Skip to main content
Log in

Molecular identification of novel intermediate host species of Angiostrongylus vasorum in Greater London

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Angiostrongylus vasorum is a parasitic nematode that can cause serious and potentially fatal disease in dogs and other canids. The aim of this study was to determine the intermediate slug species infected in nature by sampling sites in Greater London and Hertfordshire located within a known hyperendemic region. Overall, A. vasorum larvae were recovered from 6/381 slugs (1.6 %) by tissue digestion, and their identity was confirmed by PCR. Infected slugs originated from three different sites in the Greater London area: one in Waltham Forest and two in Bromley. Slugs parasitised by A. vasorum were identified by a combination of external morphological characteristics and molecular techniques and belonged to three different families: the Arionidae, the Milacidae and the Limacidae. This includes two new host records for the parasite: Arion distinctus and Tandonia sowerbyi. This is the first record of A. vasorum in the family Milacidae, indicating that the parasite has a broader intermediate host range than previously recognised.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson R (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. J Conchol 38:607–637

    Google Scholar 

  • Backeljau T, Van Beeck M (1986) Epiphallus anatomy in the Arion hortensis species aggregate (Mollusca, Pulmonata). Zool Scr 15:61–68. doi:10.1111/j.1463-6409.1986.tb00209.x

    Article  Google Scholar 

  • Barr NB, Cook A, Elder P, Molongoski J, Prasher D, Robinson DG (2009) Application of a DNA barcode using the 16S rRNA gene to diagnose pest Arion species in the USA. J Molluscan Stud 75:187–191. doi:10.1093/mollus/eyn047

    Article  Google Scholar 

  • Bolt G, Monrad J, Koch J, Jensen AL (1994) Canine angiostrongylosis: a review. Vet Rec 135:447–452. doi:10.1136/vr.135.19.447

    Article  CAS  PubMed  Google Scholar 

  • Borst A, Box ATA, Fluit AC (2004) False-positive results and contamination in nucleic acid amplification assays: suggestions for a prevent and destroy strategy. Eur J Clin Microbiol Infect Dis 23:289–299. doi:10.1007/s10096-004-1100-1

    Article  CAS  PubMed  Google Scholar 

  • Bourque A, Whitney H, Conboy G (2005) Angiostrongylus vasorum infection in a coyote (Canis latrans) from Newfoundland and Labrador, Canada. J Wildl Dis 41:816–819. doi:10.7589/0090-3558-41.4.816

    Article  PubMed  Google Scholar 

  • Cameron RAD, Eversham B, Jackson N (1983) A field key to the slugs of the British Isles. Field Stud 5:807–824

    Google Scholar 

  • Chapman PS, Boag AK, Guitian J, Boswood A (2004) Angiostrongylus vasorum infection in 23 dogs (1999–2002). J Small Anim Pract 45:435–440. doi:10.1111/j.1748-5827.2004.tb00261.x

    Article  CAS  PubMed  Google Scholar 

  • Chen D, Zhang Y, Shen H, Wei Y, Huang D, Tan Q, Lan X, Li Q, Chen Z, Li Z (2011) Epidemiological survey of Angiostrongylus cantonensis in the west-central region of Guangdong Province, China. Parasitol Res 109:305–314. doi:10.1007/s00436-011-2255-1

    Article  PubMed  Google Scholar 

  • Davies SM (1977) The Arion hortensis complex, with notes on A. intermedius Normand (Pulmonata: Arionidae). J Conchol 29:173–187

    Google Scholar 

  • Davies SM (1979) Segregates of the Arion hortensis complex (Pulmonata: Arionidae), with the description of a new species, Arion owenii. J Conchol 30:123–127

    Google Scholar 

  • De Winter AJ (1984) The Arion hortensis complex (Pulmonata: Arionidae): designation of types, descriptions, and distributional patterns, with special reference to the Netherlands. Zool Meded 59:1–17

