FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / PLoS One / Intermediate hosts of Angiostrongylus cantonensis in Tenerif...
PloS one2015; 10(3); e0120686; doi: 10.1371/journal.pone.0120686

Intermediate hosts of Angiostrongylus cantonensis in Tenerife, Spain.

Abstract: The nematode Angiostrongylus cantonensis is the causative agent of human angiostrongyliasis, the main clinical manifestation of which is eosinophilic meningitis. Although this parasite has been found recently in its definitive rat host in Tenerife (Canary Islands, Spain), showing a widespread distribution over the north-east part of the island, there are no available data regarding which snail and/or slug species are acting as intermediate hosts on this island. Consequently, the objective of this work was to determine the possible role of three mollusc species, Plutonia lamarckii, Cornu aspersum and Theba pisana, as intermediate hosts of A. cantonensis in Tenerife. Between 2011 and 2014, 233 molluscs were collected from five biotopes where rats had been found previously to harbor either adult worms or antibodies against A. cantonensis, and the identification was carried out on the basis of morphological features and a LAMP technique. The prevalence of A. cantonensis larvae in the mollusc samples, based on morphological identification, was 19.3%, whereas 59 out of the 98 individuals (60.2%) analyzed by LAMP were positive. Positive results were obtained for the three mollusc species analyzed and two of the positive samples, both obtained from P. lamarckii, were confirmed as positive by 18S rRNA and ITS1 PCR. Sequence analysis of 18S rRNA PCR products showed 100% similarity with previously published A. cantonensis sequences. These results may be relevant from a public health point of view, since all the biotopes from which the samples were obtained were in inhabited areas or areas with human activity, but it is also important from the perspective of a possible transmission to other accidental hosts, such as dogs and horses, animals that are present in some of the areas analyzed.
Get Full Text
Publication Date: 2015-03-24 PubMed ID: 25803658PubMed Central: PMC4372438DOI: 10.1371/journal.pone.0120686Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research investigates the possible intermediate hosts of Angiostrongylus cantonensis, a nematode causing human angiostrongyliasis, in Tenerife, Spain. The molluscs Plutonia lamarckii, Cornu aspersum, and Theba pisana were found to carry the parasite, posing a potential risk for both humans and animals.

Background of the Study

  • The study revolves around a nematode, Angiostrongylus cantonensis, which is known to cause a disease in humans known as angiostrongyliasis. The primary clinical symptom of this malady is eosinophilic meningitis.
  • The definitive host of this parasite is the rat. Recently, this parasite was discovered in its rat host in Tenerife (Canary Islands, Spain), especially throughout the north-east portion of the island. However, there is no existing data regarding which snail and/or slug species act as intermediate hosts on this island.
  • The study’s aim was to explore the potential role of three mollusc species – Plutonia lamarckii, Cornu aspersum, and Theba pisana – as intermediate hosts of A. cantonensis in Tenerife.

Methodology

  • From 2011 to 2014, 233 molluscs were extracted from five biotopes where rats carrying either adult worms or antibodies against A. cantonensis, had previously been discovered.
  • Identification of these molluscs was carried out based on morphological features and a Loop-Mediated Isothermal Amplification (LAMP) technique.

Results and Findings

  • The prevalence of the A. cantonensis larvae in the mollusc samples, based on morphological identification, was noted at 19.3%, while LAMP analysis showed a 60.2% positivity rate (59 out of the 98 individuals).
  • All three mollusc species tested positive for A. cantonensis based on the LAMP method, with two positive samples from P. lamarckii confirmed as positive by 18S rRNA and ITS1 PCR testing.
  • Sequence analysis of the 18S rRNA PCR products showcased a 100% similarity with published A. cantonensis sequences in the past.
  • The study’s results carry major public health implications as all the biotopes from which the samples were taken were in inhabited areas or locations with human activity. Moreover, there is also the possibility of indirect transmission to accidental hosts like dogs and horses that are present in some of the surveyed areas.

Cite This Article

APA
Martin-Alonso A, Abreu-Yanes E, Feliu C, Mas-Coma S, Bargues MD, Valladares B, Foronda P. (2015). Intermediate hosts of Angiostrongylus cantonensis in Tenerife, Spain. PLoS One, 10(3), e0120686. https://doi.org/10.1371/journal.pone.0120686

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 10
Issue: 3
Pages: e0120686

Researcher Affiliations

Martin-Alonso, Aarón
  • Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de la Laguna, La Laguna, Islas Canarias, España.
Abreu-Yanes, Estefanía
  • Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de la Laguna, La Laguna, Islas Canarias, España.
Feliu, Carlos
  • Departamento de Microbiología y Parasitología, Universidad de Barcelona, Barcelona, Cataluña, España.
Mas-Coma, Santiago
  • Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Burjassot, Spain.
Bargues, María Dolores
  • Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Burjassot, Spain.
Valladares, Basilio
  • Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de la Laguna, La Laguna, Islas Canarias, España.
Foronda, Pilar
  • Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias, Universidad de la Laguna, La Laguna, Islas Canarias, España.

