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New insights into the distribution of cardio-pulmonary nematodes in road-killed wild felids from Romania

Parasites & Vectors volume 15, Article number: 153 (2022) Cite this article

Abstract

Background

The population of wild felids is large and stable in Romania with many carnivore habitats being protected. Felids can be infected with a wide variety of cardio-pulmonary nematodes and can act as reservoirs of infection for domestic cats. The aim of this study was to evaluate the distribution and species diversity of cardio-pulmonary nematodes in wild felids from Romania.

Methods

A total of 54 wild felids (7 Lynx lynx and 47 Felis silvestris) were legally collected from different locations in Romania and analysed by complete parasitological necropsy. The entire respiratory tract was longitudinally opened and checked for the presence of nematodes. Detected nematodes were collected and morphologically identified to species level.

Results

Two Eurasian lynxes and 29 European wildcats were positive for cardio-pulmonary nematodes. Eurasian lynxes were infected with two species of cardio-pulmonary nematodes, Eucoleus aerophilus and Troglostrongylus brevior, while in wildcats the dominant parasite was E. aerophilus (34.0%) followed by Angiostrongylus chabaudi (23.4%) and T. brevior (14.9%). Dirofilaria immitis and Aelurostrongylus abstrusus were each detected in two wildcats (4.3%).

Conclusions

The present study expanded the epidemiological knowledge on felid cardiopulmonary nematodes in Romania. We confirmed the presence of A. abstrusus in wildcats and a patent infection with T. brevior in Eurasian lynx.

Graphical Abstract

Background

Cardio-pulmonary nematodes of wild and domestic felids have become increasingly popular among researchers in recent years, with a significant increase in published studies [1, 2]. However, most of these studies are focusing on domestic cats (Felis silvestris catus) [3,4,5,6,7] even though bridging infections are facilitated in areas where domestic cats share the habitat with wild felids [8, 9]. Among feline lungworms, Aelurostrongylus abstrusus (Metastrongyloidea, Angiostrongylidae) is known as the most important respiratory helminth, with a worldwide distribution, and may pose a health risk to infected animals [10]. Aelurostrongylosis in domestic cats can have various clinical manifestations, from mild clinical signs to severe pneumonia or even death in immunosuppressed cats [4, 11].

In the last years, infections of domestic and wild felines with Troglostrongylus brevior (Metastrongyloidea, Crenosomatidae) have gained attention, in some countries being the most frequent lungworm of domestic cats [5]. The genus Troglostrongylus includes five species that reside in the respiratory system of felids: T. troglostrongylus Vevers, 1922, T. brevior Gerichter 1949, T. subcrenatus Railliet and Henry, 1913, T. assadovi Sadykhov, 1952, and T. wilsoni Stough, 1953 [12]. Until recently, they were considered exclusively parasites of wild felids but, in the last decade, several papers have reported infections with T. brevior in domestic cats [6, 12,13,14,15,16]. Amidst wild felids, Troglostrongylus infection was reported in various species such as wildcats (Felis silvestris silvestris, Felis silvestris lybica, Felis chaus), leopard (Panthera pardus), tiger (Panthera tigris), bobcat (Lynx rufus) Canada lynx (Lynx canadensis), and lynx (Lynx lynx) [17, 18]. Troglostrongylus brevior was first described in F. s. lybica and F. chaus in Palestine [19] and further reported in countries where wildcats are present [14, 16, 20, 21]. In Romania, T. brevior was identified for the first time in a wildcat [20] and, more recently, in domestic cats [6]. Wildcats are the natural hosts for T. brevior and represent important reservoirs with prevalences of up to 71.4% in Italy [17]. Even though T. brevior infection seems to spread among the wild and domestic cats, there is only one report of infection in a Eurasian lynx from Bosnia and Herzegovina [18].

Angiostrongylus chabaudi Biocca, 1957 (Metastrongyloidea, Angiostrongylidae), described for the first time in Italy, resides in the pulmonary arteries and the right heart of felids. Since then, it has been reported again in Italy and several other European countries [22,23,24], including Romania [25]. Its life cycle is still not completely known, but, like other congeneric species, gastropods probably act as intermediate hosts [26, 27]. European wildcats represent the definitive hosts [23, 25], while there are no reports of natural patent infection in domestic cats [28, 29].

