Angiostronglyus vasorum lives in the heart and in the blood vessels of the lungs of dogs (Elsheikha et al. 2014). Strictly speaking it is a heartworm; it is also known as ‘French heartworm’ because the parasite was first isolated in France. However, because infection commonly causes respiratory signs it is widely known as ‘lungworm’. Crenosoma vulpis and Oslerus osleri are other lungworms that affect dogs in the UK. They are considered ‘true’ lungworms because they live in the bronchi. None of these lungworms, including A. vasorum, has zoonotic potential.
A. vasorum has an indirect life cycle involving molluscs (see the slideshows below). Dogs become infected when they ingest slugs and snails containing L3 stage larvae (Elsheikha et al. 2014). Recent data (not yet fully published) have reported that L3 larvae are deposited in the faeces of Limax maximus slugs (Conboy et al 2016 - conference abstract). However, it has not been proven that dogs can become infected through contact with slug or snail faeces or slime trails.
Lifecycle of A. vasorum: overall
Lifecycle of A. vasorum: in the dog
The time from when a dog becomes infected to when L1 larvae are released in faeces (the pre-patent period) is usually about 38–57 days (around 5–8 weeks); however, it can range widely from 28 to 108 days (4–15 weeks) (Elsheikha et al. 2014). The pre-patent period is relevant to diagnostic testing and the frequency of preventive therapy.
Infection with A. vasorum can cause a wide range of clinical signs and may lead to various clinical outcomes. These depend on the level of worm burden, the age and immune response of the infected animal, and concomitant illnesses and blood coagulation status. Respiratory signs are the most common clinical manifestation. The course of A. vasorum infection is often subtle and chronic, and dogs may show coughing, anorexia, weight loss, emaciation, and signs of pulmonary hypertension. Acutely affected dogs may show one or more of the following signs: coughing, dyspnoea, anaemia, depression, pyrexia and anorexia. Signs of bleeding disorders, such as haemoptysis, melaena, prolonged bleeding from minor injuries, and occasionally subcutaneous haematomas, are less frequent, but can be fatal (Elsheikha et al. 2014). How or why the infection causes bleeding disorders is not fully understood (Elsheikha et al. 2014). In severe infections, right-sided heart failure and sudden death may occur. Although most of the pathologies occur in the lungs, the larvae and, rarely, adult worms can reach ectopic locations, such as the brain, bladder, kidney or the eye, further complicating the clinical presentation and the pathological findings. Making a clinical diagnosis of angiostrongylosis is difficult due to the heterogeneous clinical presentation and variations in severity. This means the disease can go undetected.
A. vasorum is not notifiable and so there are no accurate figures for confirmed clinical cases or deaths in the UK. The mortality rate has been reported as 12.5% (3 out of 24 dogs) (Koch & Willesen, 2009) and 13% (3 out of 23) (Chapman et al. 2004). However, both these figures are from referral hospitals and so the rates are likely to be higher than in general practice.
There is no defined set of risk factors that can be used to guide selective screening. There is also no ideal method for diagnosis of canine angiostrongylosis and it is important to understand the limitations of the available diagnostic tests.
Tests to visibly detect larvae: Faecal detection of L1 larvae using the Baermann technique is the method most commonly used to diagnose A. vasorum infection. This test cannot detect infection during the pre-patent period (i.e. the first 4 to 15 weeks). It also has low sensitivity (detection rate) if performed on a single faecal sample because larvae may be present in low numbers and are shed intermittently (Elsheikha et al. 2014). Sensitivity is improved by collecting faecal specimens over 3 consecutive days. Larvae can also be detected in bronchoalveolar lavage samples, but this method carries risks, especially in dyspnoeic patients.
Tests to detect parasite antigens: Circulating parasite antigens can be detected in the blood using a laboratory-based sandwich ELISA assay or a point-of-care, in-clinic, antigen detection kit (IDEXX Angio Detect Test) (Elsheikha et al. 2014; Schnyder et al. 2014). Both test for parasite antigens at the same life-cycle stage and both have 100% specificity (zero false-positive rate). In a comparative trial, the sandwich ELISA test had a sensitivity of 94.9% compared to 84.6% for the Angio Detect Test (relative to the Baermann test which was used as the standard) (Schnyder et al. 2014). Seropositivity with both tests increases with time from infection. The sandwich ELISA test detected parasite antigens in some dogs at 5 weeks after infection and in all infected dogs at 11 weeks. Whereas the Angio Detect Test detected parasite antigens in some dogs from 9 weeks after infection and in all dogs at 14 weeks. The 3 to 4 week delay in detection of infection by the Angio Detect Test is considered to have minimal impact on the prevention of death on the basis that fatal coagulopathies have not occurred in experimentally-infected dogs until 13 weeks after infection (Schnyder et al. 2014; Schnyder et al. 2010).
