Clinical-parasitological screening for respiratory capillariosis in cats in urban environments

Respiratory capillariosis caused by the nematode Capillaria aerophila (Trichocephalida, Trichuridae) is a parasitic disease common in wild carnivores including foxes (Sreter et al., 2003; Lalošević et al., 2013; Čabrilo et al., 2018), coyotes (Gompper et al, 2003), wolves (Pence & Bryant, 2002), raccoons (Schuster et al., 2001) and bears (Crum et al., 1978; Paoletti et al., 2017). The nematode may also infect dogs (Traversa et al., 2009), cats (Madeira de Carvalho et al., 2009), and sporadically humans (Lalošević et al., 2008; Di Cesare et al., 2012).

Capillaria aerophila has a worldwide distribution and is considered as the second most common respiratory helminth of domestic cats in the Northern Hemisphere after Aelurostrongylus abstrusus (Knaus et al., 2015). Adult stages of the parasite live on the surface of bronchioles, bronchi, and trachea, where they are completely or partly fixated to the mucosa, causing injury to the epithelium and lung parenchyma. Although less frequently, they can also infest the nasal mucosa and nasal and frontal sinuses (Barrs et al., 2000).

Capillaria aerophila infection is usually subclinical and reported sporadically in cats. However, in the past three decades, the parasite has been increasingly detected in cats in Europe (Traversa et al., 2010), Asia (Matayoshi et al., 1996; Bowman et al., 2008), Australia (Milstein & Goldsmid, 1997), New Zealand (Langham & Charleston, 1990), North Africa (Kohart et al., 2014) and North and South America (Echeverry et al., 2012).

Knowledge of epidemiological data (e.g. range of hosts and geographic distribution) of C. aerophila in Europe is fragmentary, thus at the moment it is difficult to assess to what degree this parasite may be spreading or what influence global warming or other factors may have on the current distribution. Indeed, although climate changes seem to play a key role in the epidemiological variations for pet heart-worms and lungworms, other possible factors can not be ruled out (Traversa et al., 2010). In Europe, C. aerophila is widely distributed as supported by the published feline case reports in Hungary (Capári et al., 2013; Rehbein et al., 2014), Belgium (Thienpoint et al., 1981), France (Elhamiani Khatat et al., 2016), Germany (Krone et al., 2008), Serbia (Ilić et al., 2009), Greece (Haralampides, 1978), Italy (Di Cesare et al., 2010; Spada et al., 2013), Albania (Knaus et al., 2014), Portugal (Waap et al., 2014), Romania (Mircean et al., 2010), Austria, Bulgaria, Latvia and Lithuania (Rehbein et al., 2014. Recently, different genetic haplotypes of C. aerophila have been shown to coexist in foxes, martens, cats, and dogs in European countries, confirming a common pattern of transmission of this parasite between wild animals and pets (Di Cesare et al., 2014).

In feline medicine, respiratory parasitic infections represent a particular challenge for clinicians due to a large number of conditions with similar clinical manifestations. Knowledge of the prevalence and clinical expression of the disease in cats such as malaise, cough, sneezing, mucopurulent nasal discharge, and “air hunger” should encourage the veterinarian to consider pulmonary capillariosis in the differential diagnosis of these clinical manifestations (Traversa et al., 2010). Furthermore, given the prevalence and zoonotic potential of C. aerophila, it is recommended to include it in the differential diagnosis of cardio-respiratory diseases in dogs and cats.

Therefore, this paper aims to determine the prevalence of C. aerophila infection in cats through the parasitological examination of the feces in the city of Belgrade, Serbia, and its suburban settlements and to describe the clinical signs and complains associated with this infection.

Research showing standard clinical/laboratory practices or the advancement of standard practices.

In carnivores, C. aerophila infection usually causes chronic bronchitis (Traversa et al., 2010). However, it can follow different clinical courses, from mild subclinical infection to life-threatening acute respiratory distress (Traversa et al., 2010).

Rehbein et al. (2014) have described a prevalence of 6.6 % of Capillaria spp. eggs in the the feces of cats in seven European countries (Albania - 31,6 %, Austria - 3,8 %, Bulgaria - 4,3 %, Germany - 1,6 %, Hungary - 5,0 %, Latvia - 4,1 %, Lithuania - 2,6 %). The total number of infection varied among the regions probably because of differences in the living behavior of the studied cats (rural, suburban, or urban areas).

As the most common helminths, gastrointestinal parasites have been described in cats worldwide: ascarids (Toxocara cati and with a significantly lower prevalence of Toxascaris leonina), hookworms (mainly Ancylostoma tubaeforme and depending on climate, occasionally Uncinaria stenocephala), cestodes from family Dilepididae and Taenidae (predominantly Taenia taeniaeformis, and less frequently Echinococcus multilocularis in endemic areas) (Rehbein et al., 2014).