MeSH Terms

  • Angiostrongylus cantonensis / genetics
  • Angiostrongylus cantonensis / isolation & purification
  • Angiostrongylus cantonensis / ultrastructure
  • Animals
  • Gastropoda / parasitology
  • Humans
  • Larva / genetics
  • Larva / ultrastructure
  • RNA, Helminth / genetics
  • RNA, Helminth / isolation & purification
  • Rats / parasitology
  • Snails / parasitology
  • Spain
  • Strongylida Infections / parasitology
  • Strongylida Infections / transmission

Conflict of Interest Statement

Competing Interests: The authors have declared that no competing interests exist.

References

This article includes 33 references
  1. Eamsobhana P, Yong HS. Immunological diagnosis of human angiostrongyliasis due to Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). Int J Infect Dis 2009;13: 425–431.
    doi: 10.1016/j.ijid.2008.09.021pubmed: 19117782google scholar: lookup
  2. Martin-Alonso A, Foronda P, Quispe-Ricalde MA, Feliu C, Valladares B. Seroprevalence of Angiostrongylus cantonensis in wild rodents from the Canary Islands. PloS ONE 2011;6: e27747.
    doi: 10.1371/journal.pone.0027747pmc: PMC3215735pubmed: 22110752google scholar: lookup
  3. Wang Q, Lai D, Zhu X, Chen X, Lun Z. Human angiostrongyliasis. Lancet Infect Dis 2008;8: 621–630.
    doi: 10.1016/S1473-3099(08)70229-9pubmed: 18922484google scholar: lookup
  4. Slom TJ, Cortese MM, Gerber SI, Jones RC, Holtz TH, Lopez AS. An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. N Engl J Med 2002;346: 668–675.
    pubmed: 11870244
  5. Yii CY. Clinical observations on eosinophilic meningitis and meningoencephalitis caused by Angiostrongylus cantonensis on Taiwan. Am J Trop Med Hyg 1976;25: 233–249.
    pubmed: 1259085
  6. Bowden DK. Eosinophilic meningitis in the New Hebrides: two outbreaks and two deaths. Am J Trop Med Hyg 1981;30: 1141–1143.
    pubmed: 6974509
  7. Chotmongkol V, Sawanyawisuth K. Clinical manifestations and outcome of patients with severe eosinophilic meningoencephalitis presumably caused by Angiostrongylus cantonensis. Southeast Asian J Trop Med Public Health 2002;33: 231–234.
    pubmed: 12236418
  8. Kim JR, Hayes KA, Yeung NW, Cowie RH. Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PloS ONE 2014;9: e94969.
    doi: 10.1371/journal.pone.0094969pmc: PMC4008484pubmed: 24788772google scholar: lookup
  9. Cowie RH. Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai'i J Med Public Health 2013;72 (Supplement 2): 6–9.
    pmc: PMC3689493pubmed: 23901372
  10. Kliks MM, Palumbo NE. Eosinophilic meningitis beyond the Pacific Basin: The global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Soc Sci Med 1992;34: 199–212.
    pubmed: 1738873
  11. Qvarnstrom Y, Bishop HS, da Silva AJ. Detection of rat lungworm in intermediate, definitive, and paratenic hosts obtained from environmental sources. Hawaii J Med Public Health 2013;72 (Supplement 2): 63.
    pmc: PMC3689491pubmed: 23901387
  12. Chen R, Tong Q, Zhang Y, Lou D, Kong Q, Lv S. Loop-mediated isothermal amplification: rapid detection of Angiostrongylus cantonensis infection in Pomacea canaliculata. Parasit Vectors 2011;4: 204.
    doi: 10.1186/1756-3305-4-204pmc: PMC3213046pubmed: 22023992google scholar: lookup
  13. Liu C, Song H, Zhang R, Chen M, Xu M, Ai L. Specific detection of Angiostrongylus cantonensis in the snail Achatina fulica using a loop-mediated isothermal amplification (LAMP) assay. Mol Cell Probes 2011;25: 164–167.
    doi: 10.1016/j.mcp.2011.04.002pubmed: 21515360google scholar: lookup
  14. Foronda P, López-González M, Miquel J, Torres J, Segovia M, Abreu-Acosta N. Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Trop 2010;114: 123–127.
    doi: 10.1016/j.actatropica.2010.02.004pubmed: 20153283google scholar: lookup
  15. Groh K, Garcıa A. Phylum Mollusca In: Izquierdo I, Martín JL, Zurita N, Arechavaleta M, editors. Lista de especies silvestres de Canarias (hongos, plantas y animales terrestres). Tenerife: Consejería de Medio Ambiente y Ordenación Territorial. Gobierno de Canarias; 2004. pp. 149–154.