Practical points: A negative Angio Detect Test result alone should not be used to rule out angiostrongylosis, because a recently-infected dog may test negative despite showing clinical signs. Therefore, when there is a high clinical suspicion of lungworm infection, the test should be repeated 1 month later. The Baermann test can help achieve definitive diagnosis of A. vasorum infection.
The parasite is growing in importance because of its geographical spread both in endemic regions and areas previously free of infection in the UK and in Europe (Morgan et al. 2008; Elsheikha et al. 2014). A. vasorum is thought to have first reached Great Britain in the mid 1970s via a greyhound imported from Ireland (Jacobs and Prole 1975). Originally, hotspots were detected in southern parts of England and Wales, but it is now being found in northern England and Scotland (Philbey 2013; Yamakawa et al. 2009; Helm et al. 2009).
Three main factors are thought to be contributing to the spread:
- the growing urbanisation of foxes (the main reservoir host);
- warmer and wetter winters allowing more slugs and snails to survive;
- a rise in the movement of dogs around the UK.
Paratenic hosts (amphibians), intermediate hosts (slugs and snails) and reservoir hosts (foxes and other carnivores) can potentially disperse dog lungworm across large geographic areas. This has prompted research investigating, for instance, the correlation between the spatial distribution of the mollusc vectors and infection in dogs (Aziz et al. 2016). More studies are still needed to determine the contribution of these and other hosts to the spread of A. vasorum. It is possible that increased awareness of the parasite in the veterinary profession and the improved availability and standards of diagnostic testing might also be contributing to the apparent spread of the parasite. Conversely, the lower reported prevalence in Scotland and northern England (Morgan et al. 2010) might be due to a lack of awareness rather than true low prevalence (Di Cesare et al. 2015). The lack of evidence of A. vasorum in any region does not prove its absence, and so geographic location should not be used as the only criterion for suspecting or excluding diagnosis.
Once correctly diagnosed, treatment of angiostrongylosis requires prompt anthelmintic therapy with a macrocyclic lactone (milbemycin or moxidectin), or fenbendazole (unlicensed use). There are very few published trials assessing the efficacy of these drugs in the treatment of canine angiostrongylosis. The quality of published evidence is higher for moxidectin and fenbendazole (a randomised controlled trial) than for milbemycin (an uncontrolled study). Details of the studies are given below. Milbemycin and moxidectin are only available as combination products in the UK (see the table).
While anthelmintic therapy is the most important aspect in the treatment of angiostrongylosis, management of the associated clinical signs plays a vital role in recovery, especially in severe cases. Supportive care depends on the presence and severity of clinical signs (Elsheikha et al. 2014). For example, antibacterial and corticosteroid therapy have been used in severe cases, and bronchodilators and/or diuretics are used to control severe dyspnoea and ascites that may occur after treatment (Koch & Willesen 2009). Anaphylactic shock reported following treatment of angiostrongylosis (with the anthelmintic levamisole) is thought to be due to the sudden release of worm antigens after rapid killing of the worms (Søland & Bolt 1996).
Clinical trials of angiostrongylosis treatment
Moxidectin vs. fenbendazole
In a randomised controlled trial, 50 naturally-infected dogs (from 25 breeds) were treated with moxidectin + imidacloprid (a single dose of 0.1 ml/kg moxidectin 2.5% + imidacloprid 10% spot-on solution) or fenbendazole (25 mg/kg orally for 20 days) (Willesen et al. 2007). There was no significant difference in efficacy between the two treatments: faecal L1 larvae were absent in 85.2% of dogs on moxidectin + imidacloprid vs. 91.3% of those on fenbendazole and there was similar improvement in lung pathology in the two groups. Adverse effects (most commonly diarrhoea and vomiting) were seen in 11 of the 27 dogs on moxidectin + imidacloprid; one dog developed intracranial haemorrhage and was euthanised soon after treatment. Adverse effects (all gastrointestinal signs) were reported in 8 of the 23 dogs treated with fenbendazole (Willesen et al. 2007).