In addition, Eucoleus aerophilus and Dirofilaria immitis can infect the trachea and bronchi and the pulmonary arteries, respectively, of wildcats [30, 31], while Crenosoma vismani and Crenosoma sp. were recently reported from the bronchi and bronchioles of Eurasian lynx [32, 33]. Mixed infections with cardio-pulmonary nematodes were reported in wild felids [30,31,32, 34] and domestic cats [35].

In Romania, the population of wild felids is large and stable, and many carnivore habitats are protected [36, 37]. Overall, there are around 9000 Eurasian lynxes in Europe, from which about 2900 can be found in the Carpathian Mountains, and about 2000 live in Romania [38]. However, as Eurasian lynxes are elusive and protected animals, studies on their parasites are difficult and carcasses rarely available.

Considering the clinical relevance and apparent emergence of pulmonary nematodes, a constant epidemiological monitoring of wild felids is important, as they could represent reservoirs for domestic felids. With this view, the aim of the present study was to evaluate the distribution and species diversity of cardio-pulmonary nematodes infecting wild felids in Romania by parasitological necropsy. The rest of the detected parasites will be included in further studies.

Methods

Between 2014 and 2021, a total of 54 wild felids were legally collected from different locations in Romania and submitted to the Department of Parasitology of the University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca. Most animals included in this study were found as road kills, apart from two wildcats which died in two zoos, one from Reșița and one from Bucharest. The carcasses were kept at − 18 °C until examination. The animal species were identified based on their morphological characteristics, and wildcats were differentiated from domestic cats and hybrids based on the score obtained from the specific morphological characteristics [31]. The approximate age of the animals was established by dental examination [39, 40]. Details about the sex, approximate age, location, body condition, and date of the collection were recorded. Parasitological necropsy was performed to evaluate the lungworms. The trachea, bronchi, bronchioles, heart chambers, and pulmonary arteries were longitudinally opened and checked for the presence of nematodes under a stereo zoom microscope. The lungs were then immersed in tap water and squeezed several times, and the obtained sediment was examined diligently. The adult nematodes were collected and washed in saline solution and preserved in 2-ml labelled tubes with 70% ethanol. The nematodes were separated under a stereo zoom microscope based on their general morphology and location in the animal cardio-respiratory system. The morphological identification was performed for each of the collected specimens individually, using morphological descriptions [19, 25, 41] to genus and/or species level. When fresh carcasses were available (n = 1 for lynx and n = 4 for wildcats), the Baermann method [42] was carried out on the lungs to detect and collect metastrongyloid larvae (L1). Nematodes and larvae were measured and photographed using an optical microscope (Olympus BX 51, Soft Imaging solution GMBH LG20, Munster, Germany).

Genomic DNA was extracted from one nematode specimen collected from the trachea of a Eurasian lynx, using a commercial kit (Isolate II Genomic DNA Kit, Bioline, London, UK) according to the manufacturer’s instructions. The molecular characterization of the selected nematode was performed by amplification and external sequencing (Macrogen Europe B.V.) of fragments of various sizes of the cytochrome c oxidase subunit I (cox1) gene, using LCO1490/HCO2198 primers [43] and protocols available in literature. The attained sequences were compared to others available in the NCBI GenBank® database by means of Basic Local Alignment Search Tool (BLAST) analysis.

Pulmonary lesions were not evaluated because of the decomposition state of some of the carcasses and long-term freezing. The distribution map was elaborated using ArcMap 10.6.1 software. The statistical analysis was performed using EpiInfo™ 7.2.2.6 software (CDC, USA). The frequency, prevalence, and 95% confidence interval (CI) of infection with each species of parasite were calculated globally and according to multiple variables (host species, sex, age, and region of the country). The differences among groups were assessed by chi-square test and statistically significant for P values ≤ 0.05.

