pathogens Article The Vector-Borne Zoonotic Nematode Thelazia callipaeda in the Eastern Part of Europe, with a Clinical Case Report in a Dog in Poland Leszek Rolbiecki 1,* , Joanna N. Izdebska 1 , Marta Franke 2, Lech Iliszko 3 and Sławomira Fryderyk 1 1 Department of Invertebrate Zoology and Parasitology, Faculty of Biology, University of Gda´nsk, Wita Stwosza 59, 80-308 Gda´nsk,Poland; [email protected] (J.N.I.); [email protected] (S.F.) 2 Veterinary Office, Lutowiska 68, 38-713 Lutowiska, Poland; [email protected] 3 Department of Vertebrate Ecology and Zoology, Faculty of Biology, University of Gda´nsk,Wita Stwosza 59, 80-308 Gda´nsk,Poland; [email protected] * Correspondence: [email protected]; Tel.: +48-58-5236190 Abstract: Thelazia callipaeda is a zoonotic nematode transmitted by drosophilid flies. It causes ocular thelaziosis, a disease of carnivores, such as dogs, cats, and foxes, and also humans. The parasite has thus far been observed in various areas of Eurasia, including 20 countries within Europe. The present study documents its presence in the south-east region of Poland, near the Ukraine border. An adult nematode was removed from the conjunctival sac of a dog showing ocular inflammation and purulent discharge. The dog’s precise origin is unknown. Based on its localization and morphometrical features, the nematode was identified as a Thelazia callipaeda adult male. The present study is the first report of T. callipaeda in a dog in Poland. Keywords: Thelazia callipaeda; eyeworm; zoonotic nematode; thelaziosis; dog; Poland; Eastern Europe Citation: Rolbiecki, L.; Izdebska, J.N.; Franke, M.; Iliszko, L.; Fryderyk, S. 1. Introduction The Vector-Borne Zoonotic Nematode Thelazia callipaeda Railliet et Henry, 1910 (Spirurida, Thelaziidae) is a parasitic nema- Thelazia callipaeda in the Eastern Part tode of the eye known to cause thelaziosis, a parasite infection of carnivores, lagomorphs of Europe, with a Clinical Case Report and humans [1,2]. The infection can manifest with conjunctivitis, epiphora, visual dis- in a Dog in Poland. Pathogens 2021, turbances and even keratitis, and corneal ulceration (e.g., [3,4]). The parasite was first 10, 55. https://doi.org/10.3390/ discovered over one hundred years ago in Punjab, India [5], and has been thus far ob- pathogens10010055 served in other areas of Asia, such as China, Myanmar, India, Indonesia, Thailand, Taiwan, Received: 21 November 2020 South of Korea, Japan, Bangladesh, Nepal, Vietnam, and the former USSR [3,6–14], and Accepted: 7 January 2021 in 20 countries in Europe [15,16]. Despite its wide area of distribution and significant Published: 9 January 2021 pathogenic (including zoonotic) importance, the parasite has been identified only relatively rarely and in few localities; however, its distribution is potentially far greater, particularly Publisher’s Note: MDPI stays neu- since data obtained from veterinary practices are not always included in academic studies. tral with regard to jurisdictional clai- Previous records from Western, Central and Southern Europe suggest that the nema- ms in published maps and institutio- tode may also occur in neighboring countries, such as Poland and Ukraine. The present nal affiliations. study is the first report of T. callipaeda in a dog in Poland. 2. Results 2.1. Case Report Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. A stray dog was observed in Poland, in the border area with Ukraine (approx. 5 km This article is an open access article from the border), from July 2019 (Figure1). The dog’s precise origin is unknown. The de- distributed under the terms and con- tailed fate of the dog in the period from the first to the second observation is also unknown. ditions of the Creative Commons At- In November 2019, after adoption, the dog was subjected to a veterinary examination tribution (CC BY) license (https:// and the necessary treatments—castration, deworming, vaccinations, and treatment of skin creativecommons.org/licenses/by/ mycosis. During the first veterinary examination, an inflammation, erythema and excessive 4.0/). purulence of both eyes, particularly in one eye, were also diagnosed. The dog was in Pathogens 2021, 10, 55. https://doi.org/10.3390/pathogens10010055 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 55 2 of 8 detailed fate of the dog in the period from the first to the second observation is also un- Pathogens 2021, 10, 55 known. In November 2019, after adoption, the dog was subjected to a veterinary exami-2 of 7 nation and the necessary treatments—castration, deworming, vaccinations, and treatment of skin mycosis. During the first veterinary examination, an inflammation, erythema and generalexcessive poor purulence condition, of thus,both eyes, the ocular particularly symptoms in one were eye, not were then also linked diagnosed. to the presence The dog ofwas parasites. in general He waspoor initially condition, treated thus, with the eye ocular drops symptoms containing we antibioticre not then tobramycin linked to and the corticosteroidpresence of parasites. dexamethasone