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Alternative pathways in Angiostrongylus cantonensis (Metastrongyloidea: Angiostrongylidae) transmission

Published online by Cambridge University Press:  28 September 2020

David Modrý Open the ORCID record for David Modrý [Opens in a new window] ,
Barbora Fecková Open the ORCID record for Barbora Fecková [Opens in a new window] ,
Barbora Putnová ,
Sheina Macy Manalo  and
Domenico Otranto Open the ORCID record for Domenico Otranto [Opens in a new window]
David Modrý*
Affiliation:
University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, Brno, Czech Republic Biology Centre, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 6, 611 37, Brno, Czech Republic
Barbora Fecková
Affiliation:
University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, Brno, Czech Republic
Barbora Putnová
Affiliation:
University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, Brno, Czech Republic
Sheina Macy Manalo
Affiliation:
University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1946/1, Brno, Czech Republic Department of Veterinary Paraclinical Sciences, University of the Philippines Los Baňos, Philippines
Domenico Otranto
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Bari, Italy Faculty of Veterinary Sciences, Bu-Ali Sina University, Hamedan, Iran
*
Author for correspondence: David Modrý, E-mail: [email protected]
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Abstract

In order to elucidate the infection pathways of third stage larvae (L3) of Angiostrongylus cantonensis, we performed experiments to assess: (i) the shedding of L3 from two species of experimental veronicellid slugs drowned in water and the ratio of emerged larvae, (ii) the transmission of viable L3 from drowned terrestrial gastropods to aquatic snails, and (iii) the transmission of viable L3 between terrestrial snails. Molluscs were experimentally infected by first stage larvae (L1) of A. cantonensis. Significantly more L3 larvae were released from Veronicella cubensis than from Veronicella sloanei. Numerous L3 were observed in the muscular foot, and also in the connective tissue between internal organs. Experimental exposure of P. maculata to L3 of A. cantonensis liberated from other gastropod species led to their infection and the infectivity of larvae after intermediesis was demonstrated by infection of laboratory rats (Rattus norvegicus). The transmission of L3 was observed in three out of four experiment replications and L3 were retrieved from 6 out of 24 Subulina octona snails. The infected synanthropic molluscs represent a key component in the epidemiology of human infections by A. cantonensis. Escape of L3 larvae from bodies of dead snails or slugs and their ability to infect further gastropod hosts (intermediesis) represents a public health risk. Thus, control of molluscs living in peri-domestic environment is an essential part of prevention of human infections.

Keywords

Angiostrongylus cantonensisdiseaseemergingexperimental infectionintermediesiszoonosis
Type
Research Article
Information
Parasitology , Volume 148 , Special Issue 2: 6th International Workshop on Angiostrongylus and Angiostrongyliasis, Hilo, Hawai'i, USA, January, 2020 , February 2021 , pp. 167 - 173
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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Footnotes

