Edited November 2, 2015
The Lungworm disease guidelines were first published in the Journal of Feline Medicine and Surgery (2015) 17: 626-636 by Maria Grazia Pennisi et al., and edited by Karin Möstl.
Cardiopulmonary nematodes are emerging parasites of dogs and cats in Europe which have received growing attention by researchers in recent years.1,2,3,4 Significant progress has been made, mainly in the diagnosis and treatment of infection.
Aelurostrongylus abstrusus (Strongylida, Angiostrongylidae) is the best-known feline lungworm and is regarded as the most prevalent worldwide in domestic cats. Other lungworms in the cat include Oslerus rostratus, Troglostrongylus spp, Capillaria aerophila and Paragonimus spp.; A. abstrusus, O. rostratus and Troglostrongylus spp may cause mixed infections as they share the same intermediate and paratenic hosts.
Lungworm infections may be asymptomatic, or cause mild to severe respiratory signs due to bronchopneumonia, sometimes complicated by pleural effusion or pneumothorax (nasal discharge, tachypnoea, dyspnoea, coughing). The disease can be fatal.
Kittens may be vertically infected and develop a more severe disease at an early stage, due to the smaller diameter of the respiratory tracts and to their immature immune system.
It is advisable to investigate the presence of lungworm infestation in cases with right-sided heart disease associated with signs of pulmonary hypertension in outdoor cats. Uncared-for outdoor cats, such as those included in trap-neuter-release programs, are at higher risk for lungworms.
The Baerman migration method is considered the enrichment technique of choice, but takes 24 hours and false negatives may occur. The major limitation of copromicroscopy is the impossibility of diagnosis in the pre-patent period, which lasts about 1-2 months. A nested-PCR assay specific for A abstrusus has been validated.
Treatment options include fenbendazole paste, milbemycin oxime/praziquantel and various spot-on formulations (imidacloprid 10 % / moxidectin 1 %; emodepside 2.1 % / praziquantel 8.6 %; fipronil 8.3 % / (S)-methoprene 10 % / eprinomectin 0.4 % / praziquantel 8.3 %; or selectamin). In severe cases, broad-spectrum antibiotics should be given together with corticosteroids.
Capillaria aerophila has zoonotic potential and sporadic cases of human capillariosis have been described, causing a productive cough, haemoptysis and lung lesions.
Infection of the lower respiratory tract can be caused by a number of parasitic nematodes. Certain metastrongyloid worms are commonly defined as lungworms because the adult stage is located in the lungs of their hosts, but actually some trichuroids and flukes also live in the respiratory system.1,2,3,5 Aelurostrogylus abstrusus (Strongylida, Angiostrongylidae) is the most well-known feline lungworm and is regarded as the most prevalent in domestic cats. It is small (5-10 mm) and very narrow (less than 100 μm) and capable of colonising the respiratory bronchioles and alveolar ducts of domestic cats and other felids worldwide.2,6
Other respiratory mollusc-borne metastrongyloids are commonly reported at necropsy in wild felids but are considered rare in domestic cats. Oslerus rostratus (Strongylida, Filaroididae) exceeds 30-40 mm in length and infects the bronchial submucosa mainly in wild cats such as bobcats or in feral cats.5,7,8,9,10 Troglostrongylus spp (Strongylida, Crenosomatidae) is reported in many species of wild cats and occasionally in domestic cats;4,9,11,12,13,14 their length varies according to the species from about 10 to 25 mm and their width is up to 0.5 mm. They are located in the trachea and bronchi or even in bronchioles for the smallest species (T brevior).12,15
The trichuroid Capillaria aerophila (syn. Eucoleus aerophilus) has a low host-specificity and it is not uncommon in dogs and cats as well as wild carnivores.16 It is also a zoonotic parasite causing a potentially severe pulmonary disease in humans.17 C aerophila is found in the submucosa of the trachea, bronchi and bronchioles.2,16
Mixed infestations caused by respiratory nematodes are sometimes reported7,9,14,18,19,20 and both Troglostrongylus spp and Oslerus rostratus may be more prevalent than presumed in domestic cats since there is a risk that these infections are being misdiagnosed as A abstrusus because of morphometric similarities of their larval stages in faeces (L1).3,4
Paragonimus spp are lung flukes reported in many animals, including cats and humans, and some species are of zoonotic concern. Many species are found in cats, including P kellicotti, and 1-10 adults measuring 8-18 mm x 4-8 mm live in subpleural cysts or bullae.1
Life cycle and transmission