In this study of gastrointestinal parasitosis, the highest prevalence of toxocariasis (18.83 %) was diagnosed, followed by Isospora spp (10.97 %) and ancylostomatids (7.74 %). Of the mixed infections, only double infections were identified. The most common infection was Isospora spp. and T. mystax (3.22 %), and an identical prevalence (2.58 %) of coinfection of this ascarid with C. aerophila and ancylostomatids were found. The factors such as cat category (e.g., stray cats, cats from animal shelters, pets kept under controlled conditions), habitat (urban or rural) or access to open spaces can have a significant impact on the variation of prevalence of these endoparasitoses (Mircean et al., 2010; Capari et al., 2013). The first studies of respiratory capillariosis in cats in Serbia were conducted in the area of Belgrade in the period 2003 – 2007 when the prevalence of C. aerophila was determined to be 8.03 % (Ilić et al., 2009). In the last decade, the prevalence of this nematode in cats in Belgrade has almost doubled. The established growth trend can be attributed to the increase in the number of foxes as a reservoir of infection for pets (Traversa & Di Cesare, 2016). This claim is supported by the results of research, according to which an extremely high prevalence of C. aerophila was found in foxes in Serbia (Lalošević et al., 2013; Ilić et al., 2016).

Several studies from different countries have confirmed that in the past two decades the number of cases of respiratory capillariasis has grown both in cats and humans (Barrs et al., 2000; Di Cesare et al., 2012; Cross, 1998; Lalošević et al., 2008). Human infections have been described in Ukraine, Russia, France, Morocco, Iran (Di Cesare et al., 2012), and Serbia as well (Lalošević et al., 2008). Some recent molecular-based studies have shown that different haplotypes of C. aerophila may circulate between domestic and wild carnivores (Di Cesare et al., 2012). Indeed, genetic studies demonstrated that some C. aerophila haplotypes may infect both pet and wild animals from the same locations suggesting that wild animals may have an impact on the transmission to and the propagation of respiratory capillariosis in the feline population (Traversa & Di Cesare, 2016). In Europe, fifteen different haplotypes have been identified, out of which five are identical between pet and wild animals in Italy (Di Cesare et al., 2014). Three genetic subpopulations infecting cats and foxes were identified in Serbia (haplotype I and II) and one each in Romania (haplotype I) and Portugal (haplotype VII) (Di Cesare et al., 2014).

Literature data also suggests that cats can be infected with the nematodes from the Trichuris genus (T. felis, T. campanula, and T. serrata). Although these species are very rarely diagnosed in cats and only in limited geographical areas (Traversa et al., 2010; Traversa, 2011), the finding of their eggs in the feces additionally complicates the interpretation of coprology results and precise diagnosis (Traversa & Di Cesare, 2016; Giannelli et al., 2017).

The predominant clinical signs associated with respiratory capillarisosis are productive cough accompanied by mucopurulent nasal discharge, tachypnea, dyspnea with evident abdominal breathing, and end-inspiration crackling during auscultation. In more severe cases, respiratory failure leads to mucosal cyanosis and respiratory acidosis (Traversa et al., 2012). In 14.84 % of the studied cats, increased broncho-vesicular respiratory sounds, sneezing, wheezing and dry cough were the most frequent clinical signs detected. These clinical findings are the result of C. aerophila adult worms which are capable of inducing lesions in the trachea and lung parenchyma. In a few cases, the cough became productive probably because of a more advanced disease phase associated with secondary bacterial bronchopneumonia. Fever was the consequence of secondary bacterial bronchopneumonia.

Furthermore, the achievement of an accurate diagnosis is further complicated because some cats infected with respiratory parasites can display clinical improvement after unspecific treatment including corticosteroids and bronchodilators (Traversa & Di Cesare, 2016). This apparent improvement can delay the definitive diagnosis for several weeks (Traversa & Di Cesare, 2016).

The differential diagnosis may include all diseases causing upper and/or lower respiratory signs including other parasitic infections (dirofilariasis, pulmonary toxoplasmosis, aelurostrongylosis, troglostrongylosis) but also tracheobronchitis, tracheal stenosis, pneumonia (of bacterial, viral or fungal etiology), airway obstructions caused by foreign bodies, nasopharyngeal polyps, tumors, pulmonary granulomatosis, allergies, and chronic bronchial diseases affecting cats (asthma) (Spada et al., 2013; Ilić et al., 2015). All the before mentioned diseases are not characterized by pathognomonic symptoms which complicates the clinical diagnosis.