  16. Ash LR. Diagnostic morphology of the third-stage larvae of Angiostrongylus cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, and Anafilaroides rostratus (Nematoda: Metastrongyloidea). J Parasitol 1970;56: 249–253.
    pubmed: 5445821
  17. López C, Clemente S, Almeida C, Brito A, Hernández M. A genetic approach to the origin of Millepora sp. in the eastern Atlantic. Coral Reefs 2014.
    doi: 10.1007/s00338-015-1260-8google scholar: lookup
  18. Carreno RA, Nadler SA. Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. J Parasitol 2003;89: 965–973.
    pubmed: 14627145
  19. Qvarnstrom Y, da Silva AC, Teem JL, Hollingsworth R, Bishop H, Graeff-Teixeira C. 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.00546-10pmc: PMC2916500pubmed: 20543049google scholar: lookup
  20. Qvarnstrom Y, Sullivan JJ, Bishop HS, Hollingsworth R, da Silva AJ. PCR-based detection of Angiostrongylus cantonensis in tissue and mucus secretions from molluscan hosts. Appl Environ Microbiol 2007;73: 1415–1419.
    pmc: PMC1828786pubmed: 17194836
  21. Teem JL, Qvarnstrom Y, Bishop HS, da Silva AJ, Carter J, White-McLean J. The occurrence of the rat lungworm, Angiostrongylus cantonensis, in nonindigenous snails in the Gulf of Mexico region of the United States. Hawaii J Med Public Health 2013;72: 11.
    pmc: PMC3689474pubmed: 23901374
  22. Yen CM, Chen ER, Cheng CW. A survey of Ampullarium canaliculatus for natural infection of Angiostrongylus cantonensis in south Taiwan. J Trop Med Hyg 1990;93: 347–350.
    pubmed: 2231842
  23. Chen D, Zhang Y, Shen H, Wei Y, Huang D, Tan Q. Epidemiological survey of Angiostrongylus cantonensis in the west-central region of Guangdong Province, China. Parasitol Res 2011;109: 305–314.
    doi: 10.1007/s00436-011-2255-1pubmed: 21301874google scholar: lookup
  24. Hausdorf B. Phylogeny and biogeography of the Vitrinidae (Gastropoda: Stylommatophora). Zool J Linn Soc 2002;134: 347–358.
  25. Delgado JD, Arévalo JR, Fernández‐Palacios JM. Road and topography effects on invasion: Edge effects in rat foraging patterns in two oceanic island forests (Tenerife, Canary Islands). Ecography 2001;24: 539–546.
  26. Alicata JE. Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Adv Parasitol 1965;3: 223–248.
    pubmed: 5334821
  27. Prociv P, Carlisle MS. The spread of Angiostrongylus cantonensis in Australia. Southeast Asian J Trop Med Public Health 2001;32 (Supplement 2): 126–128.
    pubmed: 12041575
  28. Johnson MS. Founder effects and geographic variation in the land snail Theba pisana. Heredity 1988;61: 133–142.
  29. Nicolai A. The impact of diet treatment on reproduction and thermophysiological processes in the land snails Cornu aspersum and Helix pomatia. M. Sc. Thesis, The University of Sheffield. 2010. Available: https://hal.archives-ouvertes.fr/file/index/docid/525296/filename/These_Annegret_Nicolai2010.pdf. Accessed 2015 March 5.
  30. Thekisoe OM, Kuboki N, Nambota A, Fujisaki K, Sugimoto C, Igarashi I. Species-specific loop-mediated isothermal amplification (LAMP) for diagnosis of trypanosomosis. Acta Trop 2007;102: 182–189.
    pubmed: 17574198
  31. Lunn JA, Lee R, Smaller J, MacKay BM, King T, Hunt GB. Twenty two cases of canine neural angiostrongylosis in eastern Australia (2002–2005) and a review of the literature. Parasit Vectors 2012;70: 1–18.
    pmc: PMC3361490pubmed: 22480148
  32. Eamsobhana P. The rat lungworm Parastrongylus (= Angiostrongylus) cantonensis: parasitology, immunology, eosinophilic meningitis, epidemiology and laboratory diagnosis. Bangkok: Wankaew (IQ) Book Center; 2006.
  33. Cowie RH. Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawai'i J Med Public Health 2013;72 (Supplement 2): 70–74.
    pmc: PMC3689478pubmed: 23901388
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.