Aelurostrongylus abstrusus, O rostratus and Troglostrongylus spp all have an indirect life cycle involving terrestrial molluscs. Eggs of A abstrusus laid by female worms hatch in the respiratory tract and L1 larvae are coughed up, swallowed and eliminated in the environment with the faeces. They can actively enter slugs or snails where they moult into the infectious L3 stage.21,22,23,24 The biological cycle in the intermediate host is influenced by environmental temperature: a higher rate of larval development is observed at warmer temperatures.23 The L3 larvae are also found in a wide range of paratenic hosts (rat, mouse, lizard, frog, birds) commonly predated by cats.1,5,22 The ingestion of L3 by the cat is the most recognized means of transmission of lungworms but vertical transmission via the placenta or milk cannot be excluded, as adult egg-laying worms have been found in kittens as young as eight weeks of age.14 Experimental infestation demonstrated that egg production starts 4-6 weeks after infestation and may last for months, although it can be irregular.6,25,26,27,28
Vertical transmission of T brevior was recently observed in a queen and patent infection was detected in one-month old kittens.13,14,29 Troglostrongylus brevior and A abstrusus larvae may develop simultaneously in the same mollusc host (Helix aspersa) and overwinter for at least 120 days.24
C aerophila has a direct cycle and eggs laid by female worms in the respiratory tract are swallowed and reach the environment in the faeces. After 30-45 days, embryonated eggs become infective when ingested by cats. Earthworms are facultative paratenic hosts.16 When cats ingest infective eggs or earthworms carrying larvae, the larvae migrate to the lung and develop into the adult stage in 3-6 weeks.30
The life cycle of Paragonimus spp is associated with freshwater environments and is complex as it involves two intermediate hosts. Motile miracidia are freed from eggs when swallowed and then passed in faeces from infected cats and penetrate aquatic snails; cercarial stages developed in snails will move from them, actively entering the second intermediate host (crab or crayfish). Cats are infected after eating the second intermediate host where metacercariae finally develop. Young flukes develop from metacercariae in the cat intestine, cross the intestinal wall and the diaphragm to the pleural cavity where they penetrate the lung parenchyma and become reproducing adults in about 6 weeks.1
Feline lungworm infestation is receiving increasing attention.2,6 Aelurostrongylus abstrusus is a well-recognized agent of lower respiratory tract disease in cats.1,2 Epidemiological studies or case reports confirmed the presence of the parasite in the Americas, Europe, Asia and Australia.1,14,31,32,33,34,35,36,37,38,39 Prevalence rates vary and endemicity is linked to climatic and ecological factors that may influence: a) the vitality and developmental capacity of L1; b) the presence of suitable intermediate hosts in the environment; c) the number of days needed for the development of the infective stage (L3).
The diagnostic method used in epidemiological studies and the characteristics of the population investigated heavily influence the results.2,36,40,41 Feral and free-roaming cats are at higher risk because of their predator activity as are cats with respiratory signs and young cats.42,43 In Tirana (Albania), post-mortem examination of the lungs of 18 feral cats revealed that nine (50 %) were positive for A abstrusus.44 Use of a low-sensitive diagnostic method, such as faecal standard flotation technique, showed a prevalence rate of 1-25 % in a general cat population.14,45,46,47,48
Oslerus rostratus is considered an uncommon parasite in domestic cats, but the prevalence in feral cats was found to be 24 % on Majorca (Spain). It was also reported in a cat in Northern Spain.7,8 Very recently, the incidental occurrence of a few adult O rostratus worms was reported in Sicily (Italy) at the necropsy of an adult cat that had died following a road traffic accident.10
C aerophila has a sporadic occurrence in cats, dogs and humans in Europe. In Central Italy, a prevalence of 3 to 14 % was found in the feline population.2,16,35
Single cases of Troglostrongylus spp infestation were recently reported in cats from Ibiza (Spain), Central-Southern Italy and Crete (Greece).9,12,13,15,19,20,29,49 The first epidemiological data on T brevior in domestic cats were recently provided in Sardinia (Italy) where 6.5 % of a sample of 107 cats tested positive compared to 25.2 % that tested positive for A abstrusus,14 confirming that Troglostrongylus is not a negligible lungworm of domestic cats.
