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Troglostrongylus brevior is the dominant lungworm infecting feral cats in Jerusalem

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Abstract

Feline lungworms infect the respiratory tract of wild and domestic cats, causing infection often associated with clinical disease. Until recently, Aelurostrongylus abstrusus has been considered the most relevant species of lungworm, while Troglostrongylus brevior was considered of less significance. Fecal samples of feral cats from Jerusalem, Israel, collected over a year, were examined for first stage lungworm larvae (L1) using the Baermann method. Positive samples were morphologically identified, and their species identity was molecularly confirmed. Forty of 400 (10.0%) cats were lungworm-positive, of which 38/40 (95.0%) shed Troglostrongylus brevior and 6/40 (15.0%) shed Aelurostrongylus abstrusus. Four cats (10.0%) had mixed infections with both lungworm species. L1 shedding was associated with clinical respiratory signs in 11 (19.0%) T. brevior shedding cats of a total of 58 cats manifesting respiratory signs, while 23/342 (6.7%) cats without respiratory signs were L1-positive (p = 0.006). Non-respiratory clinical signs were also found to be more prevalent in L1 shedders (p = 0.012). A young kitten ≤ 4 weeks of age shed T. brevior L1 larvae. DNA sequences of both lungworm species using the ribosomal internal transcribed spacer 2 (ITS2) locus were > 99% similar to other sequences deposited in GenBank, suggesting that T. brevior and A. abstrusus ITS2 sequences are both highly conserved. In conclusion, L1 shedding in feral cats from Jerusalem were mostly caused by T. brevior with only a small proportion involving A. abstrusus, different from many studies from other geographical regions.

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References

  • Annoscia G, Latrofa MS, Campbell BE, Giannelli A, Ramos RAN, Torres FD, Brianti E, Otranto D (2014) Simultaneous detection of the feline lungworms Troglostrongylus brevior and Aelurostrongylus abstrusus by a newly developed duplex-PCR. Vet Parasitol 199:172–178

    Article  CAS  Google Scholar 

  • Bezerra-Santos MA, Mendonza-Roldan JA, Abramo F, Lia RP, Tarallo VD, Salant H, Brianti E, Baneth G, Otranto D (2020) Transmammary transmission of Troglostrongylus brevior feline lungworm: a lesson from our gardens. Vet Parasitol. https://doi.org/10.1016/j.vetpar.2020.109215

    Article  PubMed  PubMed Central  Google Scholar 

  • Brianti E, Gaglio G, Giannetto S, Annoscia G, Stefania Latrofa M, Dantas-Torres F, Traversa DE, Otranto D (2012) Troglostrongylus brevior and Troglostrongylus subcrenatus (Strongylida: Crenosomatidae) as agents of broncho-pulmonary infestation in domestic cats. Parasites Vectors. 5:178

    Article  Google Scholar 

  • Brianti E, Gaglio G, Napoli E, Falsone L (2013) Evidence for direct transmission of the cat lungworm Troglostrongylus brevior (Strongylida: Crenosomatidae). Parasitology 140:821–824

    Article  Google Scholar 

  • Brianti E, Giannetto S, Dantas-Torres F, Ortranto D (2014) Lungworms of the genus Troglostrongylus (Strongylida: Crenosomatidae): neglected parasites for domestic cats. Vet Parasitol 202:104–112

    Article  CAS  Google Scholar 

  • Capári B, Hamel D, Visser M, Winter R, Pfister K, Rehbein S (2012) Parasitic infections of domestic cats, Felis catus, in western Hungary. VetParasitol 192. https://doi.org/10.1016/j.vetpar.2012.11.011

  • Cavalera MA, Iatta R, Colella V, Dantas-Torres F, Corsaro A, Brianti E, Otranto D (2018) Troglostrongylus brevior: a feline lungworm of paediatric concern. Vet Parasitol 253:8–1

    Article  Google Scholar 

  • Conboy G (2009) Helminth parasites of the canine and feline respiratory tract. Vet Clin North Am Small Anim Pract 39:1109–1126

    Article  Google Scholar 

  • Crisi PE, Aste G, Traversa D, Di Cesare A, Febo E, Vignoli M, Santori D, Luciani A, Boari A (2017) Single and mixed feline lungworm infections: clinical, radiographic and therapeutic features of 26 cases (2013–2015). J Feline Med Surg 19(10):1017–1029

    Article  Google Scholar 

  • Deak G, Ionică AM, Mihalca AD, Gherman CM (2017) Troglostrongylus brevior: a new parasite for Romania. Parasites and Vectors 10:599

    Article  Google Scholar 

  • Di Cesare A, Crisi PE, di Giulio E, Veronesi F, di Regalbono AF, Talone T, Traversa D (2013) Larval development of the feline lungworm Aelurostrongylus abstrusus in Helix aspersa. Parasitol Res 112:3101–3108