Results

Felids were morphologically identified as Eurasian lynxes, Lynx lynx (n = 7), and wildcats, Felis silvestris (n = 47). Among wildcats, only one carcass was identified as a hybrid, which was also included in the statistical analysis as a wildcat. Overall, 28.6% (n = 2) Eurasian lynxes and 61.7% (n = 29) wildcats were infected with cardio-pulmonary adult nematodes. Co-infections were detected in 14.3% (n = 1) of the Eurasian lynxes and 19.1% (n = 9) of the wildcats. Troglostrongylus sp. was detected in the bronchi of seven European wildcats (14.9%), including a previously published case report [20], and only one Eurasian lynx (14.3%). Morphological genus identification (Fig. 1) was based on the cuticle with fine transversal striations and inflated at the anterior end; the triangular oral opening surrounded by an inner and an outer circle, the latter consisting of pairs of papillae and two lateral amphids; the vulva opening located at middle of the body and the short and conical tail; the copulatory bursa of the males small and supported by rays. BLAST analysis revealed a 99.4% identity with a T. brevior isolate from a wildcat in Germany (GenBank accession number: KP641613). The sequence is available in GenBank under the accession no. OM283595. The first-stage larvae recovered from the lung tissue of the infected Eurasian lynx were morphologically consistent with those of Troglostrongylus sp. (Fig. 2).

Fig. 1
figure 1

Morphology of a female T. brevior. Posterior extremity of a female, lateral view (a). The anterior end with an inflated cuticle. The excretory pore is visible on the right lateral part (b). Scale bar = 200 µm

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Fig. 2
figure 2

First-stage larva of T. brevior recovered using the Baermann method from the lung tissue of the positive Lynx lynx. The subterminal oral opening (arrowhead) is evident and the deep dorsal notch (black arrow). Scale bar = 100 µm

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Besides T. brevior, four other species of cardio-pulmonary nematodes were detected, namely E. aerophilus, A. abstrusus (Fig. 3) (4.3%, n = 2 in wildcats), A. chabaudi (23.4%, n = 11 in wildcats), and D. immitis (Fig. 4) (4.3%, n = 2 in wildcats). Eucoleus aerophilus adults collected from the trachea were identified based on their specific morphology [41] with 28.6% (n = 2) prevalence in Eurasian lynx and 34.0% (n = 16) in wildcats. Infections with A. abstrusus, A. chabaudi and D. immitis were not detected in Eurasian lynxes from Romania (Table 1). There were no statistically significant differences in the prevalence between age and sex categories for any nematode species. A statistically significant difference (chi-square test, χ2 = 12.228, df = 4, P < 0.015) was found for wildcats infected with D. immitis from different regions of Romania, with a higher prevalence in south and south-east Romania. Locations of the positive and negative animals and the distribution map of all pulmonary nematode species are shown in Fig. 5. The complete statistical description is available in Additional file 1, whereas the complete database is shown in Additional file 2.

Fig. 3
figure 3

First-stage larva of A. abstrusus recovered using the Baermann method from the lung tissue of a wildcat. Note the terminal oral opening (black arrowhead), deep ventral notch, and three small knobs (black arrow). Scale bar = 100 µm

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Fig. 4
figure 4

Presence of D. immitis in the thoracic cavity of a wildcat. The pulmonary artery was accidentally punctured during necropsy and the adult nematode was exteriorised

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Table 1 Prevalence of cardio-pulmonary nematodes in wild felids from Romania (given in %)
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Fig. 5
figure 5

Distribution of the cardio-pulmonary nematodes identified in Romanian felids

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Discussion

Helminthological surveys on wild felids are rare; however, in the last few years, this topic has gained more interest among researchers [1, 31]. The vast majority of studies on wild felid populations are restricted to a specific group of helminths or to specific areas or countries [24, 25, 31]. Wild felids are important reservoirs for cardio-pulmonary nematodes, and they are frequently infected with more than one species, as shown in the present study, with 19.1% (n = 9) coinfected wildcats, representing 31.0% of all infected. A recent study on endoparasites of wildcats in Greece reported polyparasitism with up to five different species of cardio-pulmonary nematodes [31]. The most prevalent lungworm in wildcats from Greece was A. chabaudi (56.5%), followed by A. abstrusus (43.5%) and T. brevior (34.8%). In contrast to the previously mentioned study [31], the dominant parasite in wildcats from Romania was E. aerophilus followed by A. chabaudi and T. brevior. Interestingly, the prevalence of A. abstrusus in wildcats is lower than in domestic cats in Romania [6]. This may be related to the diagnostic method (necropsy), as adult worms are localized in the pulmonary parenchyma and the infection can be easily missed [31], but also to different ecological niches of domestic vs. wildcats [2]. Diagnosis by parasitological necropsy may have disadvantages too, like missing some parasitic infections because of the detection of only adult parasites, which sometimes can be missed as previously reported [18].