*

Authors contributed equally

References

Anderson, RC (2000) Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd Edn. Wallingford, Oxon (UK): CABI Publishing, 650 pp.CrossRefGoogle Scholar
Barratt, J, Chan, D, Sandaradura, I, Malik, R, Spielman, D, Lee, R, Mariott, 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.CrossRefGoogle ScholarPubMed
Campbell, BG and Little, MD (1988) The finding of Angiostrongylus cantonensis in rats in new Orleans. American Journal of Tropical Medicine and Hygiene 38, 568–573.CrossRefGoogle ScholarPubMed
Červená, B, Modrý, D, Fecková, B, Hrazdilová, K, Foronda, P, Alonso, AM, Lee, R, Walker, J, Niebuhr, CN, Malik, R and Šlapeta, J (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 and Vectors 12, 241.CrossRefGoogle ScholarPubMed
Cheng, TC and Alicata, JE (1964) Possible role of water in the transmission of Angiostrongylus cantonensis (Nematoda: Metastrongylidae). The Journal of Parasitology 50, 39–40.Google Scholar
Colella, V, Giannelli, A, Brianti, E, Ramos, RAN, Cantacessi, C, Dantas-Torres, F and Otranto, D (2015) Feline lungworms unlock a novel mode of parasite transmission. Scientific Reports 5, 13105.CrossRefGoogle ScholarPubMed
Conboy, G, Guselle, N and Schaper, R (2017) Spontaneous shedding of metastrongyloid third-stage larvae by experimentally infected Limax maximus. Parasitology Research 116, 41–54.CrossRefGoogle ScholarPubMed
Cowie, RH (2013a) Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai'i Journal of Medicine & Public Health: A Journal of Asia Pacific Medicine & Public Health 72, 6–9.Google Scholar
Cowie, RH (2013b) Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawai'i Journal of Medicine & Public Health: A Journal of Asia Pacific Medicine & Public Health 72, 70–74.Google Scholar
Crook, JR, Fulton, SE and Supanwong, K (1971) The infectivity of third stage Angiostrongylus cantonensis larvae shed from drowned Achatina fulica snails and the effect of chemical agents on infectivity. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 602–605.CrossRefGoogle ScholarPubMed
Dard, C, Tessier, E, Nguyen, D, Epelboin, L, Harrois, D, Swale, C, Cabié, A, de Meuron, K, Miossec, C and Desbois-Nogard, N (2020) First cases of Angiostrongylus cantonensis infection reported in Martinique 2002–2017. Parasite 27, 31.CrossRefGoogle ScholarPubMed
Epelboin, L, Blondé, R, Chamouine, A, Chrisment, A, Diancourt, L, Villemant, N, Atale, A, Cadix, C, Caro, V, Malvy, D and Collet, L (2016) Angiostrongylus cantonensis infection on Mayotte Island, Indian Ocean, 2007–2012. PLoS Neglected Tropical Diseases 10, e0004635.CrossRefGoogle ScholarPubMed
Giannelli, A, Colella, V, Abramo, F, do Nascimento Ramos, RA, Falsone, L, Brianti, E, Varcasia, A, Dantas-Torres, F, Knaus, M, Fox, MT and Otranto, D (2015) Release of lungworm larvae from snails in the environment: potential for alternative transmission pathways. PLoS Neglected Tropical Diseases 9, e0003722.CrossRefGoogle ScholarPubMed
Grewal, PS, Grewal, SK, Tan, L and Adams, BJ (2003) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 35, 146–156.Google ScholarPubMed
Hollingsworth, RG, Howe, K and Jarvi, SI (2013) Control measures for slug and snail hosts of Angiostrongylus cantonensis, with special reference to the semi-slug Parmarion martensi. Hawai'i Journal of Medicine & Public Health: A Journal of Asia Pacific Medicine & Public Health 72, 75–80.Google ScholarPubMed
Howe, K, Kaluna, L, Lozano, A, Torres Fischer, B, Tagami, Y, McHugh, R and Jarvi, S (2019) Water transmission potential of Angiostrongylus cantonensis: larval viability and effectiveness of rainwater catchment sediment filters. PLoS ONE 14, e0209813.CrossRefGoogle ScholarPubMed
Jarvi, SI, Farias, MEM, Howe, K, Jacquier, S, Hollingsworth, R and Pitt, W (2012) Quantitative PCR estimates Angiostrongylus cantonensis (rat lungworm) infection levels in semi-slugs (Parmarion martensi). Molecular and Biochemical Parasitology 185, 174–176. https://doi.org/10.1016/j.molbiopara.2012.08.002 .CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kim, JR, Hayes, KA, Yeung, NW and Cowie, RH (2016) Identity and distribution of introduced slugs (Veronicellidae) in the Hawaiian and Samoan Islands. Pacific Science 70, 477–493.CrossRefGoogle Scholar
Kramer, K, Posner, J and Gosnell, W (2018) The role of gastropod mucus in the transmission of Angiostrongylus cantonensis, a potentially serious neurological infection. ACS Chemical Neuroscience 9, 629–632.CrossRefGoogle ScholarPubMed
Mendoza-Roldan, JA, Modrý, D and Otranto, D (2020) Zoonotic parasites of reptiles: a crawling threat. Trends in Parasitology 36, 677–687.CrossRefGoogle ScholarPubMed
Morley, N (2010) Aquatic molluscs as auxiliary hosts for terrestrial nematode parasites: implications for pathogen transmission in a changing climate. Parasitology 137, 1041–1056.CrossRefGoogle Scholar
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, 241–246.CrossRefGoogle Scholar
Rachford, FW (1976) Host-parasite relationship of Angiostrongylus cantonensis in Lymnaea palustris. II. Histopathology. Experimental Parasitology 39, 382–392.CrossRefGoogle ScholarPubMed
Richards, CS and Merritt, JW (1967) Studies on Angiostrongylus cantonensis In molluscan intermediate hosts. The Journal of Parasitology 53, 382.CrossRefGoogle ScholarPubMed
Thomé, JW (1972) Redescrição dos tipos de Veronicellidae (Mollusca, Gastropoda) neotropicais: VIII. Espécies depositadas no ‘Institut für Spezielle Zoologie und zoologisches Museum’ de Berlim, Alemanha Oriental. Arquivos de Zoologia 21, 235–281.CrossRefGoogle Scholar