Troglostrongylus brevior is a nematode belonging to the order Strongylida, family Crenosomatidae. The genus Troglostrongylus includes four species that normally infest the respiratory tract of wild felids: Troglostrongylus brevior, Troglostrongylus subcrenatus, Troglostrongylus troglostrongylus, Troglostrongylus wilsoni. Of these, T. brevior has also been reported in domestic cats (Felis silvestris catus), at times as the cause of severe - often fatal - clinical cases involving young subjects. T. subcrenatus has also been reported in domestic cats, however in view of the considerable rarity of this parasite (i.e., to date only two cases of T. brevior infestations have been reported, in 1961 and in 2012) this article will only focus on T. brevior.
THE PARASITE
Adult females of T. brevior are around 6-16.8 mm long and 260-430 μm wide;males are between 5-7.2 mm long and 220-365 μm wide. The nematode infests the bronchi and bronchioles of wild felids and of domestic cats, their definitive hosts. The life cycle is indirect. After mating, adult females lay embryonated eggs that mature and hatch within the respiratory tract, releasing the first-stage larvae (L1). These larvae actively ascend the respiratory tract, reaching the trachea, larynx and pharynx, from where they are subsequently ingested. After passing through the gastrointestinal tract unharmed, the L1 are shed into the external environment through the faeces. For the process to continue, intermediate hosts are necessary: gastropod molluscs (e.g., Helix aspersa, Chondrula septemdentata, Helicella barbesiana, Helicella vestalis joppensis, Limax flavus, Monacha syriaca, Retinella nitellina and Theba pisana), within which the L1 undergo two mutations before reaching the third larval stage (L3), which then infests the definitive host.The time-interval necessary to reach the infective larval stage mainly depends on the mollusc species involved and on the ambient temperature. For example, in the snails of the Helicella spp., parasite development occurs in eight days at a temperature comprised between 22 and 27°C. Other animals, such as birds, reptiles and small rodents, may act as paratenic hosts, in which the parasite remains viable and infective, although quiescent in terms of its development. The definitive host is infested by ingesting the molluscs containing the L3 or by preying on the paratenic hosts, which have in turn ingested the infested molluscs. It has been recently speculated that the L3 may also be present in the mucus of molluscs, and that this may be an additional source of infestation for the definitive hosts, which could be exposed to the L3 through contaminated food or water. However, this mode of infestation has never been confirmed. After ingestion, the L3 penetrate the intestinal mucosa and reach, through the blood and lymph, the lungs of the definitive host, completing their life cycle in about 28 days. Recently, the possibility of vertical transmission, from mother to neonate - transplacentally or via the milk - has also been hypothesized.
With regards to the epidemiology of troglostrongylosis, the existing knowledge and the data currently available are scarce, making it difficult to draw a comprehensive picture of the spread of the parasite and of its main transmission pattern. The nematode was described for the first time in the last century, in some wild felids in Palestine and, later, in wild and feral cats in central Italy. Only in recent years has the presence of T. brevior been again described in domestic cats in Spain, Italy and Greece, and in wildcats in Italy and continental Europe. In particular, as regards Italy, the parasite has been repeatedly reported in domestic cats in Sicily, Sardinia and in central and southern sub-Apennine areas, especially in the Italian Regions of Abruzzo, Marche, Umbria, Latium, Apulia, Molise and Basilicata. In these areas, the presence of the wildcat (Felis silvestris silvestris), a natural host and reservoir of the parasite, appears to play a key role in the spread of the disease. In fact, the cases of troglostrongylosis in domestic cats reported so far come from areas in which the wildcat is present, and where the T. brevior infestation rate in this species is very high. In addition, recently, the distribution of the wildcat in Italy has been increasing - because of the fragmentation of wooded habitats - and this phenomenon may have favoured the increased sharing of the same ecological niches between domestic and wild felids, thus increasing the possibility for the domestic cat to come into contact with T. brevior. The wildcat may therefore represent the main source of infestation for the intermediate and paratenic hosts and, consequently, for domestic cats. Nevertheless, given the by-now endemic presence of the parasite in domestic cats in sub-Apennine areas, it is likely that in coming years we may witness an expansion of T. brevior to geographic areas where the wildcat is currently absent. In northern Italy T. brevior seems for the moment to be virtually absent, as only a single case has been reported in a cat in Friuli, in the only area of northern Italy where the wildcat is also present.
Other environmental factorsthat may influence the presence and distribution of feline troglostrongylosis are the climatic conditions and the ubiquitous spread of intermediate and paratenic hosts. As for the definitive host, cats at greater risk of infestation are those living in rural or peri-urban areas, with outdoor-access,which may come into contact and ingest intermediate and/or paratenic hosts. Compared to adult subjects, young subjects are particularly at risk, as confirmed by the frequency of diagnosis of troglostrongylosis in kittens or in animals under one year of age.