The presence of D. immitis in Romania is known and has been well studied in both domestic and wild animals, including felids [30, 44,45,46], with higher prevalence values in the southern part of the country in relation to a warmer climate [44, 45]. In accordance with the known data, the prevalence in felid hosts is very low, as shown in the present case. Interestingly, there are no reports of D. immitis in Eurasian lynx (Lynx lynx), which could be related to the lower number of studies or examined animals, its unsuitability as a host, or the lower infection risk associated with the higher altitudes [47] where lynxes are generally more common.

Troglostrongylus brevior was previously detected only in one Eurasian lynx from Bosnia and Herzegovina [18]. However, there are some studies that investigated the helminth fauna of this host in Europe [33, 48,49,50,51]. Previously, T. assadovi was described from the same animal host in Azerbaijan [52], but no other mention of this species has been available since its original description. Interestingly, Troglostrongylus spp. were reported more often in bobcats (Lynx rufus) and Canada lynxes (Lynx canadensis) from North America [53,54,55]. Moreover, there is always a possibility of misidentification of the larvae with A. abstrusus [56], a parasite also known to infect L. lynx [57]. More recently, in a study conducted on the population of Eurasian lynx in Germany, the authors identified only Crenosoma and Angiostrongylus larvae [32], even though T. brevior was reported in wildcats in Germany [22]. Severe histological lesions were detected in both domestic and wild felids and the life-threatening potential of these nematodes was underlined [18, 58]. Troglostrongylus brevior often produces fatal bronchopneumonia in kittens and juvenile cats; however, clinical signs in adult felines are rare [59]. In the present study, all the examined animals had a good body state, but unfortunately the presence and severity of the cardio-respiratory lesions could not be determined because of long-time freezing and partial decomposition of the carcasses.

Overall, the significance of our results could have implications for both wildlife and companion animal medicine. As recently reviewed by Morelli et al. [9], three species inhabiting the airways of domestic cats are clinically relevant: A. abstrusus, T. brevior, and E. aerophilus. All seem to be expanding in distribution [2]. Our results highlighted the role of wild felids as reservoirs of infection for domestic cats in Romania.

Conclusion

In this large-scale survey on the cardio-pulmonary nematodes of wild felids in Romania, we detected a significant variety of cardio-pulmonary nematodes. Infection with A. abstrusus was confirmed in wildcats for the first time in Romania. We confirm the Eurasian lynx as a host of patent infection with T. brevior.

Availability of data and materials

All data generated or analyzed during this study are included in this published article and its additional files. Other information is available from the corresponding author on reasonable request.

References

  1. Stevanović O, Diakou A, Morelli S, Paraš S, Trbojević I, Nedić D, et al. Severe verminous pneumonia caused by natural mixed infection with Aelurostrongylus abstrusus and Angiostrongylus chabaudi in a European wildcat from Western Balkan area. Acta Parasitol. 2019;64:411–7.

    Article  PubMed  Google Scholar 

  2. Traversa D, Morelli S, Di Cesare A, Diakou A. Felid cardiopulmonary nematodes: dilemmas solved and new questions posed. Pathogens. 2021;10:30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bulbul KH, Akand AH, Choudhury D, Begam R, Hussain J, Hussain I, et al. An update of lungworm infection in cat with especial reference to aelurostrongylosis. IJVSAH. 2020;5:37–9.

    Google Scholar 

  4. Morelli S, Diakou A, Di Cesare A, Schnyder M, Colombo M, Strube C, et al. Feline lungworms in Greece: copromicroscopic, molecular and serological study. Parasitol Res. 2020;119:2877–83.

    Article  PubMed  Google Scholar 

  5. Salant H, Yasur-Landau D, Rojas A, Otranto D, Mazuz ML, Baneth G. Troglostrongylus brevior is the dominant lungworm infecting feral cats in Jerusalem. Parasitol Res. 2020;119:3443–50.

    Article  CAS  PubMed  Google Scholar 

  6. Gyӧrke A, Dumitrache MO, Kalmár Z, Paştiu AI, Mircean V. Molecular survey of metastrongyloid lungworms in domestic cats (Felis silvestris catus) from Romania: a retrospective study (2008–2011). Pathogens. 2020;9:80.