Complications associated with a fatal outcome in infected animals are interstitial emphysema, lung edema, and secondary bacterial infections (Traversa et al. 2012). In some cases, these infections may be complicated by pleural effusions or pneumothorax (Traversa et al., 2009). An additional complication is an absence or the non-pathognomonic abnormalities detect on thoracic radiographs (Traversa et al. 2012) The most common finding is an alveolar lung pattern, possibly associated with the bronchial and interstitial pattern, with bronchial wall thickening and reduced interstitial transparency (Traversa et al. 2012). In chronic or mixed infections, right-side cardiomegaly may develop, associated with eccentric hypertrophy, occurring secondary to pulmonary hypertension. This condition is the consequence of severe bronchopneumonia caused by a secondary bacterial infection or mixed infection with A. abstrusus or Dirofilaria immitis (Dirven et al., 2012).

Secondary bacterial infections contribute to the severity of parasitic infections of the lungs; that is the reason why broad-spectrum antibiotics combined with corticosteroids should always be administered (at anti-inflammatory doses) to all cats with bronchopneumonia symptoms (Foster, 2004). Pleural effusion and pneumothorax require immediate thoracocentesis (pleural tap) (Pechman, 1984). The care of a cat with respiratory failure should include the management in an intensive care unit with mandatory use of oxygen therapy and nebulization (Foster, 2004).

All the cats included in this study reached a complete improvement (absence of clinical signs and negative coprology results) after treatment with fenbendazole. However, in some of these cats, clinical signs were present for even up to six weeks after anthelminthic treatment, as shown by positive coprology results for C. aerophila. This could be explained by either reinfection due to living conditions (households with many cats and free access to open spaces) or by a partial response to fenbendazole treatment. Several protocols have been reported in the literature for the treatment of respiratory capillariosis in cats, such as the combinations of fenbendazole paste, milbemycin-oxime/praziquantel, various spot-on formulations, abamectin, ivermectin, and levamisole (Brianti et al., 2013; Traversa & Di Cesare, 2013). Oral administration of fenbendazole with different doses and duration of treatment has been suggested by several authors (from 20 mg/kg in 5 days to 50 mg/kg in 15 days) as effective treatment (Grandi et al., 2005). Although positive results have been reported with ivermectin, there is a prevailing opinion that these agents should not be used in cats, especially in kittens, due to toxicity concerns (Brianti et al., 2013; Traversa & Di Cesare, 2013). In fieldwork, individual administration of the formulation imidacloprid 10 % / moxidectin 1 % in naturally infected cats has been reported to be safe and effective. To improve clinical signs, supportive therapy is recommended to help respiratory function, eliminate secondary infection, and stimulate the appetite of affected cats (Gianelli et al., 2014).

Environmental changes resulting from global warming in addition to oral vaccination against rabies have significantly increased the population of wild carnivores, especially foxes (Ilić et al., 2016a). The population of foxes has to be considered as a constant reservoir of infection for domestic carnivores in suburban areas. therefore, data on the way of living and the territory of owned cats are very important to collect when taking anamnesis. Similarly, canine and feline stray populations have increased in both urban and suburban environments in Serbia (Đurić et al., 2011; Lažetić et al., 2012). Consequently, the increase in both populations of will and stray carnivores has contributed to significantly raise the population of possible reservoirs for pets, creating favorable conditions for the constant maintenance and spread of zoonotic parasites (Obrenovic et al., 2003; Nikolić et al., 2008; Ilić et al., 2017; Ilić et al., 2017a) including C. aerophila.

Because of the direct life cycle and zoonotic potential of C. aerophila, sanitary measures are necessary to control the disease, especially in living environments with larger groups of animals (Brianti et al., 2012; Gianelli et al., 2014; Brianeri et al., 2014).

Considering the zoonotic potential of C. aerophila and the spreading tendency of parasitic diseases caused by nematodes, more effort should be managed to achieve an accurate diagnosis of the causal organism. This study stressed out the importance of including parasitic diseases in the differential diagnosis of respiratory conditions in cats. Although allergic bronchitis is usually considered the most frequent cause of chronic cough in cats, it is recommended to delay the steroid therapy until a potential infection is excluded.

In humans, the disease is characterized by a non-specific clinical picture and is usually detected accidentally, which is the reason why prevention measures are essential in the fight against this parasitosis of cats. Finally, this study contributes to a better understanding of the epidemiology of respiratory capillariosis in the city of Belgrade and highlights the possibility of human infection due to the close contact between infected pet cats and their owners.