PATHOGENIC ROLE AND SYMPTOMATOLOGY
The size of the parasite and its presence within the respiratory tract are the cause of obstruction of the bronchial lumen with atelectasis and haemorrhage of the lung parenchyma. The symptomatology of troglostrongylosis is of respiratory nature and can be particularly severe and even fatal in subjects under one year of age, due to the extent of the pulmonary damage and the widespread obstruction of the infested bronchi. In adult cats, subclinical or self-limiting forms of troglostrongylosis are instead more common. In infested animals the clinical signs are nonspecific and among these the most common ones are cough, dyspnoea, tachypnoea, nasal and/or oculoconjunctival discharge and sneezing. In more severe cases there can be lethargy, dehydration, poor general condition, severe respiratory failure and death. In addition, a case of irreversible pulmonary hypertension has been described in a four month-old subject, despite adequate antiparasitic and support therapy. Necropsy findings reveal the presence of congestion, hypertrophy and pulmonary oedema, diffuse haemorrhages, lobular inflammation and parenchymal hepatization.
DIAGNOSIS
The clinical diagnosisof troglostrongylosis is virtually impossible, in view of the non-specificity of the clinical findings. However, a careful evaluation of the signalment and of the clinical history may allow the clinician to suspect the diagnosis. The clinical signs of the disease are such that the differential diagnoses must include a variety of viral, bacterial, parasitic, fungal and non-infectious disorders (e.g., foreign bodies, tumours).
Even additional tests (such as diagnostic imaging) do not allow an aetiologic diagnosis and are only useful to highlight the eventual presence and severity of non-specific lung lesions. Radiographic signs include an alveolar pattern, or an interstitial and/or a bronchiolar one in more advanced stages, with increased parenchymal opacity. The definitive diagnosis is therefore only possible with the identification of the parasite in the infested cat. In veterinary clinical practice, conventional copromicroscopic analysis remains the most frequently used diagnostic methodology, in view of its speed, ease of use and its non-invasiveness. Flotation enrichment methodologies with saturated solutions of salts or sugars (SG 1200-1350) may sometimes allow the detection of the L1 stage of the parasite in the faeces of infested animals but, often, the larvae, when in contact with these solutions, suffer an osmotic damage which makes them unidentifiable from the morphological point of view. The gold standard technique for the diagnosis of feline troglostrongylosis is therefore represented by the Baermann technique, which exploits the hydrophilicity of the L1 stage and allows the isolation of live and viable parasites. The technique is very simple and economical but does present some disadvantages, such as the need to wait 24-48 hours to obtain a result and its sensitivity, which is lower than 100%. In fact, due to the inconsistent elimination of L1 in the faeces, the test should be repeated on three stool samples collected on alternate days in a week, or for three consecutive days. In addition, an experienced microscopist is necessary for the morphological recognition of the larvae. The L1 of T. brevior, which are ~300-360 µm long and ~18 µm wide, present a sub-terminal oral aperture (Fig. 1A) and a tapered terminal end provided with two incisures, one dorsal and one ventral, less profound (Fig. 1B). A careful evaluation of the front and posterior ends and of the size of the parasite thus allows the morphologic and morphometric identification of the L1 and to distinguish them from those of other parasitic nematodes of the cat having a similar morphology (e.g. Aelurostrongylus abstrusus) or from free-ranging nematodes. Finally, molecular biology methodologies have recently been developed which can detect the DNA of the parasite in the faeces as well as in the mucus of infested cats, even when the samples are negative to the classical methods.
TREATMENT
Data gathered in case series or in studies on limited number of cats have shown that moxidectin, milbemycin oxime, emodepside and eprinomectin are effective, with a certain degree of variability, against T. brevior. The administration of a spot-on formulation of moxidectin 1% was not effective in a case of severe troglostrongylosis, while in another cat it determined the parasitological cure and clinical improvement after a single administration. Milbemycin oxime, at a dose of 2 mg/kg, also showed variable results when administered per os in two subjects with mixed infestation from T. brevior and A. abstrusus, being effective against T. brevior in only one of the two kittens treated. In two cases of mixed infestation by T. brevior and of other feline respiratory nematodes (A. abstrusus and Capillaria aerophila), a spot-on formulation of emodepside 2.1% was effective after one or two administrations. Recent studies have shown that a spot-on formulation of eprinomectin 0.4% is able to prevent the shedding of larvae in naturally infested cats and has also shown larvicidal and adulticidal activity under experimental conditions.
In severe cases, the anthelmintic therapy should be integrated with symptomatic supportive care, in order to limit inflammatory reactions and to ensure good oxygenation.
Suggested reading
- Di Cesare A, Veronesi F, Grillotti E, Manzocchi S, Perrucci S, Beraldo P, Cazzin S, De Liberato C, Barros LA, Simonato G, Traversa D. Respiratory nematodes in cat populations of Italy. Parasitol Res. (Epub ahead of print) PubMed PMID 2015:26319524.
- Traversa D, Di Cesare A. Feline lungworms: what a dilemma. Trends Parasitol. 2013; 29(9):423-30. doi: 10.1016/j.pt.2013.07.004.
- Traversa D, Di Cesare A. Cardio-pulmonary parasitic nematodes affecting cats in Europe: unraveling the past, depicting the present, and predicting the future. Frontiers Vet Sci 2014; doi: 10.3389/fvets.2014.00011.
- Di Cesare A, Veronesi F, Traversa D. Felid lungworms and heartworms in Italy: more questions than answers? Trends Parasitol. 2015; in press.