    Article  PubMed Central  Google Scholar 

  7. Lopez-Osorio S, Navarro-Ruiz JL, Rave A, Taubert A, Hermosilla C, Chaparro-Gutierrez JJ. Aelurostrongylus abstrusus infections in domestic cats (Felis silvestris catus) from Antioquia, Colombia. Pathogens. 2021;10:337.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Traversa D, Di Cesare A. Diagnosis and management of lungworm infections in cats: cornerstones, dilemmas and new avenues. J Feline Med Surg. 2016;18:7–20.

    Article  PubMed  Google Scholar 

  9. Morelli S, Diakou A, Colombo M, Di Cesare A, Barlaam A, Dimzas D, Traversa D. Cat respiratory nematodes: current knowledge, novel data and warranted studies on clinical features, treatment and control. Pathogens. 2021;10:454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Traversa D, Veronesi F, Diakou A, Iorio R, Simonato G, Marcer F, et al. Mitochondrial haplotypes of Aelurostrongylus abstrusus and Troglostrongylus brevior (Nematoda, Metastrongyloidea) from domestic and wild felids. Parasitol Res. 2017;116:1227–35.

    Article  PubMed  Google Scholar 

  11. Crisi PE, Aste G, Traversa D, Di Cesare A, Febo E, Vignoli M, et al. Single and mixed feline lungworm infections: clinical, radiographic and therapeutic features of 26 cases (2013–2015). J Feline Med Surg. 2017;19:1017–29.

    Article  PubMed  Google Scholar 

  12. Brianti E, Giannetto S, Dantas-Torres F, Otranto D. Lungworms of the genus Troglostrongylus (Strongylida: Crenosomatidae): neglected parasites for domestic cats. Vet Parasitol. 2014;202:104–12.

    Article  CAS  PubMed  Google Scholar 

  13. Jefferies R, Vrhovec MG, Wallner N, Catalan DR. Aelurostrongylus abstrusus and Troglostrongylus sp. (Nematoda: Metastrongyloidea) infections in cats inhabiting Ibiza, Spain. Vet Parasitol. 2010;173:344–8.

    Article  PubMed  Google Scholar 

  14. Diakou A, Di Cesare A, Barros LA, Morelli S, Halos L, Beugnet F, et al. Occurrence of Aelurostrongylus abstrusus and Troglostrongylus brevior in domestic cats in Greece. Parasit Vectors. 2015;8:590.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Diakou A, Sofroniou D, Di Cesare A, Kokkinos P, Traversa D. Occurrence and zoonotic potential of endoparasites in cats of Cyprus and a new distribution area for Troglostrongylus brevior. Parasitol Res. 2017;116:3429–35.

    Article  PubMed  Google Scholar 

  16. Giannelli A, Capelli G, Hinney B, Joachim A, Losson B, Kirkova Z, et al. Epidemiology, diagnosis and treatment of lungworm and gastrointestinal parasitic infections in cats: an European perspective. Int J Parasitol. 2017;47:517–28.

    Article  PubMed  Google Scholar 

  17. Falsone L, Brianti E, Gaglio G, Napoli E, Anile S, Mallia E, et al. The European wildcats (Felis silvestris silvestris) as reservoir hosts of Troglostrongylus brevior (Strongylida: Crenosomatidae) lungworms. Vet Parasitol. 2014;205:193–8.

    Article  CAS  PubMed  Google Scholar 

  18. Alić A, Traversa D, Duscher GG, Kadrić M, Di Cesare A, Hodžić A. Troglostrongylus brevior in an Eurasian lynx (Lynx lynx) from Bosnia and Herzegovina. Parasit Vectors. 2015;8:1–5.

    Article  CAS  Google Scholar 

  19. Gerichter CB. Studies on the nematodes parasitic in the lungs of Felidae in Palestine. Parasitol. 1949;39:251–62.

    Article  CAS  Google Scholar 

  20. Deak G, Ionică AM, Mihalca AD, Gherman CM. Troglostrongylus brevior: a new parasite for Romania. Parasit Vectors. 2017;10:1–4.

    Article  CAS  Google Scholar 

  21. Umur S, Barılı Ö, Topçu EBG, Gürler AT. First report of a Troglostrongylus brevior case in a domestic cat in Turkey. Turk J Parasitol. 2020;44:176–8.

