References

Albanese F, Abramo F, Braglia C Nodular lesions due to infestation by Dirofilaria repens in dogs from Italy. Vet Dermatol. 2013; 24:(2)255-e56 https://doi.org/10.1111/vde.12009

Alsarraf M, Levytska V, Mierzejewska EJ Emerging risk of Dirofilaria spp. infection in Northeastern Europe: high prevalence of Dirofilaria repens in sled dog kennels from the Baltic countries. Sci Rep. 2021; 11:(1) https://doi.org/10.1038/s41598-020-80208-1

Attipa C, Papasouliotis K, Solano-Gallego L Prevalence study and risk factor analysis of selected bacterial, protozoal and viral, including vector-borne, pathogens in cats from Cyprus. Parasit Vectors. 2017; 10:(1) https://doi.org/10.1186/s13071-017-2063-2

Attipa C, Maguire D, Solano-Gallego L Hepatozoon canis in three imported dogs: a new tickborne disease reaching the United Kingdom. Vet Rec. 2018; 183:(23) https://doi.org/10.1136/vr.105087

Baneth G Perspectives on canine and feline hepatozoonosis. Vet Parasitol. 2011; 181:(1)3-11 https://doi.org/10.1016/j.vetpar.2011.04.015

Basso W, Grandt LM, Magnenat AL, Gottstein B, Campos M Strongyloides stercoralis infection in imported and local dogs in Switzerland: from clinics to molecular genetics. Parasitol Res. 2019; 118:(1)255-266 https://doi.org/10.1007/s00436-018-6173-3

Berberich M, Grochow T, Roßner N, Schmäschke R, Rentería-Solís Z Linguatula serrata in an imported dog in Germany: single-case or emerging disease?. Vet Parasitol Reg Stud Reports. 2022; 30 https://doi.org/10.1016/j.vprsr.2022.100717

Bordicchia M, Falcioni D, Scarpona S, Rossi G Nasal carcinoma in a dog with Linguatula serrata infection. Vet Rec Case Rep. 2014; 2:(1) https://doi.org/10.1136/vetreccr-2013-000015

Buczek A, Buczek W Importation of ticks on companion animals and the risk of spread of tick-borne diseases to non-endemic regions in Europe. Animals (Basel). 2020; 11:(1) https://doi.org/10.3390/ani11010006

Diakou A Thelazia callipaeda: vigilance is the best course of action. Vet Rec. 2017; 181:(13)344-345 https://doi.org/10.1136/vr.j4454

Diakou A, Prichard RK Concern for Dirofilaria immitis and macrocyclic lactone loss of efficacy: current situation in the USA and Europe, and future scenarios. Pathogens. 2021; 10:(10) https://doi.org/10.3390/pathogens10101323

Diakou A, Di Cesare A, Tzimoulia S, Tzimoulias I, Traversa D Thelazia callipaeda (Spirurida: Thelaziidae): first report in Greece and a case of canine infection. Parasitol Res. 2015; 114:(7)2771-2775 https://doi.org/10.1007/s00436-015-4457-4

Diakou A, Kapantaidakis E, Tamvakis A, Giannakis V, Strus N Dirofilaria infections in dogs in different areas of Greece. Parasit Vectors. 2016a; 9:(1) https://doi.org/10.1186/s13071-016-1797-6

Diakou A, Psalla D, Migli D First evidence of the European wildcat (Felis silvestris silvestris) as definitive host of Angiostrongylus chabaudi. Parasitol Res. 2016b; 115:(3)1235-1244 https://doi.org/10.1007/s00436-015-4860-x

Diakou A, Di Cesare A, Accettura PM Intestinal parasites and vector-borne pathogens in stray and free-roaming cats living in continental and insular Greece. PLoS Negl Trop Dis. 2017; 11:(1) https://doi.org/10.1371/journal.pntd.0005335

Diakou A, Di Cesare A, Morelli S Endoparasites and vector-borne pathogens in dogs from Greek islands: pathogen distribution and zoonotic implications. PLoS Negl Trop Dis. 2019; 13:(5) https://doi.org/10.1371/journal.pntd.0007003

Diakou A, Sofroniou D, Paoletti B Ticks, fleas, and harboured pathogens from dogs and cats in Cyprus. Pathogens. 2022; 11:(12) https://doi.org/10.3390/pathogens11121403