He was (Tobradexinitially treated®, S.A. with ALCON-COUVREUR eye drops containing N.V., antibiotic Belgium) tobra- for ® threemycin weeks, and corticosteroid but with no effect. dexamethasone At the subsequent (Tobradex examination,, S.A. ALCON-COUVREUR a nematode was found N.V., inBelgium) one of the for eyes. three No weeks, worms but were with foundno effect in. theAt the other subsequent eye. Symptoms examination, and eye a nematode irritation resolvedwas found several in one days of afterthe eyes. removal No worms of the nematodewere found and in thethe administrationother eye. Symptoms of an antipara- and eye siticirritation drug composed resolved several of imidacloprid days after and removal moxidectin of the (Advocate nematode® ,and KVP the Pharma administration + Veterinär of ® Produktean antiparasitic GmbH, drug Kiel, composed Germany). of imidacloprid and moxidectin (Advocate , KVP Pharma + Veterinär Produkte GmbH, Kiel, Germany). Figure 1. Geographical distribution of Thelazia callipaeda in Europe and locality (Krywe) of the pre- Figure 1. Geographical distribution of Thelazia callipaeda in Europe and locality (Krywe) of the present sent report in a dog in Poland. report in a dog in Poland. 2.2.2.2. Description Description of of the the Nematode Nematode TheThe isolated isolated nematodenematode (Figure (Figure 2)2) had had a abody body length length of of9.5 9.5mm mm and anda maximum a maximum width widthof 450 of μ 450m, whileµm, whilethe width the widthat the level at the of level the oesophagus-intestina of the oesophagus-intestinall junction junction was 265was μm. 265Theµ m.caudal The end caudal was end ventrally was ventrally curved with curved pre-cloacal with pre-cloacal and post-cloacal and post-cloacal papillae. The papillae. nem- Theatode nematode had a clearly had aserrated clearly cuticle, serrated except cuticle, for except the buccal for thecapsule. buccal The capsule. buccal capsule The buccal was capsulehexagonal, was 25 hexagonal, μm long and 25 µ 30m μ longm wide. and The 30 µ oesophagusm wide. The was oesophagus 580 μm in length, was 580 whileµm inits length,width whilewas 92.5 its μ widthm at the was posterior 92.5 µm end at theand posterior 60 μm at endthe anterior and 60 µend.m at The the tail anterior was 90 end. μm The tail was 90 µm long and showed two spicules; the left spicule was 1.88 mm long and the right spicule was 170 mm long. Based on its localization and morpho-anatomical and metrical features, the nematode was identified as a T. callipaeda adult male (Figure2). Pathogens 2021, 10, 55 3 of 8 Pathogens 2021, 10, 55 long and showed two spicules; the left spicule was 1.88 mm long and the right spicule3 was of 7 170 mm long. Based on its localization and morpho-anatomical and metrical features, the nematode was identified as a T. callipaeda adult male (Figure 2). Figure 2.2. ThelaziaThelazia callipaedacallipaeda,(, A(A)) total total view, view, (B ()B anterior) anterior end, end, (C )(C junction) junction between between oesophagus oesophagus and and intestine, intestine, (D) cephalic(D) cephalic end, (end,E) posterior (E) posterior end, ( Fend,) tail, (F ()G tail,) tail (G and) tail papillae; and papillae; a: annellations, a: annellations, bc: buccal bc: capsule,buccal capsule, i: intestine, i: intestine, j: junction, j: junction, oe: oesophagus, oe: oesoph- pc: agus, pc: pre-cloacal papillae, ps: post-cloacal papillae, sl: left spicule, sr: right spicule. pre-cloacal papillae, ps: post-cloacal papillae, sl: left spicule, sr: right spicule. 3. Discussion 3. DiscussionIn recent years, an increased number of T. callipaeda infection clinical cases have been observedIn recent throughout years, anEurope increased (Figure number 1) [4,15]. of CarnivoresT. callipaeda areinfection considered clinical the main cases defin- have beenitive hosts observed of T. throughout callipaeda, including Europe (Figure domestic1)[ 4carnivores,,15]. Carnivores such areas domestic considered dogs the or main do- mesticdefinitive cats hosts [17–20], of T. or callipaeda wild carnivores,, including such domestic as the red carnivores, fox Vulpes such vulpes as domestic(Linnaeus, dogs 1758), or thedomestic European cats [17badger–20], orMeles wild meles carnivores, (Linnaeus, such as1758), the redthe foxbeechVulpes marten vulpes Martes(Linnaeus, foina 1758),(Erx- leben,the European 1777), th badgere EurasianMeles lynx meles Lynx(Linnaeus, lynx (Linnaeus, 1758), the 1758), beech the marten goldenMartes jackals foina Canis(Erxleben, aureus 1777),Linnaeus, the Eurasian1758, the lynx grayLynx wolf lynx Canis(Linnaeus, lupus Linnaeus, 1758), the 1758, golden the jackals racoonCanis dog aureusNyctereutesLinnaeus, pro- 1758,cyonoides the (Gray, gray wolf 1834),Canis thelupus sableLinnaeus, Martes zibellina 1758, the(Linnaeus, racoon dog1758),Nyctereutes the wild cats procyonoides Felis sil- (Gray,vestris 1834),Schreber, the sable1777, Martesand the zibellina Asiatic(Linnaeus, black bear 1758), Ursus the thibetanus wild cats G.[Baron]Felis silvestris Cuvier,Schreber, 1823 1777,[21–26].