Range of metastrongylids (superfamily Metastrongyloidea) of public health and veterinary concern present in livers of the endemic lizard Gallotia galloti of Tenerife, Canary Islands, Spain
Language English Country Great Britain, England Media electronic
Document type Journal Article
Grant support
grant M-ULL, convocatoria 2019
Universidad de La Laguna
PhD Mobility scholarship
Masaryk University
National Institute of Virology and Bacteriology (Programme EXCELES, ID Project No. LX22NPO5103)
European Union - Next Generation EU
ProID2021010013
FEDER 2014-2020/UE
"Estudio de patógenos en aves migratorias y especies exóticas en un escenario de cambio climático" agreement
Canary Government, Dirección General de Lucha contra el Cambio Climático y Medio Ambiente
ProID2021010013
Canary Government, Spain
22-26136S
Czech Science Foundation
PubMed
36890511
PubMed Central
PMC9997015
DOI
10.1186/s13071-023-05653-z
PII: 10.1186/s13071-023-05653-z
Knihovny.cz E-resources
- Keywords
- Aelurostrongylus abstrusus, Angiostrongylus cantonensis, Angiostrongylus vasorum, Crenosoma striatum, Gallotia galloti, Multiplex PCR,
- MeSH
- Ecosystem MeSH
- Liver MeSH
- Lizards * parasitology MeSH
- Rats MeSH
- Metastrongyloidea * MeSH
- Public Health MeSH
- Animals MeSH
- Check Tag
- Rats MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Spain epidemiology MeSH
BACKGROUND: Endemic lizards of the genus Gallotia are of high ecological value to the terrestrial ecosystem of the archipelago of the Canary Islands, being potent seed spreaders as well as an important component of the diet of other vertebrates. The endemic lizard Gallotia galloti in Tenerife has recently been reported to be a paratenic host of Angiostrongylus cantonensis, an invasive metastrongylid with zoonotic potential that is associated with rats as definitive hosts. However, microscopic examination of G. galloti tissue samples also revealed the presence of other metastrongylid larvae inside granulomas on the liver of this reptile. The aim of this study was to investigate the presence of helminths other than A. cantonensis in tissues of G. galloti from Tenerife. METHODS: A multiplex-nested PCR targeting the internal transcribed spacer 1 was designed that enabled the species-specific detection of A. cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, Crenosoma striatum and Crenosoma vulpis. Liver samples from 39 G. galloti were analysed. RESULTS: Five metastrongylids were detected: A. cantonensis (15.4% of samples analysed), A. vasorum (5.1%), Ae. abstrusus (30.8%), C. striatum (30.8%) and undetermined metastrongylid sequences (12.8%). Co-infection was highly prevalent among the lizards which tested positive. CONCLUSIONS: The study provides a new specific tool for the simultaneous detection of a range of metastrongylids of veterinary importance as well as new data on the circulation of metastrongylids in an ecosystem dominated by lizards.
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Institute of Parasitology Biology Center of Czech Academy of Sciences Prague Czech Republic
See more in PubMed
Anderson RC. Nematode parasites of vertebrates: their development and transmission. 2. Wallingford: CABI Publishing; 2000.
Anettová L, Izquierdo-Rodriguez E, Foronda P, Baláž V, Novotný L, Modrý D. Endemic lizards Gallotia galloti are paratenic hosts in the life cycle of invasive Angiostrongylus cantonensis in Tenerife, Spain. Parasitology. 2022;149:934–939. doi: 10.1017/S0031182022000336. PubMed DOI PMC
Arechavaleta M, Rodríguez S, Zurita N, García A (2010) Lista de Especies Silvestres de Canarias. Hongos, Plantas y Animales Terrestres. Santa Cruz de Tenerife: Gobierno de Canarias. 2021 (in Spanish).
Asato R, Sato Y, Otsuru M. The occurrence of Angiostrongylus cantonensis in toad and frogs in Okinawa Prefecture, Japan. Japan J Parasitol. 1978;27:1–8.