Dimzas D, Morelli S, Traversa D Intermediate gastropod hosts of major feline cardiopulmonary nematodes in an area of wildcat and domestic cat sympatry in Greece. Parasit Vectors. 2020; 13:(1) https://doi.org/10.1186/s13071-020-04213-z

do Vale B, Lopes AP, da Conceição Fontes M, Silvestre M, Cardoso L, Coelho AC Thelaziosis due to Thelazia callipaeda in Europe in the 21st century - a review. Vet Parasitol. 2019; 275 https://doi.org/10.1016/j.vetpar.2019.108957

European Centre for Disease Prevention and Control and European Food Safety Authority. 2021. https//ecdc.europa.eu/en/disease-vectors/surveillance-and-disease-data/tick-maps

Fuehrer HP, Morelli S, Unterköfler MS Dirofilaria spp. and Angiostrongylus vasorum: current risk of spreading in central and northern Europe. Pathogens. 2021; 10:(10) https://doi.org/10.3390/pathogens10101268

García-Livia K, Reyes R, Amaro-Ramos V Metastrongyloid infection with Aelurostrongylus abstrusus, Troglostrongylus brevior, Oslerus rostratus and Angiostrongylus chabaudi in feral cats from the Canary Islands (Spain). Animals (Basel). 2023; 13:(13) https://doi.org/10.3390/ani13132168

Genchi C, Kramer LH, Rivasi F Dirofilarial infections in Europe. Vector Borne Zoonotic Dis. 2011; 11:(10)1307-1317 https://doi.org/10.1089/vbz.2010.0247

Globokar Vrhovec M, Pantchev N, Norden C Linguatula serrata infestation in four imported dogs. Kleintierpraxis. 2005; 50:(12)779-784

Hajipour N, Tavassoli M Prevalence and associated risk factors of Linguatula serrata infection in definitive and intermediate hosts in Iran and other countries: a systematic review. Vet Parasitol Reg Stud Reports. 2019; 16 https://doi.org/10.1016/j.vprsr.2019.100288

Hansford KM, Pietzsch ME, Cull B, Gillingham EL, Medlock JM Potential risk posed by the importation of ticks into the UK on animals: records from the Tick Surveillance Scheme. Vet Rec. 2018; 182:(4) https://doi.org/10.1136/vr.104263

Hunter A Canine infections and parasites imported to the UK from continental Europe. Vet Rec. 2016; 178:(16) https://doi.org/10.1136/vr.i2116

Ioniță M, Mitrea IL Linguatula serrata (Pentastomida: Linguatulidae) infection in dog, Romania: a case report. AgroLife Sci J. 2016; 5:(2)85-89

Koehsler M, Walochnik J, Georgopoulos M Linguatula serrata tongue worm in human eye, Austria. Emerg Infect Dis. 2011; 17:(5)870-872 https://doi.org/10.3201/eid1705.100790

Koutinas AF, Polizopoulou ZS, Saridomichelakis MN, Argyriadis D, Fytianou A, Plevraki KG Clinical considerations on canine visceral leishmaniasis in Greece: a retrospective study of 158 cases (1989–1996). J Am Anim Hosp Assoc. 1999; 35:(5)376-383 https://doi.org/10.5326/15473317-35-5-376

Leschnik M, Löwenstein M, Edelhofer R, Kirtz G Imported non-endemic, arthropod-borne and parasitic infectious diseases in Austrian dogs. Wien Klin Wochenschr. 2008; 120:(19–20 Suppl 4)59-62 https://doi.org/10.1007/s00508-008-1077-3

Macrelli M, Mackintosh A Tongue worm (Linguatula serrata) infection in a dog imported into the United Kingdom from Romania. Vet Rec Case Rep. 2022; 10:(2) https://doi.org/10.1002/vrc2.281

Maia C, Cardoso L Spread of Leishmania infantum in Europe with dog travelling. Vet Parasitol. 2015; 213:(1–2)2-11 https://doi.org/10.1016/j.vetpar.2015.05.003

Marino V, Gálvez R, Mascuñán C Update on the treatment and prevention of ocular thelaziosis (Thelazia callipaeda) in naturally infected dogs from Spain. Int J Parasitol. 2021; 51:(1)73-81 https://doi.org/10.1016/j.ijpara.2020.08.007

Mettler M, Grimm F, Naucke TJ, Maasjost C, Deplazes P Canine leishmaniosis in central Europe: retrospective survey and serological study of imported and travelling dogs. Berl Munch Tierarztl Wochenschr. 2005; 118:(1–2)37-44