    Article  Google Scholar 

  • Di Cesare A, di Regalbono AF, Tessarin C, Seghetti M, Iorio R, Simonato G, Traversa D (2014) Mixed infection by Aelurostrongylus abstrusus and Troglostrongylus brevior in kittens from the same litter in Italy. Parasitol Res 113(2):613–618

    Article  Google Scholar 

  • Di Cesare A, Veronesi F, Grillotti E, Manzocchi S, Perrucci S, Beraldo P, Cazzin S, De Liberato C, Barros LA, Simonato G, Traversa D (2015) Respiratory nematodes in cat populations of Italy. Parasitol Res 114:4463–4469

    Article  Google Scholar 

  • Diakou A, di Cesare A, Aeriniotaki T, Traversa D (2014) First report of Troglostrongylus brevior in a kitten in Greece. Parasitol Res 113:3895–3898

    Article  Google Scholar 

  • Diakou A, Di Cesare A, Barros LA, Morelli S, Halos L, Beugnet F, Traversa D (2015) Occurrence of Aelurostrongylus abstrusus and Troglostrongylus brevior in domestic cats in Greece. Parasites Vectors 8:590

    Article  Google Scholar 

  • Elsheikha HM, Schnyder M, Traversa D, Di Cesare A, Wright I, Lacher DW (2016) Updates on feline aelurostrongylosis and research priorities for the next decade. Parasites and. Vectors 9(1):389

    Article  Google Scholar 

  • Falsone L, Brianti E, Gaglio G, Napoli E, Anile S, Mallia E, Giannelli A, Poglayen G, Giannetto S, Otranto D (2014) The European wildcats (Felis silvestris silvestris) as reservoir hosts of Troglostrongylus brevior (Strongylida: Crenosomatidae) lungworms. Vet Parasitol 205(1–2):193–198

    Article  CAS  Google Scholar 

  • Gasser RB, Chilton NB, Hoste H, Beveridge I (1993) Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res 21(10):2525–2526

    Article  CAS  Google Scholar 

  • Gerichter CB (1949) Studies on the nematodes parasitic in the lungs of felidae in Palestine. Parasitology 39:251–262

    Article  CAS  Google Scholar 

  • Giannelli A, Passantino G, Nascimento Ramos RA, Lo Presti G, Lia RP, Brianti E, Dantas-Torres F, Papadopoulos E, Otranto D (2014) Pathological and histological findings associated with the feline lungworm Troglostrongylus brevior. Vet Parasitol 204:416–419

    Article  Google Scholar 

  • Giannelli A, Capelli G, Joachim A, Hinney B, Losson B, Kirkova Z, René-Martellet M, Papadopoulos E, Farkas R, Napoli E, Brianti E, Tamponi C, Varcasia A, Margarida A, de Carvalho AL, Cardoso L, Maia C, Mircean V, Mihalca AD, Miró G, Schnyder M, Cantacessi C, Colella V, Cavalera MA, Latrofa MS, Annoscia G, Knaus M, Halos L, Beugnet F, Otranto D (2017) Lungworms and gastrointestinal parasites of domestic cats: a European perspective. Int J Parasitol 47(9):517–528

    Article  Google Scholar 

  • Györke A, Dumitrache MO, Kalmár Z, Pastiu AI, Mircean V (2020) Molecular survey of Metastrongyloid lungworms in domestic cats (Felis silvestris catus) from Romania: a retrospective study (2008–2011). Pathogens 9:80

    Article  Google Scholar 

  • Jefferies R, Vrhovec MG, Wallner N, Catalan DR (2010) Aelurostrongylus abstrusus and Troglostrongylus sp. (Nematoda: Metastrongyloidea) infections in cats inhabiting Ibiza, Spain. Vet Parasitol 173:344–348

    Article  Google Scholar 

  • Kiszely S, Yurrkovsky MG, Solymosi N, Farkas F (2019) Survey of lungworm infection of domestic cats in Hungary. Acta Vet Hung 67(3):407–417

    Article  Google Scholar 

  • Knaus M, Kusi I, Rapti D, Xhaxhiu D, Winter R, Visser M, Rehbein R (2011) Endoparasites of cats from the Tirana area and the first report on Aelurostrongylus abstrusus (Railliet, 1898) in Albania. Wien Klin Wochenschr 123:31–35

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Mendoza-Roldan JA, Modry D, Otranto D (2020) Zoonotic parasites of reptiles: a crawling threat. Trends Parasitol 36(8):677–687. https://doi.org/10.1016/j.pt.2020.04.014

    Article  PubMed  PubMed Central  Google Scholar 

  • Pennisi M-G, Hartmann K, Addie DD, Boucraut-Baralon C, Egberink H, Frymus T, Gruffydd-Jones T, Horzinek MC, Hosie MJ, Lloret A, Lutz H, Marsilio F, Radford AD, Thiry E, Truyen U, Möstl K (2015) Lungworm disease in cats: ABCD guidelines on prevention and management. J Fel Med Surg 17:626–636