    Article  Google Scholar 

  22. Steeb S, Hirzmann J, Eskens U, Volmer K, Bauer C. Lungenwurm Infektionen bei der Europischen Wildkatze. Kompakt Vet. 2014;3:9 (in German).

    Google Scholar 

  23. Diakou A, Psalla D, Migli D, Di Cesare A, Youlatos D, Marcer F, et al. First evidence of the European wildcat (Felis silvestris silvestris) as definitive host of Angiostrongylus chabaudi. Parasitol Res. 2016;115:1235–44.

    Article  PubMed  Google Scholar 

  24. Veronesi F, Traversa D, Lepri E, Morganti G, Vercillo F, Grelli D, et al. Occurrence of lungworms in European wildcats (Felis silvestris silvestris) of central Italy. J Wildl Dis. 2016;52:270–8.

    Article  CAS  PubMed  Google Scholar 

  25. Gherman CM, Ionică AM, D’Amico G, Otranto D, Mihalca AD. Angiostrongylus chabaudi (Biocca, 1957) in wildcat (Felis silvestris silvestris, S) from Romania. Parasitol Res. 2016;115:2511–7.

    Article  PubMed  Google Scholar 

  26. Colella V, Cavalera MA, Deak G, Tarallo VD, Gherman CM, Mihalca AD, et al. Larval development of Angiostrongylus chabaudi, the causative agent of feline angiostrongylosis, in the snail Cornu aspersum. Parasitol. 2017;144:1922–30.

    Article  CAS  Google Scholar 

  27. Dimzas D, Morelli S, Traversa D, Di Cesare A, Van Bourgonie YR, Breugelmans K, et al. Intermediate gastropod hosts of major feline cardiopulmonary nematodes in an area of wildcat and domestic cat sympatry in Greece. Parasit Vectors. 2020;13:345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Varcasia A, Tamponi C, Brianti E, Cabras PA, Boi R, Pipia AP, et al. Angiostrongylus chabaudi Biocca, 1957: a new parasite for domestic cats? Parasit Vectors. 2014;17:588.

    Article  Google Scholar 

  29. Di Cesare A, Morelli S, Colombo M, Simonato G, Veronesi F, Marcer F, et al. Is angiostrongylosis a realistic threat for domestic cats? Front Vet Sci. 2020;7:195.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Gherman CM, Ionică AM, Deak G, Chișamera GB, Mihalca AD. Co-infection with Angiostrongylus chabaudi and Dirofilaria immitis in a wildcat, Felis silvestris from Romania—a case report. Act Vet Brno. 2019;88:303–6.

    Article  Google Scholar 

  31. Diakou A, Migli D, Dimzas D, Morelli S, Di Cesare A, Youlatos D, et al. Endoparasites of European Wildcats (Felis silvestris) in Greece. Pathogens. 2021;10:594.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Segeritz L, Velez J, Anders O, Middelhoff L, Taubert A, Hermonsilla C. Autochthonous Angiostrongylus sp. and Crenosoma sp. infections is wild Eurasian lynx (Lynx lynx) in Germany and new insights into lynx gastrointestinal parasite fauna. In: poster presentation during WAAVP conference, Dublin 2021.

  33. Stunžėnas V, Binkienė R. Description of Crenosoma vismani n. sp., parasitic in the lungs of Lynx lynx (L.) (Carnivora: Felidae), with identification key to the species of the genus Crenosoma Molin, 1861 (Nematoda: Crenosomatidae). Syst Parasitol. 2021;98:73–83.

    Article  PubMed  Google Scholar 

  34. Diakou A, Dimzas D, Astaras C, Savvas I, Di Cesare A, Morelli S, et al. Clinical investigations and treatment outcome in a European wildcat (Felis silvestris silvestris) infected by cardio-pulmonary nematodes. Vet Parasitol Reg Stud Rep. 2020;19:100357.

    Google Scholar 

  35. Traversa D, Lepri E, Veronesi F, Simonato G, Diaferia M, Di Cesare A. Metastrongyloid infection by Aelurostrongylus abstrusus, Troglostrongylus brevior and Angiostrongylus chabaudi in a domestic cat. Int J Parasitol. 2015;45:685–90.