Bhaibulaya M. A new species of Angiostrongylus in an Australian rat, Rattus fuscipes. Parasitology. 1968;58:789–799. doi: 10.1017/S0031182000069572. DOI
Bolt G, Monrad J, Koch J, Jensen AL. Canine angiostrongylosis: a review. Vet Rec. 1994;135:447–452. doi: 10.1136/vr.135.19.447. PubMed DOI
Box EK, Yabsley MJ, Garrett KB, Thompson AT, Wyckoff ST, Cleveland CA. Susceptibility of anurans, lizards, and fish to infection with Dracunculus species larvae and implications for their roles as paratenic hosts. Sci Rep. 2021;11:11802. doi: 10.1038/s41598-021-91122-5. PubMed DOI PMC
Burke JB, Rodgers LJ. Gastric ulceration associated with larval nematodes (Anisakis sp. type I) in pen reared green turtles (Chelonia mydas) from Torres Strait. J Wildl Dis. 1982;18:41–46. doi: 10.7589/0090-3558-18.1.41. PubMed DOI
Bursey CR. Histological aspects of natural eustrongyloid infections of the northern water snake, Nerodia sipedon. J Wildl Dis. 1986;22:527–532. doi: 10.7589/0090-3558-22.4.527. PubMed DOI
Colella V, Knaus M, Lai O, Cantile C, Abramo F, Rehbein S, et al. Mice as paratenic hosts of Aelurostrongylus abstrusus. Parasit Vectors. 2019;12:49. doi: 10.1186/s13071-019-3293-2. PubMed DOI PMC
Deslyper G, Doherty DG, Carolan JC, Holland CV. The role of the liver in the migration of parasites of global significance. Parasit Vectors. 2019;12:531. doi: 10.1186/s13071-019-3791-2. PubMed DOI PMC
Djennoune D, Marniche F, Amroun M, Boulay R. Comparative diet of hedgehogs (Atelerix algirus) in two localities in Kabylia, Algeria. Turk J Zool. 2018;42:207–217. doi: 10.3906/zoo-1705-51. DOI
Falsone L, Colella V, Napoli E, Brianti E, Otranto D. The cockroach Periplaneta americana as a potential paratenic host of the lungworm Aelurostrongylus abstrusus. Exp Parasitol. 2017;182:54–57. doi: 10.1016/j.exppara.2017.09.023. PubMed DOI
Foronda P, López-González M, Miquel J, Torres J, Segovia M, Abreu-Acosta N, et al. Finding of Parastrongylys cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain) Acta Trop. 2010;114:123–127. doi: 10.1016/j.actatropica.2010.02.004. PubMed DOI
Fuehrer HP, Morelli S, Bleicher J, Brauchart T, Edler M, Eisschiel N, et al. Detection of Crenosoma spp, Angiostrongylus vasorum and Aelurostrongylus abstrusus in gastropods in eastern Austria. Pathongens. 2020;9:1046. doi: 10.3390/pathogens9121046. PubMed DOI PMC
Gerichter ChB. Studies on the nematodes parasitic in the lungs of Felidae in Palestine. Parasitology. 1949;39:251–262. doi: 10.1017/S0031182000083827. PubMed DOI
Hidelaratchi MD, Riffsy MT, Wijesekera JC. A case of eosinophilic meningitis following monitor lizard meat consumption, exacerbated by anthelminthics. Ceylon Med J. 2005;50:84–86. doi: 10.4038/cmj.v50i2.1577. PubMed DOI
Hobmaier M, Hobmaier A. Intermediate hosts of Aelurostrongylus abstrusus of the cat. Exp Biol Med. 1935;32:1641–1647. doi: 10.3181/00379727-32-8210C. DOI
Izquierdo-Rodriguez E, Martin-Carrillo N, Valladares B, Foronda P. Study of zoonotic enteric pathogens of Atelerix algirus in Tenerife, Canary Islands, Spain. Front Vet Sci. 2020;8:579602. doi: 10.3389/fvets.2020.579602. PubMed DOI PMC
Jeżewski W, Buńkowska-Gawlik K, Hildebrand J, Perec-Matysiak A, Laskowski Z. Intermediate and paratenic hosts in the life cycle of Aelurostrongylus abstrusus in natural environment. Vet Parasitol. 2013;198:401–405. doi: 10.1016/j.vetpar.2013.09.003. PubMed DOI
Jones HI. Abbreviata (Nematoda: Physalopteroidea) from western Australian snakes. Aust J Zool. 1978;26:789–807. doi: 10.1071/ZO9780789. DOI
Jones HI. Dwarf monitor lizards (Varanidae: Varanus, Odatria s. gen.) as definitive and paratenic hosts for physalopteran nematodes. Aust J Zool. 2010;58:69–75. doi: 10.1071/ZO09122. DOI
Kanpittaya J, Jitpimolmard S, Tiamkao S, Mairiang E. MR findings of eosinophilic meningoencephalitis attributed to Angiostrongylus cantonensis. Am J Neuroradiol. 2000;21:1090–1094. PubMed PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
Lai CH, Yen CM, Chin C, Chung HC, Kuo HC, Lin HH. Eosinophilic meningitis caused by Angiostrongylus cantonensis after ingestion of raw frogs. Am J Trop Med Hyg. 2007;76:399–402. doi: 10.4269/ajtmh.2007.76.399. PubMed DOI
Lange M, Penagos-Tabares F, Hirzmann J, Failing K, Schaper R, Van der Bourgonie YR, et al. Prevalence of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Crenosoma vulpis larvae in native slug populations in Germany. Vet Parasitol. 2018;30:120–130. doi: 10.1016/j.vetpar.2018.03.011. PubMed DOI
Mackerras MJ. Observations on the life history of the cat Lungworm. Aelurostrongylus abstrusus (Railliet, 1898) (Nematoda: Metastrongylidae) Aust J Zool. 1957;5:188–195. doi: 10.1071/ZO9570188. DOI
Magnino S, Colin P, Dei-Cas E, Madsen M, McLauchlin J, Nöckler K, et al. Biological risks associated with consumption of reptile products. Int J Food Microbiol. 2009;134:163–175. doi: 10.1016/j.ijfoodmicro.2009.07.001. PubMed DOI
Martin-Alonso A, Abreu-Yanes E, Feliu C, Mas-Comas S, Bargues MD, Valladares B, et al. Intermediate hosts of Angiostrongylus cantonensis in Tenerife, Spain. PLoS ONE. 2015;10:e0120686. doi: 10.1371/journal.pone.0120686. PubMed DOI PMC
Medina M, Nogales M. A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna. Biodivers Conserv. 2009;18:829–846. doi: 10.1007/s10531-008-9503-4. DOI
Morand S, Bouamer S, Hugot JP. Micromammals and macroparasites: from evolutionary ecology to management. 1. Tokyo: Springer Japan; 2006.