Miró G, Wright I, Michael H Seropositivity of main vector-borne pathogens in dogs across Europe. Parasit Vectors. 2022; 15:(1) https://doi.org/10.1186/s13071-022-05316-5

Mitchell S, Bell S, Wright I Tongue worm (Linguatula species) in stray dogs imported into the UK. Vet Rec. 2016; 179:(10)259-260 https://doi.org/10.1136/vr.i4829

Morchón R, Montoya-Alonso JA, Rodríguez-Escolar I, Carretón E What has happened to heartworm disease in Europe in the last 10 years?. Pathogens. 2022; 11:(9) https://doi.org/10.3390/pathogens11091042

Morelli S, Diakou A, Traversa D First record of Hepatozoon spp. in domestic cats in Greece. Ticks Tick Borne Dis. 2021a; 12:(1) https://doi.org/10.1016/j.ttbdis.2020.101580

Morelli S, Diakou A, Di Cesare A, Colombo M, Traversa D Canine and feline parasitology: analogies, differences, and relevance for human health. Clin Microbiol Rev. 2021b; 34:(4) https://doi.org/10.1128/CMR.00266-20

Morelli S, Diakou A, Colombo M Cat respiratory nematodes: current knowledge, novel data and warranted studies on clinical features, treatment and control. Pathogens. 2021c; 10:(4) https://doi.org/10.3390/pathogens10040454

Montoya JA, Morales M, Ferrer O, Molina JM, Corbera JA The prevalence of Dirofilaria immitis in Gran Canaria, Canary Islands, Spain (1994–1996). Vet Parasitol. 1998; 75:(2–3)221-226 https://doi.org/10.1016/s0304-4017(97)00175-1

Nolan TJ, Lok JB Macrocyclic lactones in the treatment and control of parasitism in small companion animals. Curr Pharm Biotechnol. 2012; 13:(6)1078-1094 https://doi.org/10.2174/138920112800399167

Oliva G, Scalone A, Foglia Manzillo V Incidence and time course of Leishmania infantum infections examined by parasitological, serologic, and nested-PCR techniques in a cohort of naive dogs exposed to three consecutive transmission seasons. J Clin Microbiol. 2006; 44:(4)1318-1322 https://doi.org/10.1128/JCM.44.4.1318-1322.2006

Otranto D, Traversa D Thelazia eyeworm: an original endo- and ecto-parasitic nematode. Trends Parasitol. 2005; 21:(1)1-4 https://doi.org/10.1016/j.pt.2004.10.008

Otranto D, Lia RP, Buono V, Traversa D, Giangaspero A Biology of Thelazia callipaeda (Spirurida, Thelaziidae) eyeworms in naturally infected definitive hosts. Parasitology. 2004; 129:(Pt 5)627-633 https://doi.org/10.1017/s0031182004006018

Otranto D, Cantacessi C, Testini G, Lia RP Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: evidence for pathogen transmission by a male arthropod vector. Int J Parasitol. 2006; 36:(10–11)1167-1173 https://doi.org/10.1016/j.ijpara.2006.06.006

Paltrinieri S, Solano-Gallego L, Fondati A Guidelines for diagnosis and clinical classification of leishmaniasis in dogs. J Am Vet Med Assoc. 2010; 236:(11)1184-1191 https://doi.org/10.2460/javma.236.11.1184

Pantchev N, Etzold M, Daugschies A, Dyachenko V Diagnosis of imported canine filarial infections in Germany 2008 – 2010. Parasitol Res. 2011; (109 Suppl 1)S61-S76 https://doi.org/10.1007/s00436-011-2403-7

Pimenta P, Cardoso L, Pereira MJ Canine ocular thelaziosis caused by Thelazia callipaeda in Portugal. Vet Ophthalmol. 2013; 16:(4)312-315 https://doi.org/10.1111/j.1463-5224.2012.01074.x

Sarmadian H, Nasiri Z, Saeedinia S Clinical manifestation and epidemiological findings of human linguatula serrate infection in Iran: systematic review. J Parasit Dis. 2021; 45:(1)50-58 https://doi.org/10.1007/s12639-020-01276-8

