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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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
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
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
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
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
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
Conboy G (2009) Helminth parasites of the canine and feline respiratory tract. Vet Clin North Am Small Anim Pract 39:1109–1126
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
Deak G, Ionică AM, Mihalca AD, Gherman CM (2017) Troglostrongylus brevior: a new parasite for Romania. Parasites and Vectors 10:599
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
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
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
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
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
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
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
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
Gerichter CB (1949) Studies on the nematodes parasitic in the lungs of felidae in Palestine. Parasitology 39:251–262
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
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
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
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
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
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
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
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
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
Ribeiro VM, Lima WS (2001) Larval production of cats infected and re-infected with Aelurostrongylus abstrusus (Nematoda: Protostrongylidae). Rev Med Vet 152:815–829
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
Roll U, Dayan T, Simberloff D, Mienis HK (2009) Non-indigenous land and freshwater gastropods in Israel. Biol Invasions 11:1963–1972
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
Scott DW (1973) Current knowledge of aelurostrongylosis in the cat. Literature review and case reports. Cornell Vet 63:483–500
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
Traversa D, di Cesare A (2013) Feline lungworms: what a dilemma. Trends Parasitol 29:423–430
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
Traversa D, Guglielmini C (2008) Feline aelurostrongylosis and canine angiostrongylosis: a challenging diagnosis for two emerging verminous pneumonia infections. Vet Parasitol 157:163–174
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
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
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
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
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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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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DOI: https://doi.org/10.1007/s00436-020-06852-8