pathogens Review Felid Cardiopulmonary Nematodes: Dilemmas Solved and New Questions Posed Donato Traversa 1,*, Simone Morelli 1 , Angela Di Cesare 1 and Anastasia Diakou 2 1 Faculty of Veterinary Medicine, University of Teramo, 64100 Teramo, Italy; [email protected] (S.M.); [email protected] (A.D.C.) 2 School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece; [email protected] * Correspondence: [email protected] Abstract: In the past decade cardiopulmonary nematodes affecting felids have become a core research topic in small animal parasitology. In the late 2000s, an increase in studies was followed by unex- pected findings in the early 2010s, which have stimulated research teams to start investigating these intriguing parasites. Prolific scientific debate and exchanges have then fostered field and laboratory studies and epizootiological surveys. New data have improved basic and applied knowledge, solved dilemmas and posed new questions. This article discusses the past and present background to felid cardiopulmonary nematodes after the last few years of intense scientific research. New data which have demonstrated the key role of Aelurostrongylus abstrusus and Troglostrongylus brevior in causing respiratory infections in domestic cats, and on the nil to negligible current importance of other species, i.e., Troglostrongylus subcrenatus, Oslerus rostratus and Angiostrongylus chabaudi, are presented. Biological information and hypothesized alternative routes of infection are analysed and discussed. Novel identification and taxonomical data and issues are reported and commented upon. On the whole, recent biological, ecological and epizootiological information on felid metastrongyloids is critically analysed, with the aim to answer outstanding questions, stimulate future studies, and underline new research perspectives. Citation: Traversa, D.; Morelli, S.; Di Cesare, A.; Diakou, A. Felid Keywords: cardiopulmonary nematodes; domestic cats; wildcats Cardiopulmonary Nematodes: Dilemmas Solved and New Questions Posed. Pathogens 2021, 10, 30. https://doi.org/10.3390/ 1. A Pandora’s Box Containing Parasitic Nematodes pathogens10010030 In 2010 the record of a practically unknown respiratory nematode in two domestic Received: 14 December 2020 cats (Felis catus) from Ibiza [1] opened a Pandora’s box. Two years later, this parasite was Accepted: 30 December 2020 identified in a further case in Sicily as the crenosomatid Troglostrongylus brevior and its Published: 2 January 2021 role in causing verminous bronchopneumonia in domestic cats was acknowledged [2]. Until then, nematodes of the genus Troglostrongylus were considered affiliated to wild Publisher’s Note: MDPI stays neu- felids, with a limited geographic distribution and no importance in cat parasitology, whilst tral with regard to jurisdictional clai- the angio-strongylid Aelurostrongylus abstrusus (the “cat lungworm”) was known as the ms in published maps and institutio- prevailing respiratory nematode of F. catus [3,4]. After these first findings, T. brevior has nal affiliations. been recorded in cats from more European regions, especially southern mountainous areas and islands [5–8]. These new descriptions have changed the scenario regarding metastrongyloids affecting felids, revealing dilemmas and mistakes, fostering scientific debates and posing outstanding questions [3,9–11]. Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. Various speculations, investigations and hypotheses were presented aiming at un- This article is an open access article derstanding the origin of the unexpected records of T. brevior in domestic cats in the early distributed under the terms and con- 2010s. Evidence has indicated that under certain conditions T. brevior infects F. catus due to ditions of the Creative Commons At- a spillover (Figure1) from its natural host, i.e., the European wildcat ( Felis silvestris). Over- tribution (CC BY) license (https:// lapping morphological/morphometric and biological features of A. abstrusus and T. brevior, creativecommons.org/licenses/by/ along with the sporadic occurrence of the latter, have been considered sources of frequent 4.0/). confusion in past identifications of lungworms [2,4,9]. According to this speculation, the Pathogens 2021, 10, 30. https://doi.org/10.3390/pathogens10010030 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, x FOR PEER REVIEW 2 of 18 Pathogens 2021, 10, 30 2 of 17 frequent confusion in past identifications of lungworms [2,4,9]. According to this specu‐ lation, the emergence of feline troglostrongylosis was not “true”, but rather the result of anemergence increased of awareness, feline troglostrongylosis after the “re was‐appearance” not “true”, in but 2010 rather of this