An uncontrolled study assessed milbemycin in naturally-infected dogs in veterinary practices in Canada. (Conboy 2004). The 16 dogs had chronic cough and dyspnoea and/or exercise intolerance and A. vasorum larvae were detected in the faeces. Milbemycin (0.5mg/kg) stopped larval shedding in 14 dogs (87.5%). Of these, three were initially treated with two single doses 1 week apart, but faecal samples taken 48–70 days later remained positive for A. vasorum, prompting a change in the protocol to four single doses one week apart. One dog (co-infected with Crenosoma vulpis) died after receiving the first treatment (attributed to congestive heart failure) but it is unknown whether this was drug-induced or related to the infection.
Anthelmintics can be used to disrupt the life cycle of A. vasorum, so reducing environmental contamination with infective larvae and preventing the development of clinical disease. Judging the need to use preventive therapy is a balance between the risk of angiostrongylosis and the risk of drug resistance and the adverse effects of drug therapy. (See module 3 of the Parasiticides series for more on strategies for parasiticide use). If a dog is judged to be at high risk of infection, it is reasonable to use regular anthelmintic therapy to prevent the development of clinical angiostrongylosis. And, as intermediate and paratenic hosts of A. vasorum are widespread and may be present in the environment throughout the year, it seems rational to consider all-year-round control. However, if there is little risk of infection, regular preventive therapy may be considered unnecessary. Veterinary professionals need to keep up to date with information about the lungworms that might affect dogs visiting their practices, so that they can provide appropriate advice to clients. Practices should check for regular updates on parasite distribution from ESCCAP UK& Ireland. Maps created by Bayer Animal Health (which markets anthelmintics) and IDEXX Laboratories (which markets the Angio Detect Test) can be used to check for reported cases of A. vasorum infection in the UK.
Before prescribing preventive anthelmintic therapy, a full parasite risk assessment is needed (see module 3 of the Parasiticide series for more on risk assessment). With respect to A. vasorum, this involves considering the following:
aspects of the dog’s lifestyle that might bring it into contact with slugs, snails and paratenic hosts (e.g. time spent outdoors; hunting; consumption of slugs or snails, or grass that might contain these)
likelihood of travel (especially to known endemic areas)
history of A. vasorum infection; previously infected dogs remain susceptible to infection and past infection may be a risk factor for repeated exposure.
There is some evidence suggesting purebred dogs (in particular, Cavalier King Charles Spaniels and Staffordshire Bull Terriers (Chapman et al. 2004) are at a higher risk of infection than crossbreeds. More research is needed to investigate a possible hereditary susceptibility in these breeds. Younger dogs may be at higher risk because their exploratory behaviour may bring them into contact with slugs and snails.
Milbemycin and moxidectin (in combination products) have been shown to prevent the development of adult worms and lung pathology in dogs experimentally infected with A. vasorum (see below for details of the trials). However, not all products containing the drugs are licensed for prevention (see the table). The dose instructions for the licensed products recommends monthly administration. This is logical, given that the pre-patent period can be as short as 28 days. There is no evidence that less frequent administration with these drugs prevents angiostrongylosis. The slightly different wording in the licensed indications of the milbemcyin + praziquantel and moxidectin + imidacloprid products (see the table) is unlikely to reflect a real difference in clinical efficacy; the combinations have not been compared directly in published clinical trials. In any case, the need for protection against other parasites, the formulation, contraindications, adverse effects and drug interactions are all important determinants in the choice of product. For more on choice of product, see modules 3 and 6 of the Veterinary Prescriber Parasiticides series.
Published trials of preventive therapy
A randomised, “partially-blinded” placebo-controlled trial evaluated the efficacy of milbemycin + spinosad tablets in the prevention on angiostrongylosis (Böhm et al. 2014). Sixteen healthy beagle dogs were inoculated with A. vasorum and treated 30 days later with a single dose of milbemycin + spinosad (milbemycin at a dose of 0.75–1.0 mg/kg) or placebo. The combination reduced the number of adult worms recovered at necropsy by 98.8% compared with placebo (p<0.0001), and also prevented faecal shedding of larvae and substantially prevented lung pathology. This drug combination is not marketed in the UK.
A randomised trial evaluated the efficacy of milbemycin + afoxolaner (Nexgard Spectra) (Lebon et al. 2016). Twenty healthy beagles were inoculated with larvae from infected snails and randomised to monthly treatment with milbemycin + afoxolaner (dose of milbemycin 0.5mg/kg) or no treatment, for 4 months. The combination reduced the number of adult worms recovered at necropsy by 94.9% (p<0.0001) and also reduced faecal shedding of larvae by 99.9% (p<0.0001) and substantially prevented lung pathology.
We could find no published trials assessing milbemycin + praziquantel.