The recent development of molecular assays specific for mollusc-borne feline lungworms sharing the same ecological niches, as well as for C aerophila, is likely to be of great value for epidemiological investigations, overcoming the difficulties of copromicroscopy for differentiating the metastrongylid L1.3,9,49,50,51
Paragonimus spp infestation are reported in cats from the Americas, Africa and Asia.1,52,53 Paragonimiasis is most prevalent in cats and dogs in some parts of Asia.54
Prevalence rates and occurrence of case reports for A abstrusus, C aerophila, O rostratus and Troglostrongylus in some European countries are shown in Table 1.
The severity of lesions depends on the worm species and burden. Kittens also seem to develop a more severe disease.18,26,27,55 This may be explained by the smaller lung volume and small diameter of the trachea and bronchi, which are more easily blocked by worms, in particular for the larger Troglostrongylus. The immature immune system also seems to facilitate infestation: experimental re-infestation of kittens with A abstrusus L3 larvae about one after the initial symptomatic infestation failed to induce respiratory signs or lung lesions.25 In cats with natural aelurostrongylosis, the more severe radiologic abnormalities and the higher larval burdens were found in younger animals56 (Fig. 1).
An infectious dose of A abstrusus larvae of <100 L3 does not induce clinical signs but infective doses of 800 to 3200 larvae severely affect the lung and may even be lethal.57,58 However, at normal infective doses, the individual immune response significantly affects the parasite life cycle.28 Cats repeatedly infected with a low number of larvae do not develop clinical disease when challenged with a high dose.59
The role of immunity is also confirmed. Passive immunity protects experimentally infected kittens and can help some cats halt the parasite life cycle in the lung by preventing the patent phase of infection.28,60
It has been known for a long time that eosinophilia is evident 2-6 weeks after the ingestion of L3 larvae A abstrusus and immune-mediated reactions of I, III and IV type are associated with alveolar, interstitial, peribronchial and vascular lesions and may lead to the death of parasites several months later.1,61 A more recent experimental study provides more detailed information on the clinical signs, haematology, biochemistry, coagulation analysis, computed tomography, coprology and post-mortem examination in young adult cats.28,58 Infected cats had moderate, non-specific clinical signs (fever, apathy, weight loss, lymph node enlargement) and respiratory signs (dyspnoea, respiratory sounds, cough).
Leucocytosis, massive and persistent eosinophilia and, in some cases, severe lymphocytosis were the most frequently observed abnormalities but no changes were detected in serum biochemistry. Various coagulation abnormalities were found, with a frequent occurrence of low fibrinogen values suggesting an increased consumption. Dose-dependent imaging changes in the thorax consisted of pulmonary nodules, bronchial pattern and lymphadenomegaly and were found even in a cat that did not develop a patent infection.58 A abstrusus eggs accumulate in alveoli and bronchioles inducing an inflammatory reaction in the lung (Fig. 2).