    Google Scholar 

  • Dreijers E, Reise H, Hutchinson JMC (2013) Mating of the slugs Arion lusitanicus auct. non Mabille and A. rufus (L.): different genitalia and mating behaviours are incomplete barriers to interspecific sperm exchange. J Molluscan Stud 79:51–63. doi:10.1093/mollus/eys033

    Article  Google Scholar 

  • Eckert J, Lämmler G (1972) Angiostrongylose bei Mensch und Tier. Z Parasitenkd 39:303–322. doi:10.1007/BF00329093

    Article  CAS  PubMed  Google Scholar 

  • Ferdushy T, Kapel CMO, Webster P, Al-Sabi MNS, Grønvold J (2009) The occurrence of Angiostrongylus vasorum in terrestrial slugs from forests and parks in the Copenhagen area, Denmark. J Helminthol 83:379–383. doi:10.1017/S0022149X09377706

    Article  CAS  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Gasser RB, Chilton NB, Hoste H, Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21:2525–2526

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guilhon J, Cens B (1973) Angiostrongylus vasorum (Baillet, 1866). Etude biologique et morphologique. Ann Parasitol Hum Comp 48:567–596

    CAS  PubMed  Google Scholar 

  • Helm J, Gilleard JS, Jackson M, Redman E, Bell R (2009) A case of canine Angiostrongylus vasorum in Scotland confirmed by PCR and sequence analysis. J Small Anim Pract 50:255–259. doi:10.1111/j.1748-5827.2009.00741.x

    Article  CAS  PubMed  Google Scholar 

  • Jefferies R, Morgan ER, Shaw SE (2009) A SYBR green real-time PCR assay for the detection of the nematode Angiostrongylus vasorum in definitive and intermediate hosts. Vet Parasitol 166:112–118. doi:10.1016/j.vetpar.2009.07.042

    Article  CAS  PubMed  Google Scholar 

  • Jones GW, Neal C, Turner GR (1980) Angiostrongylus vasorum infection in dogs in Cornwall. Vet Rec 106:83

    Article  CAS  PubMed  Google Scholar 

  • Kirk L, Limon G, Guitian J, Hermosilla C, Fox M (2014) Angiostrongylus vasorum in United Kingdom mainland—a nationwide postal questionnaire survey of veterinary practices. Vet Rec 175:118. doi:10.1136/vr.102196

    Article  CAS  PubMed  Google Scholar 

  • Mc Donnell RJ, Paine TD, Stouthamer R, Gormally MJ, Harwood JD (2008) Molecular and morphological evidence for the occurrence of two new species of invasive slugs in Kentucky, Arion intermedius Normand and Arion hortensis Férussac (Arionidae: Stylommatophora). J Ky Acad Sci 69:117–123. doi:10.3101/1098-7096-69.2.117

    Google Scholar 

  • Morgan E, Shaw S (2010) Angiostrongylus vasorum infection in dogs: continuing spread and developments in diagnosis and treatment. J Small Anim Pract 51:616–621. doi:10.1111/j.1748-5827.2010.01000.x

    Article  CAS  PubMed  Google Scholar 

  • Morgan ER, Shaw SE, Brennan SF, De Waal TD, Jones BR, Mulcahy G (2005) Angiostrongylus vasorum: a real heartbreaker. Trends Parasitol 21:49–51. doi:10.1016/j.pt.2004.11.006

    Article  PubMed  Google Scholar 

  • Morgan ER, Tomlinson A, Hunter S, Nichols T, Roberts E, Fox MT, Taylor MA (2008) Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Vet Parasitol 154:48–57. doi:10.1016/j.vetpar.2008.02.030

    Article  CAS  PubMed  Google Scholar 

  • Morgan ER, Jefferies R, Krajewski M, Ward P, Shaw SE (2009) Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitol Int 58:406–410. doi:10.1016/j.parint.2009.08.003