    Article  Google Scholar 

  • Ribeiro VM, Lima WS (2001) Larval production of cats infected and re-infected with Aelurostrongylus abstrusus (Nematoda: Protostrongylidae). Rev Med Vet 152:815–829

    Google Scholar 

  • Riggio F, Mannella R, Ariti G, Perrucci S (2013) Intestinal and lung parasites in owned dogs and cats from central Italy. Vet Parasitol 193(1–3):78–84

    Article  Google Scholar 

  • Roll U, Dayan T, Simberloff D, Mienis HK (2009) Non-indigenous land and freshwater gastropods in Israel. Biol Invasions 11:1963–1972

    Article  Google Scholar 

  • Schnyder M, Di Cesare A, Basso W, Guscetti F, Riond B, Glaus T, Crisi P, Deplazes P (2014) Clinical, laboratory and pathological findings in cats experimentally infected with Aelurostrongylus abstrusus. Parasitol Res 113:1423–1433

    Article  Google Scholar 

  • Scott DW (1973) Current knowledge of aelurostrongylosis in the cat. Literature review and case reports. Cornell Vet 63:483–500

    CAS  PubMed  Google Scholar 

  • Tamponi C, Varcasia A, Brianti E, Pipia AP, Frau V, Pinna Parpaglia ML, Sanna G, Garippa G, Otranto D, Scala A (2014) New insights on metastrongyloid lungworms infecting cats of Sardinia. ItalyVet Parasitol 203:222–226

    CAS  Google Scholar 

  • Traversa D, di Cesare A (2013) Feline lungworms: what a dilemma. Trends Parasitol 29:423–430

    Article  Google Scholar 

  • Traversa D, Di Cesare A (2016) Diagnosis and management of lungworm infections in cats. Cornerstones, dilemmas and new adventures. J Feline Med Surg 18:7–20

    Article  Google Scholar 

  • Traversa D, Guglielmini C (2008) Feline aelurostrongylosis and canine angiostrongylosis: a challenging diagnosis for two emerging verminous pneumonia infections. Vet Parasitol 157:163–174

    Article  Google Scholar 

  • Traversa D, Lia RP, Iorio R, Boari A, Paradies P, Capelli G, Avolio S, Otranto D (2008a) Diagnosis and risk factors of Aelurostrongylus abstrusus (Nematoda, Strongylida) infection in cats from Italy. Vet Parasitol 153:182–186

    Article  Google Scholar 

  • Traversa D, Iorio R, Otranto D (2008b) Diagnostic and clinical implications of a nested PCR specific for ribosomal DNA of the feline lungworm Aelurostrongylus abstrusus (Nematoda, Strongylida). J Clin Microbiol 46(5):1811–1817

  • Traversa D, Di Cesare A, Conboy G (2010) Canine and feline cardiopulmonary parasitic nematodes in Europe: emerging and underestimated. Parasite Vectors 3:62

    Article  Google Scholar 

  • Traversa D, Lepri E, Veronesi F, Paoletti B, Simonato G, Diaferia M, Di Cesare A (2015) Metastrongyloid infection by Aelurostrongylus abstrusus, Troglostrongylus brevior and Angiostrongylus chabaudi in a domestic cat. Int J Parasitol 45:685–690

    Article  Google Scholar 

  • Watson JM, Al-Hafidh R (1957) A modification of the Baermann funnel technique, and its use in establishing the infection potential of human hookworm-carriers. Annals Trop Med Parasitol 51(1):15–16

    Article  CAS  Google Scholar 

  • Yasur-Landau D, Rojas A, Zehavi T, YafeY AY, Baneth G (2019) First molecular identification of Aelurostrongylus abstrusus in a cat presenting severe respiratory disease from Israel. Vet Parasitol: Regional Studies and Reports 100304

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We thank Lidorr Elements and Bayer Animal Health for supporting this study.

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Correspondence to H. Salant.

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Not applicable. The study involved collection of fecal samples from the floor of cages of cats housed in the Jerusalem Municipality cattery with no invasive or painful manipulations to animals. This does not require an animal experimentation permit.

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Figure 2

(Supplementary file): Bayesian inference phylogenetic tree of the ITS-2 fragments of A. abstrusus and T. brevior. Posterior probabilities of each node are shown above each branch. The sequences obtained in the present study (n=4) are with a green circle. (PNG 3.66 mb)

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Salant, H., Yasur-Landau, D., Rojas, A. et al. Troglostrongylus brevior is the dominant lungworm infecting feral cats in Jerusalem. Parasitol Res 119, 3443–3450 (2020). https://doi.org/10.1007/s00436-020-06852-8

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