Multiple subpleural nodules (Fig. 3) are caused by the granulomatous reaction surrounding clusters of eggs and adult worms and emphysema is due to parasitic accumulation in the alveolar spaces. Bronchitis is severe and diffuse, usually manifested by bronchial and peribronchial lymphoid hyperplasia, hypertrophy of the smooth muscle layer and mucosal hyperplasia with increased mucous cell secretion in the bronchi. Vascular and perivascular changes are also seen with hypertrophy and hyperplasia of pulmonary arteriolar smooth muscle, subendothelial fibrosis associated with eosinophilic infiltrates, endothelial and perivascular hyperplasia. Pulmonary hypertension may be the consequence of lung disease and arteriolar and bronchial changes may persist after the parasite dies, mimicking the changes found in feline asthma.27,61,62,63
Bacterial complication is frequent and can be associated with pleural effusion.26 Salmonella typhimurium, Pseudomonas spp and Escherichia coli have been isolated in some cases and infection with enteric bacteria probably results from larvae migrating from the intestine.53,64
In a kitten with severe pulmonary aelurostrongylosis, enteritis and mild diarrhoea were associated with the presence of a high number of L1 larvae invading the mucosa of small intestine.39
Lethal T brevior infestation was associated in three kittens with catarrhal bronchitis occluding the lumen together with the adult worms and multifocal pulmonary haemorrhages, consolidation and emphysematous foci.12,15
O rostratus does not seem to be associated with severe pathologic changes in domestic cats, as few adult worms are found embedded in bronchial or peribronchial tissues inside pseudo-cysts.7,10Capillaria aerophila usually induces chronic bronchitis.16,65
The penetration of Paragonimus in the lung is associated with haemorrhagic foci, usually in the diaphragmatic lobe. Fluke cysts communicate with bronchi and may evolve into bullae, with a risk of developing pneumothorax.
Although most publications concern A abstrusus, it has been suggested that many cases of infestation or co-infestations caused by other metastrongyloids may have been erroneously attributed to the better-known A abstrusus because of difficulties with the morphometric differentiation of L1 larvae.3,4,9 Genetic characterization of larvae now offers new insights and is likely to allow more accurate diagnoses.
Lungworm infestations may be asymptomatic, or cause mild to severe respiratory signs due to bronchopneumonia, sometimes complicated by pleural effusion or pneumothorax.26,55,66,67 A productive cough is therefore the main clinical sign, together with mucopurulent nasal discharge, tachypnoea, dyspnoea with laboured, abdominal breathing and end-inspiratory crackles upon auscultation. In more severe cases, respiratory failure causes cyanotic mucosae and respiratory acidosis.9,18,27,41,68
Diagnostic imaging, e.g. thoracic radiographs or tomography, shows bronchial thickening and poorly defined, small nodules during the patent phase but may persist after clearing the infestation and should be differentiated from other chronic bronchial disease such as asthma.69,70 Imaging changes may be evident even before the patent phase of disease.28,58
Right side cardiomegaly associated with eccentric hypertrophy and secondary to pulmonary hypertension has been described in two kittens affected by a severe bronchopneumonia caused by A abstrusus.27 Both kittens presented with heart murmurs with maximum intensity on the right hemithorax due to tricuspidal and pulmonary regurgitation. One of the kittens died but, in the surviving kitten, the heart murmur disappeared several months after the parasitological and clinical cure. Echo-Doppler examination confirmed the resolution of pulmonary hypertension.27
It is therefore advisable to investigate the presence of lungworm infestation in cases of right heart disease associated with signs of pulmonary hypertension in outdoor cats. In a study of 54 cats that died during anaesthesia in spay-neutering programs in USA, 9 % of post-mortem investigations revealed the presence of Aelurostrongylus abstrusus.71 Uncared-for outdoor cats, such as those included in trap-neuter-release programs, are at higher risk of lungworm infection.
Eosinophilia is a frequent abnormality but is not found systematically in cell blood counts or in bronchoalveolar lavage (BAL) cytology.18,55,64,72
Trogostrongylus spp was considered the cause of death of parasitized kittens presenting with coughing and severe respiratory failure at diagnosis, but cases of asymptomatic infestation have also been reported.12,13,15,19,73
Capillaria infestation may induce coughing (mostly dry cough), sneezing and wheezing in cats but asymptomatic carriers have also been reported.16,74
Mixed infestations are increasingly reported but they do not necessarily have a more severe clinical picture or poorer outcome.19,73,74
L1 larvae are very active in the faeces and are readily detected in fresh faecal samples. Care should be taken to prevent soil contamination, as the presence of free-living nematodes may lead to misdiagnosis. L1 can be observed in direct faecal smears or by the floatation technique. In the latter method, high specific gravity of concentrated salt or sugar solutions may induce osmotic damage to the larvae, making identification difficult.1 The Baerman migration method is considered the enrichment technique of choice for metastrongyloid lungworms, and is based on the positive hydro-thermo tropism observed for live nematode larvae40,41,75 (Figs. 4; Table 1). It can provide quantitative information on the number of larvae found in each gram of faeces, which correlates well with the severity of the disease.46,56 Unfortunately, 24 hours are necessary to obtain the result and negative results should be repeated three times for the best sensitivity.