    Article  PubMed  Google Scholar 

  36. Yamaguchi N, Kitchener A, Driscoll C, Nussberger B. Felis silvestris. IUCN Red List Threat Species. 2015. https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T60354712A50652361.en.

    Article  Google Scholar 

  37. Cristescu B, Domokos C, Teichman KJ, Nielsen SE. Large carnivore habitat suitability modelling for Romania and associated predictions for protected areas. PeerJ. 2019;7: e6549. https://doi.org/10.7717/peerj.6549.

    Article  PubMed  PubMed Central  Google Scholar 

  38. https://wwf.ro/ce-facem/specii/rasul/. Accessed Nov 2021.

  39. Condé B, Schauenberg P. Replacement des canines chez le chat forestier Felis silvestris Schreb. Rev Suisse Zool. 1978;85:241–5.

    Article  PubMed  Google Scholar 

  40. Marti I, Ryser-Degiorgis MP. A tooth wear scoring scheme for age estimation of the Eurasian lynx (Lynx lynx) under field conditions. Eur J Wildl Res. 2018;64:1–13.

    Article  Google Scholar 

  41. Anderson R, Chabaud A, Willmot S. Keys to the nematode parasites of vertebrates, vol. Archival. Wallingford: Cabi; 2009.

    Book  Google Scholar 

  42. Willcox HP, Coura JR. A new design of the Baermann, Moraes, Coutinho’s technique for the isolation of nematode larva. Mem Inst Oswaldo Cruz. 1989;84:563–5 (in Portuguese).

    Article  CAS  PubMed  Google Scholar 

  43. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.

    CAS  PubMed  Google Scholar 

  44. Ionică AM, Matei IA, Mircean V, Dumitrache MO, D’Amico G, Győrke A, et al. Current surveys on the prevalence and distribution of Dirofilaria spp. and Acanthocheilonema reconditum infections in dogs in Romania. Parasitol Res. 2015;114:975–82.

    Article  PubMed  Google Scholar 

  45. Ionică AM, Matei IA, D’Amico G, Daskalaki AA, Juránková J, Ionescu DT, et al. Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania. Parasit Vectors. 2016;9:1–6.

    Article  CAS  Google Scholar 

  46. Pană D, Rădulescu A, Mitrea IL, Ionita M. First report on clinical feline heartworm (Dirofilaria immitis) infection in Romania. Helminthol. 2020;57:49.

    Article  Google Scholar 

  47. Angelou A, Gelasakis AI, Verde N, Pantchev N, Schaper R, Chandrashekar R, et al. Prevalence and risk factors for selected canine vector-borne diseases in Greece. Parasit Vectors. 2019;12:283.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Schmidt-Posthaus H, Breitenmoser-Wörsten C, Posthaus H, Bacciarini L, Breitenmoser U. Causes of mortality in reintroduced Eurasian lynx in Switzerland. J Wildl Dis. 2002;38:84–92.

    Article  PubMed  Google Scholar 

  49. Valdmann H, Moks E, Talvik H. Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia. J Widl Dis. 2004;40:356–60.

    Article  CAS  Google Scholar 

  50. Szczęsna J, Popiołek M, Schmidt K, Kowalczyk R. Coprological study on helminth fauna in Eurasian Lynx (Lynx lynx) from the Białowieża Primeval Forest in eastern Poland. J Paras. 2008;94:981–4.

    Article  Google Scholar 

  51. Deksne G, Laakkonen J, Näreaho A, Jokelainen P, Holmala K, Kojola I, Sukura A. Endoparasites of the Eurasian lynx (Lynx lynx) in Finland. J Paras. 2013;99:229–34.

    Article  Google Scholar 

  52. Sadikhov IA. Troglostrongylus assadovi n sp from Felts (Lynx) lynx in Azerbaidhan. Mä'ruzälär. 1952;8:311–4 (in Russian).

  53. Sarmiento L, Stough BD. Troglostrongylus wilsoni (Stough, 1953) n. comb. (Nematoda: Metastrongylidae) from the lungs of the bobcat, Lynx rufus rufus. J Parasitol. 1956;42:45–8.

    Article  CAS  PubMed  Google Scholar 

  54. Smith JD, Addison EM, Joachim DG, Smith LM, Quinn NWS. Helminth parasites of Canada lynx (Felis canadensis) from northern Ontario. Can J Zool. 1986;64:358–64.