A blinded randomised controlled trial evaluated the efficacy of moxidectin + imidacloprid in 24 healthy beagle dogs inoculated with larvae from infected snails. The dogs were randomised to no treatment, or to treatment with a single dose of moxidectin + imidacloprid spot-on ([Advocate] dose of moxidectin 2.5mg/kg) either 4 days or 32 days after inoculation (Schnyder et al. 2009). Compared to no treatment, moxidectin + imidacloprid in both treatment groups reduced the number of adult worms in the lung by 100% (p<0.0001) and also reduced larval shedding by 100% and substantially prevented lung pathology. The researchers found that dogs in the group that received later treatment (32 days after inoculation) had more signs of lung pathology than those treated earlier, although no parasites were detected in the lungs of dogs in either group. They interpreted this finding as being due to larvae being allowed to develop to immature L5 and young adult stages in the later-treated dogs and causing lung damage.
UK products containing fenbendazole, milbemycin or moxidectin
All are POM-V, except fenbendazole products
*as reported in the SPCs. Very common – more than 1 in 10 dogs; common - up to 1 in 10 dogs; uncommon - up to 1 in 100 dogs; Rare - up to 1 dog in 1000; Very rare - up to 1 dog in 10,000
The lungworm Angiostrongylus vasorum can cause serious disease, including death, in dogs. This parasite is becoming more widespread in the UK. Veterinary professionals need to keep up to date with information about the distribution of A. vasorum so that they can provide appropriate advice to clients. Dogs become infected with A. vasorum when they ingest slugs and snails containing L3 stage larvae. It can be difficult to make a clinical diagnosis of angiostrongylosis because of the heterogeneous clinical presentation and variations in severity and so the disease can go undetected. The absence of reports of A. vasorum locally does not mean it should be discounted at diagnosis. Once correctly diagnosed, treatment of angiostrongylosis requires anthelmintic therapy with a macrocyclic lactone (milbemycin or moxidectin), or fenbendazole (unlicensed use). If a dog is judged to be at high risk of infection, it is reasonable to use regular anthelmintic therapy to prevent the development of clinical angiostrongylosis. Products containing milbemycin and moxidectin have been shown to prevent the development of adult worms and lung pathology in dogs experimentally infected with A. vasorum. Before prescribing any preventive anthelmintic therapy, a full parasite risk assessment is needed.
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Goal of activity: Update knowledge; help clinical decision-making
Authors/disclosures: Veterinary Prescriber editorial team/no conflict of interest
Specific learning objectives: to improve knowledge and understanding of lungworm (Angiostrongylosis vasorum) infection in dogs; to be able to discuss confidently the risks with clients and reach an informed decision about preventive therapy.
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How we produced this module
Our modules start with a detailed outline and electronic literature search. We commission a collaborating author, who is a specialist in the module topic, to write a draft module. The collaborating author on this module was Hany Elsheikha. The draft is circulated unsigned to a wide range of commentators, include practising first-opinion vets, other topic specialists, the companies that market any mentioned drugs and other organisations and individuals, as appropriate. They can raise points about the interpretation of evidence, ask questions that are important to clinical practice, and present alternative viewpoints. There is a rigorous editing and checking process and the result is a module that is evidence-based, impartial and relevant to clinical practice. The final module is unsigned because it is the result of collaboration. References
Aziz NA et al. Distribution of Angiostrongylus vasorum and its gastropod intermediate hosts along the rural-urban gradient in two cities in the United Kingdom, using real time PCR. Parasit Vectors 2016; 9: 56.
Conboy G et al. Gastropod shedding of third-stage larvae after infection of metastrongyloid lungworms. Parasites Vectors 2016; 10 (Suppl 1): A38.
Morgan ER et al. Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Vet Parasitol 2008;154: 48–57.
Schnyder M et al. Seroepidemiological survey for canine angiostrongylosis in dogs from Germany and the UK using combined detection of Angiostrongylus vasorum antigen and specific antibodies. Parasitology 2013; 140: 1442–50.
Søland J, Bolt G. Hypovolaemic shock after anthelmintic treatment of canine angiostrongylosis. J Small Anim Pract 1996; 37: 594–6.
Willesen JL et al. Efficacy and safety of imidacloprid/moxidectin spot-on solution and fenbendazole in the treatment of dogs naturally infected with Angiostrongylus vasorum (Baillet, 1866). Vet Parasitol 2007; 147: 258–64.
Yamakawa Y et al. Emerging canine angiostrongylosis in northern England: five fatal cases. Vet Rec 2009; 164: 149–52.