A new parasitological device for multivalent quantitative estimation of eggs, larvae and oocysts named FLOTAC, was evaluated for suitability in the diagnosis of A abstrusus infestation. The authors reported that it was more sensitive than the Baerman test.76 However, the major limitation of copromicroscopy in general is the impossibility of making diagnosis in the pre-patent period, which lasts about 1-2 months, or when egg shedding has stopped but parasites persist and clinical signs are manifest. A well-trained observer is required to differentiate the different strongylid L1 forms on the basis of their morphometric and morphologic characteristics3,12 (Figs. 5 and 6).
Lungworm larvae can be found in tracheal swabs or wash and BAL cytology but with less sensitivity than in faeces, so there is no benefit in using this invasive procedure that risks severe respiratory disease.40 Antibodies to A abstrusus can be detected as early as 3 weeks p.i. by IFAT but past and currently active infestations cannot be differentiated by serology.77
Significant progress has been obtained in diagnosis with the use of molecular methods. A nested-PCR assay specific for A abstrusus has been validated on different biological samples (faeces, floatation supernatant, Baermann sediment and pharyngeal swabs) collected from cats with natural infestations. A specificity of 100 % and a sensitivity of up to 96.6 % were obtained and the best results were found using pharyngeal swabs.50 This method allows early diagnosis in the pre-patent phase with a potential positive impact on prognosis. Molecular techniques are expected to significantly improve the understanding of lungworm infections. A new multiplex PCR has also been developed for the simultaneous detection of both A abstrusus and T brevior.49
Capillariosis is diagnosed by standard faecal flotation but molecular techniques are also available for screening tests and for human cases.2,51
Paragonomiasis is diagnosed by formalin-ether sedimentation technique.52 Molecular methods are available for epidemiological purposes in cats and are used for human cases.78,79
Information on the efficacy of various drugs is available from controlled studies or clinical case reports (Table 2). Oral administration of fenbendazole has been suggested, with different dosages and durations of therapy (from 20 mg/kg for five days to 50 mg/kg for 15 days) but an oral paste is licenced in UK for treating aelurostrongylosis in cats at 50 mg/kg once a day for three days.2
Off-label use of ivermectin has been reported with controversial results and should not be considered because of the risk of toxicity mainly in kittens.55
Two spot-on formulations administered at the recommended dosage were compared to the three-day-course of therapy with fenbendazole and they were found to be effective and safe in the treatment of twelve naturally infected cats each: one formulation containing imidacloprid 10 % and moxidectin 1 % (Advocate®, Bayer), the other emodepside 2.1 % and praziquantel 8.6 % (Profender®, Bayer).80,81 The moxidectin formulation gave the best results in terms of efficacy among all the three protocols, with 100 % efficacy after 30 days.81 In a controlled study, the imidacloprid 10 % and moxidectin 1 % spot-on formulation was significantly effective also against C aerophila infestation.74 The efficacy of a new spot-on combination of fipronil 8.3 %, (S)-methoprene 10 %, eprinomectin 0.4 % and praziquantel 8.3 % (Broadline®, Merial) was evaluated under experimental conditions and it was found to be highly effective for both the prevention and treatment of A abstrusus infestation.82
In a case series study, cats with natural infestation treated with the association imidacloprid 10 % and moxidectin 1 % were rechecked at day 14, and those still found positive (4/7) were re-treated and checked one week later. At this time, one cat remained positive and was treated for a third time. At the end of the study (day 50), two negative faecal tests had been obtained for all treated cats, confirming the efficacy of the treatment with imidacloprid and moxidectin.46