    Article  Google Scholar 

  55. Reichard MV, Caudell DL, Kocan AA. Survey of helminth lung parasites of bobcats (Lynx rufus) from Alabama, Kansas, New Mexico, Oklahoma, and Virginia, U.S.A. Comp Parasitol. 2004;71:88–90.

    Article  Google Scholar 

  56. Brianti E, Gaglio G, Giannetto S, Annoscia G, Latrofa MS, Dantas-Torres F, et al. Troglostrongylus brevior and Troglostrongylus subcrenatus (Strongylida: Crenosomatidae) as agents of broncho-pulmonary infestation in domestic cats. Parasit Vectors. 2012;5:178.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Otranto D, Brianti E, Dantas-Torres F. Troglostrongylus brevior and a nonexistent ‘dilemma.’ Trends Parasitol. 2013;29:517–8.

    Article  PubMed  Google Scholar 

  58. Giannelli A, Passantino G, Ramos RAN, Presti GL, Lia RP, Brianti E, et al. Pathological and histological findings associated with the feline lungworm Troglostrongylus brevior. Vet Paras. 2014;204:416–9.

    Article  Google Scholar 

  59. Traversa D, Di Cesare A. Cardio-pulmonary parasitic nematodes affecting cats in Europe: unravelling the past, depicting the present, and predicting the future. Front Vet Sci. 2014;1:11.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank our dear students, especially Alexandru Felea, Andreea Iani, and Mihai Ilea, who helped with the collection of carcasses and who participated in the post-mortem examinations of the felids. We also thank all the people involved in the collection of the carcasses: Alexandru Sarmași, Ana Maria Balea, Alexandru Bulacu, and Grigore Antipa National History Museum.

Funding

This work was supported by an internal Grant of USAMVCN nr.21659/1.10.2021.

Author information

Authors and Affiliations

  1. Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372, Cluj-Napoca, Romania

    Georgiana Deak, Andrei Daniel Mihalca & Călin Mircea Gherman

  2. Molecular Biology and Veterinary Parasitology Unit (CDS 9), “Regele Mihai I Al României” Life Science Institute, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăştur 3-5, 400372, Cluj-Napoca, Romania

    Angela Monica Ionică

  3. Molecular Diagnosis Laboratory, Clinical Hospital of Infectious Diseases of Cluj-Napoca, 23 Iuliu Moldovan, 400348, Cluj-Napoca, Romania

    Angela Monica Ionică

  4. Department and Clinic of Reproduction, Obstetrics and Gynaecology, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372, Cluj-Napoca, Romania

    Raul Alexandru Pop

Authors
  1. Georgiana Deak
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  2. Angela Monica Ionică
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  3. Raul Alexandru Pop
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  4. Andrei Daniel Mihalca
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  5. Călin Mircea Gherman
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Contributions

GD performed the necropsies, identified the parasites, and wrote the manuscript. AMI performed the molecular biology work and the statistical analysis. RAP helped with the collection of carcasses. ADM substantively revised the manuscript. CMG coordinated the study. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Andrei Daniel Mihalca.

Ethics declarations

Ethics approval and consent to participate

The wild felids included in this study were legally collected—Ethical Committee Decision No. 232/23.11.2020. All the activities were performed according to ethical permits and national legislation.

Consent for publication

Not applicable.

Competing interests

Andrei Daniel Mihalca is an AE for Ticks and Tick-borne Diseases section.

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Supplementary Information

Additional file 1: Table S1.

Prevalences of cardio-respiratory nematodes in wildcats and lynxes. Table S2. Prevalences of cardio-pulmonary nematodes in wildcats by their sex. Table S3. Prevalences of cardio-pulmonary nematodes in wildcats by their age. Table S4. Prevalences of cardio-pulmonary nematodes in wildcats by their geographical location.

Additional file 2: Table S5.

The exact location of each examined cat, their age sex, and positivity to lungworms.

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Deak, G., Ionică, A.M., Pop, R.A. et al. New insights into the distribution of cardio-pulmonary nematodes in road-killed wild felids from Romania. Parasites Vectors 15, 153 (2022). https://doi.org/10.1186/s13071-022-05281-z

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Keywords

Parasites & Vectors

ISSN: 1756-3305

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