the resultneglected of an nematode increased [1,4,9].awareness, Nevertheless, after the “reappearance” bibliographic analyses in 2010 and of this more neglected recent data nematode have demonstrated [1,4,9]. Neverthe- that misdiagnosisless, bibliographic can be analyses only marginally and more recent included data in have an demonstratedaccount of the that emergence misdiagnosis of feline can troglostrongylosis,be only marginally which included rather in an relies account on a spillover of the emergence from wildcats of feline to domestic troglostrongylosis, cats. Mis‐ whichdiagnosis rather in the relies past on was a spillover evidently from the wildcatscase only to in domestic sporadic cats.detections. Misdiagnosis Soon after in the firstpast records, was evidently the pathogenic the case onlypotential in sporadic of T. brevior detections. has been Soon questioned after the first[9]. To records, date, it the is ascertainedpathogenic potentialthat clinical of T.troglostrongylosis brevior has been is questioned often severe [9]. and To date,fatal, itespecially is ascertained in kittens that andclinical young troglostrongylosis cats. If T. brevior is oftenwas frequently severe and confused fatal, especially with A. in abstrusus kittens and, severe young and cats. fatal If T.aelurostrongylosis brevior was frequently would confused have often with beenA. abstrususreported,, severebut this and has fatal been aelurostrongylosis extremely infre‐ quentwould until have now often [5]. been At reported,present, the but frequent this has beenlife‐threatening extremely infrequentcases of troglostrongylosis, until now [5]. At withpresent, evidence the frequent of vertical life-threatening transmission, cases which of troglostrongylosis,has never been a concern with evidence for aelurostron of verti-‐ gylosis,cal transmission, leave no whichroom for has lingering never been doubts a concern [6,12–14]. for aelurostrongylosis, Moreover, a large leave retrospective no room studyfor lingering demonstrated doubts that [6,12 from–14]. 2002 Moreover, to 2013 a T. large brevior retrospective was diagnosed study with demonstrated extremely thatlow frequencyfrom 2002 toin 2013cats livingT. brevior in areaswas diagnosedenzootic for with meta extremely‐strongyloids low frequency [15]. To date, in cats areas living enzo in‐ oticareas for enzootic T. brevior for reflect metastrongyloids the distribution [15 area]. To of date, F. silvestris areas enzootic and neighboring for T. brevior zonesreflect (Figure the 2)distribution [14,16,17], areaand ofregionsF. silvestris from andwhere neighboring the samples zones in the (Figure retrospective2)[ 14,16 study,17], and mentioned regions abovefrom where [15] were the samplescollected in are the encompassed retrospective in study the distribution mentioned area above of the [15 ]European were collected wild‐ cat.are encompassedIn those areas ina true the distributionincrease of troglostrongylosis area of the European is glaring, wildcat. as Inthe those infection areas may a true be responsibleincrease of troglostrongylosisfor 42% of metastrongyloid is glaring, infections as the infection in domestic may cats be responsible [17]. Other forbiological, 42% of clinicalmetastrongyloid and pathological infections evidence in domestic [3,5,8,12] cats [17 indicates]. Other biological,that misdiagnosis clinical and and pathological increase in awarenessevidence [3 have,5,8,12 had] indicates only a thatlimited misdiagnosis role in the and current increase epi in‐zootiological awareness have scenario had onlyof cat a troglostrongylosis,limited role in the current and that epizootiological T. brevior has been scenario overlooked of cat troglostrongylosis, by parasitologists. and In that anyT. case, bre- vior A. abstrusus A. abstrusushas been remains overlooked a genuinely by parasitologists. cat‐affiliated In lungworm any case, and the onlyremains species a that genuinely can be cat-affiliated lungworm and the only species that can be named “cat lungworm”. named “cat lungworm”. Figure 1. Schematic representationrepresentation of of the theTroglostrongylus Troglostrongylus brevior breviorspillover spill‐over from from the the European European wildcat wildcat (Felis (Felis silvestris silvestris) to) the to domesticthe domestic cat (catFelis (Felis catus catus). ). PathogensPathogens2021, 10 2021, 30, 10, x FOR PEER REVIEW 3 of 18 3 of 17 FigureFigure 2. Geographic 2. Geographic distribution distribution of ofTroglostrongylus Troglostrongylus brevior brevior inin Europe and and Middle Middle East. East. The The geographic geographic distribution distribution of of Troglostrongylus brevior in domestic cats (red triangles) [6,7,16–21] reflects the distribution area of wildcats