Indonesia. The Southeast Asian Journal of Tropical Medicine and Public Health 1(1), 41–44.Google Scholar
Teles, HMS and Fontes, LR (2002) Implicações da introdução e dispersão de Achatina fulica Bowdich, 1882 no Brasil [Implications of the introduction and dispersion of Achatina fulica Bowdich, 1882 in Brazil]. Boletim do Instituto Adolfo Lutz 12(1), 3–5. [In Portuguese.]Google Scholar
Thiengo, SC and Fernandez, MA (2016) Moluscos como hospederos intermediarios de Angiostrongylus cantonensis en Brasil [Molluscs as intermediate hosts of Angiostrongylus cantonensis in Brazil]. pp. 270–276. In Angiostrongylus cantonensis emergencia em America [Angiostrongylus cantonensis emergence in America]. Havana, Editorial Academia. [In Spanish.]Google Scholar
Thiengo, SC, Farraco, 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(6), 693–702.CrossRefGoogle Scholar
Thiengo, SC, Fernandez, MA, Torres, EJ, Coelho, PM and Lanfredi, RM (2008) First record of a nematode Metastrongyloidea (Aelurostrongylus abstrusus larvae) in Achatina (Lissachatina) fulica (Mollusca, Achatinidae) in Brazil. Journal of Invertebrate Pathology 98(1), 34–39.CrossRefGoogle ScholarPubMed
Thiengo, SC, Simões, RO, Fernandez, MA and Maldonado, A Jr (2013) Angiostrongylus cantonensis and Rat lungworm disease in Brazil. Hawai'i Journal of Medicine & Public Health 72(1), 18–22.Google ScholarPubMed
Thiengo, SC, Maldonado, A, Mota, EM, et al. (2010) The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernambuco, northeast Brazil. Acta Tropica 115(3), 194–199.CrossRefGoogle ScholarPubMed
Tokiwa, T, Harunari, T, Tanikawa, T, Komatsu, N, Koizumi, N, Tung, KC and Ohta, N (2012) Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitology International 61(3), 431–436.CrossRefGoogle ScholarPubMed
Tomaz, TP, Gentile, R, Garcia, JS, Teixeira, BR and Faro, MJ (2018) A survey of freshwater and terrestrial snails in a predominantly urban municipality of Rio de Janeiro State, Brazil, with emphasis on human parasites vectors. Revista do Instituto de Medicina Tropical de São Paulo 60(1), e76.CrossRefGoogle Scholar
Tujan, MA, Angelica, A, Fontanilla, IKC and Paller, VGV (2016) Vectors and spatial patterns of Angiostrongylus cantonensis in selected rice-farming villages of Munoz, Nueva Ecija, Philippines. Journal of Parasitology Research 2016(2), 1–7.CrossRefGoogle ScholarPubMed
Valente, R, Diaz, JI, Lorenti, EA, Salomón, OD and Navone, GT (2016) Nematodes from Achatina fulica Bowdich, 1822 (Mollusca: Gastropoda) in Argentina. Helminthologia 53(1), 109–112.CrossRefGoogle Scholar
Valente, R, Diaz, JI, Salomón, OD and Navone, GT (2017) Natural infection of the feline lungworm Aelurostrongylus abstrusus in the invasive snail Achatina fulica from Argentina. Veterinary Parasitology 235(1), 17–19.CrossRefGoogle ScholarPubMed
Valente, R, Robles, MR and Diaz, JI (2020) Gastropods as intermediate hosts of Angiostrongylus spp. in the Americas: bioecological characteristics and geographical distribution. Memórias do Instituto Oswaldo Cruz 115(1), e200236.CrossRefGoogle ScholarPubMed
Vázquez, AA and Sánchez, J (2015) First record Angiostrongylus cantonensis of the invasive land snail Achatina (Lissachatina) fulica (Bowdich, 1822) (Gastropoda: Achatinidae), vector of (Nematoda: Angiostrongylidae), in Havana, Cuba. Molluscan Research 35(2), 139–142.CrossRefGoogle Scholar
Vijayan, K, Suganthasakthivel, R, Sajeev, TV, Soorae, PS, Naggs, F and Wade, CM (2020) Genetic variation in the Giant African Snail Lissachatina fulica (Bowdich, 1822) in its invasive ranges of Asia and West Africa. Biological Journal of the Linnean Society 131(4), 973–985.CrossRefGoogle Scholar
Vitta, A, Nateeworanart, S and Tattiyapong, M (2011) Survey of Angiostrongylus cantonensis in rats and giant African land snails in Phitsanulok province, Thailand. Asian Pacific Journal of Tropical Medicine 4(8), 597–599.CrossRefGoogle ScholarPubMed
Vitta, A, Srisongcra, N, Thiproaj, J, Wongma, A, Polsut, W, Fukruksa, C and Dekumyoy, P (2016) Phylogeny of Angiostrongylus cantonensis in Thailand based on cytochrome c oxidase subunit I gene sequence. Southeast Asian Journal of Tropical Medicine and Public Health 47(3), 377–386.Google Scholar
Wallace, GD and Rosen, L (1969) Studies on eosinophilic meningitis. V. Molluscan hosts of Angiostrongylus cantonensis on the Pacific Islands. American Journal of Tropical Medicine and Hygiene 18(2), 206–216.CrossRefGoogle Scholar
Wang, QP, Lai, DH, Zhu, XQ, Chen, XG and Lun, ZR (2008) Human angiostrongyliasis. Lancet Infectious Diseases 8(10), 621–630.CrossRefGoogle ScholarPubMed
Yang, X, Qu, Z, He, H, et al. (2012) Enzootic angiostrongyliasis in Guangzhou, China, 2008–2010. The American Journal of Tropical Medicine and Hygiene 86(5), 846–849.CrossRefGoogle ScholarPubMed
Zanol, J, Fernandez, MA, Oliveira, APMD, Russo, CADM and Thiengo, SC (2010) O caramujo exótico invasor Achatina fulica (Stylommatophora, Mollusca) no Estado do Rio de Janeiro (Brasil): situação atual [The invasive exotic snail Achatina fulica (Stylommatophora, Mollusca) in the State of Rio de Janeiro (Brazil): current situation]. Biota Neotropica 10(3), 447–444. [In Portuguese.]CrossRefGoogle Scholar
Supplementary material: File

Silva et al. supplementary material

Silva et al. supplementary material

Download Silva et al. supplementary material(File)
File 99.8 KB