    Article  PubMed  Google Scholar 

  • Patteson MW, Wotton PR, Lucke VM, Wright AI, Gibbs C (1987) Angiostrongylus vasorum in a terrier. Vet Rec 120:349

    Article  CAS  PubMed  Google Scholar 

  • Pfleger V, Chatfield J (1988) A guide to the snails of Britain and Europe. Hamlyn, London

    Google Scholar 

  • Roth S, Hatteland BA, Solhøy T (2012) Some notes on reproductive biology and mating behaviour of Arion vulgaris Moquin-Tandon 1855 in Norway including a mating experiment with a hybrid of Arion rufus (Linnaeus 1758) x ater (Linnaeus 1758). J Conchol 41:249–257

    Google Scholar 

  • Schnyder M, Fahrion A, Riond B, Ossent P, Webster P, Kranjc A, Glaus T, Deplazes P (2010) Clinical, laboratory and pathological findings in dogs experimentally infected with Angiostrongylus vasorum. Parasitol Res 107:1471–1480. doi:10.1007/s00436-010-2021-9

    Article  PubMed  Google Scholar 

  • Schnyder M, Schaper R, Bilbrough G, Morgan ER, Deplazes P (2013) Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 140:1442–1450. doi:10.1017/S0031182013001091

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Segovia JM, Torres J, Miquel J, Llaneza L, Feliu C (2001) Helminths in the wolf, Canis lupus, from north-western Spain. J Helminthol 75:183–192. doi:10.1079/JOH200152

    CAS  PubMed  Google Scholar 

  • Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597–608. doi:10.1017/s0031182098003448

    Article  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. doi:10.1038/msb.2011.75

    Article  PubMed Central  PubMed  Google Scholar 

  • Simpson VR, Neal C (1982) Angiostrongylus vasorum infection in dogs and slugs. Vet Rec 111:303–304

    Article  CAS  PubMed  Google Scholar 

  • Soroka M, Skujiene G (2011) Species identification of slugs of genus Arion Férussac, 1819 (Mollusca, Pulmonata) on the basis of genetics studies. Ekologija 57:70–80. doi:10.6001/ekologija.v57i2.1887

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taubert A, Pantchev N, Vrhovec MG, Bauer C, Hermosilla C (2009) Lungworm infections (Angiostrongylus vasorum, Crenosoma vulpis, Aelurostrongylus abstrusus) in dogs and cats in Germany and Denmark in 2003-2007. Vet Parasitol 159:175–180. doi:10.1016/j.vetpar.2008.10.005

    Article  PubMed  Google Scholar 

  • Trees AJ (1987) Angiostrongylus vasorum in dogs in Wales. Vet Rec 120:424

    Google Scholar 

  • Yamakawa Y, McGarry JW, Denk D, Dukes-McEwan J, Macdonald N, Mas A, McConnell F, Tatton B, Valentine EG, Wayne J, Williams JM, Hetzel U (2009) Emerging canine angiostrongylosis in northern England: five fatal cases. Vet Rec 164:149–152. doi:10.1136/vr.164.5.149

    Article  CAS  PubMed  Google Scholar 

  • Yousif F, Lämmler G (1975) The suitability of several aquatic snails as intermediate hosts for Angiostrongylus cantonensis. Z Parasitenkd 47:203–210. doi:10.1007/BF00418203

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214. doi:10.1089/10665270050081478

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Emma Wanostrocht for sample collection and The Royal Veterinary College for financial support (Royal Veterinary College manuscript number 715).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Christina Gill.

Additional information

Zainab Patel and A. Christina Gill contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patel, Z., Gill, A.C., Fox, M.T. et al. Molecular identification of novel intermediate host species of Angiostrongylus vasorum in Greater London. Parasitol Res 113, 4363–4369 (2014). https://doi.org/10.1007/s00436-014-4111-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4111-6

Keywords

Navigation