Mouhoub-Sayah C, Djoudad-Kadji H, Kletty F, Malan A, Robin JP, Saboureau M, et al. Seasonal variations in the diet and food selection of the Algerian hedgehog Atelerix algirus. Afr Zool. 2018;53:1–10. doi: 10.1080/15627020.2017.1419072. DOI
Mozzer LR, Lima WS. Gallus gallus domesticus: paratenic host of Angiostrongylus vasorum. Vet Parasitol. 2015;207:81–84. doi: 10.1016/j.vetpar.2014.11.003. PubMed DOI
Panackel C, Vishad CG, Vijayakumar K, Sharma RN. Eosinophilic meningitis due to Angiostrongylus cantonensis. Indian J Med Microbiol. 2006;24:220–221. doi: 10.1016/S0255-0857(21)02355-0. PubMed DOI
Parker GA, Ball MA, Chubb JC. Evolution of complex life cycles in trophically transmitted helminths. 1. Host incorporation and tropic ascent. J Evol Biol. 2015;28:267–291. doi: 10.1111/jeb.12575. PubMed DOI
Pleguezuelos JM. In: Pleguezuelos JM, Márquez R, Lizana M, eds. Atlas y libro rojo de los anfibios y reptiles de España. Madrid: Dirección General de Conservación de la Naturaleza; 2002.
Pozio E. The broad spectrum of Trichinella hosts: from cold- to warm-blooded animals. Vet Parasitol. 2005;132:3–11. doi: 10.1016/j.vetpar.2005.05.024. PubMed DOI
Qvarnstrom Y, da Silva AC, Teem JL, Hollingsworth R, Bishop H, Graeff-Teixeira C, et al. Improved molecular detection of Angiostrongylus cantonensis in mollusks and other environmental samples with a species-specific internal transcribed spacer 1-based TaqMan assay. Appl Environ Microbiol. 2010;76:5287–5289. doi: 10.1128/AEM.00546-10. PubMed DOI PMC
Rosen L, Laigret J, Bories S. Observation on an outbreak of eosinophilic meningitis on Tahiti, French Polinesia. Am J Epidemiol. 1961;74:26–42. doi: 10.1093/oxfordjournals.aje.a120198. PubMed DOI
Sánchez Vicente S. Contribución al conocimiento de la parasitofauna (Helmintos y Artrópodos) de mamíferos no lagomorfos de Canarias. Barcelona: Departament de Microbiologia i Parasitologia Sanitàries, Universitat de Barcelona; 2013 (in Spanish).
Segeritz L, Cardona A, Taubert A, Hermosilla C, Ruiz A. Autochthonous Angiostrongylus cantonensis, Angiostrongylus vasorum and Aelurostrongylus abstrusus infections in native terrestrial gastropods from the Macaronesian Archipelago of Spain. Parasitol Res. 2021;120:2671–2680. doi: 10.1007/s00436-021-07203-x. PubMed DOI PMC
Udiz-Rodriguez R, García-Livia K, Valladares-Salmerón M, Dorta-Almenar MN, Martín-Carrillo N, Martin-Alonso A, et al. First ocular report of Gurltia paralysans (Wolffhügel, 1933) in cat. Vet Parasitol. 2018;15:74–77. doi: 10.1016/j.vetpar.2018.03.027. PubMed DOI PMC
Wallace GD, Rosen L. Studies on eosinophilic meningitis. 2. experimental infection of shrimps and crabs with Angiostrongylys cantonensis. Am J Epidemiol. 1986;84:120–131. doi: 10.1093/oxfordjournals.aje.a120617. PubMed DOI
Wang QP, Wu ZD, Wei J, Owen RL, Lun ZR. Human Angiostrongylus cantonensis: an update. Eur J Clin Microbiol Infect Dis. 2012;31:389–395. doi: 10.1007/s10096-011-1328-5. PubMed DOI
Lizards as sentinels for the distribution of Angiostrongylus cantonensis