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Editorial
Slugs and Angiostrongylus vasorum – how much do we know?
  1. M. Schnyder, Dr Med Vet, DiplEVPC
  1. Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland e-mail: manuela.schnyder{at}uzh.ch

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THE numerous case reports, prevalence studies and clinical surveys published in the past few decades confirm the international success of Angiostrongylus vasorum. Accordingly, in the UK, its spread from single endemic spots in Cornwall (Martin and Neal 1992) and south Wales (Patteson and others 1993) to wider areas in southern (Blehaut and others 2014) and northern England (Yamakawa and others 2009) has been documented. The reasons for the apparent success of this parasite are attributed to a multitude of factors, including changes in the population of intermediate and final hosts, increased disease awareness and better diagnostic tools. Due to the broad range of clinical manifestations (Koch and Willesen 2009), and the challenge to diagnose this parasite before dogs die of a parasitosis that could be treated with appropriate anthelmintics, information about the occurrence of A vasorum is important.

The first endemic case in a dog in Scotland was described in 2009 (Helm and others 2009). A study by Helm and colleagues (2015), summarised on p 46 of this issue of Veterinary Record, reports on the occurrence of A vasorum in slugs. Of the intermediate hosts collected in three defined areas around Glasgow, 6.7 per cent were positive for A vasorum DNA. The prevalence was highest in the area of the so-called index case, with gastropod species in the Arionidae, Limacidae and Milacidae families being positive for A vasorum. This indicates that active transmission of A vasorum has persisted over time in this focal area. In addition, positive snails were collected from a park where clinically suspected dogs were walked and had been reported, and, more surprisingly, also from a park which was used as a negative control. Large arionid specimens, which were abundant in all investigated areas, were hypothesised to play an important role in the emergence of A vasorum in dogs. Morgan (2014) discussed the highly patchy occurrence of A vasorum hotspots and questioned the reasons behind their heterogeneity. The restricted activity range of intermediate hosts, compared to final hosts, suggests that surveys like that of Helm and colleagues (2015) can identify local hot spots.

A focus of infected slugs without dog cases accounts for a role of wild canids in the spread of A vasorum. Little is known about larval excretion by foxes, but in dogs the parasite has a very high reproductive potential. Previous trials have shown that dogs can excrete up to 17,000 larvae (L1) per gram of faeces (Schnyder and others 2010). Therefore, a single slug feeding on such faeces can become heavily infected. Thus, it can hypothesised that the ingestion of a single infected slug by a dog may result in clinical angiostrongylosis that would be noticed by the owner or vet. Under field conditions, the number of L1 acquired by a slug (and the number of slugs ingested by the final hosts) cannot be determined. Nevertheless, the coprophagic behaviour of some Arionidae species (Boschi 2011) together with their large size can result in higher larval burdens (Patel and others 2014), confirming their importance (Helm and others 2015).

Alternatively, since dog owners often walk the same paths, repeated contact with a population of gastropods harbouring low numbers of infectious stages (L3) A vasorum could be possible. Little is known about protective immunity in dogs infected with A vasorum and how this might prevent the development of L3 A vasorum to L4 and adults stages. Adult parasites can survive for up to five years (Guilhon and Cens 1973), and it has been shown that larval excretion in re-infected dogs persisted (Oliveira-Junior and others 2006). Consequently, at the time of diagnosis, it is not known how many adult parasites dogs are harbouring and if they originated from one or more slugs. When considering dogs, some animals such as young or hunting dogs seem to be more prone to infection (Conboy 2004, Morgan and others 2010). Not all dog owners report ingestion of slugs by their dogs and accidental ingestion, ie, when eating grass for digestion purposes, is more probable. Dogs also have the habit of carrying sticks and we have observed, while searching for snails, that some sticks were covered in slugs, representing a risk associated with dog behaviour. Also the free-living L3 should not be forgotten (Barçante and others 2003); these could be ingested when drinking from puddles.

Angiostrongylus vasorum appears to have spread, but how much do we know about its epidemiology?

The lack of detection of A vasorum-positive dogs from some of the positive gastropod areas led Helm and others (2015) to discuss their relatively low number of analysed samples and the sensitivity and specificity of the adopted diagnostic methods. Diagnostic tools are inherently more sensitive in cases of heavier infections. Furthermore, patency and worm survival vary considerably in dogs, and the mechanisms limiting survival are not known. Single dogs may get rid of their worms for unknown reasons, independent of anthelmintic treatment (Schnyder and others 2015). We also do not know if the use of some active components may (temporarily) suppress production of L1, as described for Dirofilaria immitis infection and microfilarial production (McCall and others 2008). For these reasons, Baermann analysis is recommended to be undertaken with faeces collected over three days, in order to overcome apparent intermittent excretion. When considering serology, antibodies can be detected during a prepatent A vasorum infection, while antigen detection starts in parallel with larval excretion. With longer duration of infections, more consistent results are observed with both serological methods than with Baermann analysis or PCR performed with blood, faecal or tracheal swabs (Schnyder and others 2015). Diagnostic tools have to be chosen according to the clinical scenario, and, if relevant, as suggested by Helm and others (2015), according to the study objectives. The commercially available in-clinic antigen detection test is particularly recommended for clinically suspected dogs with infections persisting for at least nine weeks (Schnyder and others 2014).

Gastropod infection can be analysed by PCR methods or by microscopy after tissue digestion. Both methods require time for collection and species identification, followed by labour intensive work, but have been able to detect A vasorum (Ferdushy and others 2009, Patel and others 2014, Helm and others 2015), demonstrating local endemicity. Importantly, Helm and others (2015) showed that different gastropod species and prevalences are observed, even in nearby areas. Seasonality, meteorological conditions and time of the day can additionally affect slug collection and corresponding prevalence data. The results do not allow conclusions to be drawn about final hosts, since dogs and foxes could shed equivalent numbers of L1. Road kills or hunted foxes have been investigated for A vasorum occurrence and prevalences observed in foxes are usually higher than those in dogs (Koch and Willesen 2009), suggesting that colonisation of urban habitats by foxes favours the transmission of parasites to companion animals and people (Liccioli and others 2015). In contrast to foxes, dogs are generally presumed to be responsible for the long distance dispersal of A vasorum, which is facilitated, among others, by the free movement of dogs within Europe (Bourne and others 2015).

If large epidemiological surveys in final hosts help to clarify the occurrence of A vasorum on a wide scale, gastropod investigations are instructive at a local level and contribute to solving the tricky jigsaw puzzle that is A vasorum transmission. Both procedures are important in identifying areas suitable for A vasorum establishment, and therefore for targeting appropriate information and disease awareness among veterinary practitioners and animal owners in those areas.

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