An association of milbemycin oxime (4 mg) and praziquantel (10 mg) (Milbemax®, Novartis) was administered as single oral dose (half tablet per kg) three times, fifteen days apart, to a kitten affected with A abstrusus bronchopneumonia and pulmonary hypertension obtaining parasitological and clinical cure.27 Standard topical administration of selamectin spot-on formulation (6mg/kg) (Stronghold®, Zoetis) was reported in some cases.55,72,83 In one study, selamectin was effective in one of four cats at day 30 and in two of the three cats re-treated and followed up at day 60.55 In the other study, treatment was effective in nine of ten cats.83 Capillariosis was successfully treated in a cat with two injections of abamectin (14 days apart) at a dose of 0.3 mg/kg.84
Information on the treatment of Troglostrongylus, as well as on mixed infestations, is derived from case reports only. Severe respiratory cases of Troglostrongylus infestations were not cured by imidacloprid 10 % and moxidectin 1 % or febendazole treatment.12 A combination of milbemycin oxime (4 mg) and praziquantel (10 mg) was administered as single oral dose (half tablet per kg) in two kittens with mixed infestations caused by A abstrusus and T brevior. The asymptomatic kitten was cured but the sibling with severe respiratory disease died two days later.19 Mixed infestations caused by T brevior and A abstrusus or C aerophila were cured in two kittens using the emodepside 2.1 % and praziquantel 8.6 % spot-on combination but in one case two administrations were required to clear Trogostrongylus larval shedding.73
Bacterial secondary infections may contribute to the severity of the disease and broad-spectrum antibiotics should always be given together with corticosteroids at anti-inflammatory doses. Pleural effusion and pneumothorax require immediate resolution by thoracocentesis and medical care in intensive care unit (oxygen administration) is required for all cats with respiratory failure.
|Country||Reference||A abstrusus||O rostratus||Troglostrongylus||C aerophila|
|Italy||Brianti et al. (2008), Traversa et al. (2008a), Iorio and Traversa (2008), Mugnaini et al. (2012), Riggio et al. (2013), Spada et al. (2013), Brianti et al. (2014b), Tamponi et al. (2014), Giannelli et al. (2014a), Varcasia et al. (2014)||1.2-25.2 %(CR)||(CR)||6.5 %(CR)||1.2-14.3 %(CR)|
|Spain||Mir et al. (2004), Jefferies et al. (2010)||1 %(CR)||24 %(CR)||(CR)||1.3 %|
|Greece||Diakou et al. (2014)||(CR)|
|Portugal||Payo-Puente et al. (2008)||17.4 %||-||-||0.3-0.6|
|Netherlands||Robben et al. (2004)||2.6(CR)||-||-||-|
|Germany||Taubert et al. (2009), Becker et al. (2012), Barutzki and Schaper(2013)||0.7-6.5(CR)||-||-||0.2|
|Croatia||Grabarevi_ et al. (1999)||22%||-||-||-|
|Albania||Knaus et al. (2011)||50%||-||-||-|
|Romania||Mircean et al. (2010)||5.6%||-||-||3.1|
|Hungary||Andras and Peter (2002), Capari et al. (2013)||14.5(CR)||-||-||3.8|
|Bulgaria||Stoichev et al. (1982)||33.3||-||-||-|
|CR= Case report|
In cases of A abstrusus infestation, a delay in the diagnosis and treatment may lead to lethal cardio-pulmonary lesions, while early diagnosis and treatment greatly improves the prognosis. The level of larval burden obtained by the Baerman test is usually related to the severity of the disease but prognosis should be mainly based on physical examination (severity of dyspnoea and occurrence of cyanosis) and radiographic findings (severity of diffuse bronchial, alveolar and interstitial disease).
Stray and free-roaming cats have a higher risk of becoming infested with lungworms in endemic areas.42
Avoiding predation is at present the only preventative measure for metastrongyloid or trematode pulmonary worms with indirect life cycles. The prophylactic activity of some molecules used to treat nematode respiratory infestations – as for Angiostrongylus vasorum infestation in dogs – is currently unknown but appears promising.82
Capillaria aerophila has zoonotic potential and sporadic cases of human capillariosis have been described worldwide. The disease manifests as bronchitis with a productive cough but the presence of haemoptysis and nodular infiltrative lesions in the lung require a differential diagnosis with lung cancer.17
Paragonimiasis is a food-borne zoonosis acquired by people eating raw crustaceans. Infected cats are not dangerous for people.54,85
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