Schäfer I, Volkmann M, Beelitz P, Merle R, Müller E, Kohn B Retrospective evaluation of vector-borne infections in dogs imported from the Mediterranean region and southeastern Europe (2007–2015). Parasit Vectors. 2019a; 12:(1) https://doi.org/10.1186/s13071-018-3284-8

Schäfer I, Volkmann M, Beelitz P, Merle R, Müller E, Kohn B Retrospective analysis of vector-borne infections in dogs after travelling to endemic areas (2007–2018). Vet Parasitol. 2019b; 276S https://doi.org/10.1016/j.vpoa.2019.100015

Schäfer I, Müller E, Nijhof AM First evidence of vertical Hepatozoon canis transmission in dogs in Europe. Parasit Vectors. 2022a; 15:(1) https://doi.org/10.1186/s13071-022-05392-7

Schäfer I, Kohn B, Nijhof AM, Müller E Molecular detection of Hepatozoon species infections in domestic cats living in Germany. J Feline Med Surg. 2022b; 24:(10)994-1000 https://doi.org/10.1177/1098612X211055680

Schnyder M, Reichler IM, Eichenberger RM, Hofer-Inteeworn N, Kümmerle-Fraune C, Grimm F Strongyloides stercoralis in Swiss dogs - a retrospective study suggests an increasing occurrence of this potentially zoonotic parasite as a consequence of dog imports. Schweiz Arch Tierheilkd. 2022; 164:(1)89-104 https://doi.org/10.17236/sat00340

Sievänen M, Pohjoismäki J, Saari S, Miro G, Näreaho A The first Linguatula serrata case in an imported dog in Finland. Vet Parasitol Reg Stud Reports. 2021; 26 https://doi.org/10.1016/j.vprsr.2021.100654

Simón F, Siles-Lucas M, Morchón R Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev. 2012; 25:(3)507-544 https://doi.org/10.1128/CMR.00012-12

Simón F, Diosdado A, Siles-Lucas M, Kartashev V, González-Miguel J Human dirofilariosis in the 21st century: a scoping review of clinical cases reported in the literature. Transbound Emerg Dis. 2022; 69:(5)2424-2439 https://doi.org/10.1111/tbed.14210

Solano-Gallego L, Miró G, Koutinas A LeishVet guidelines for the practical management of canine leishmaniosis. Parasit Vectors. 2011; 4 https://doi.org/10.1186/1756-3305-4-86

Springer A, Fiedler H, Raue K, Strube C Linguatula serrata-infection in a dog imported from Romania to Germany. Tierarztl Prax Ausg K Kleintiere Heimtiere. 2018; 46:(4)260-264 https://doi.org/10.15654/TPK-170651

Szymański S Case of mass infestation with mites of genus Rhipicephalus sanguineus (Latreile, 1806) in a Warsaw apartment. Wiad Parazytol. 1979; 25:(4)453-459

Tabaripour R, Shokri A, Hosseini Teshnizi S, Fakhar M, Keighobadi M Status of Linguatula serrata infection in livestock: a systematic review with meta-analysis in Iran. Parasite Epidemiol Control. 2019; 7 https://doi.org/10.1016/j.parepi.2019.e00111

Thomas M Linguatula serrata in an imported Romanian street dog. Vet Rec. 2018; 182:(4)112-113 https://doi.org/10.1136/vr.k356

Traversa D, Morelli S, Di Cesare A, Diakou A Felid cardiopulmonary nematodes: dilemmas solved and new questions posed. Pathogens. 2021; 10:(1) https://doi.org/10.3390/pathogens10010030

Trees AJ, Ridge A Threat of imported diseases to UK dogs. Vet Rec. 2016; 178:(14)347-348 https://doi.org/10.1136/vr.i1799

Villedieu E, Sanchez RF, Jepson RE, Ter Haar G Nasal infestation by Linguatula serrata in a dog in the UK: a case report. J Small Anim Pract. 2017; 58:(3)183-186 https://doi.org/10.1111/jsap.12611

Wright I, Jongejan F, Marcondes M Parasites and vector-borne diseases disseminated by rehomed dogs. Parasit Vectors. 2020; 13:(1) https://doi.org/10.1186/s13071-020-04407-5

Pet travellers' unwanted companions: a parasitic voyage across Europe

02 June 2024
17 mins read
Volume 29 · Issue 6
Figure 5. Thelazia callipaeda (arrow) under the eye lid of an infected dog.
Figure 5. Thelazia callipaeda (arrow) under the eye lid of an infected dog.

Abstract

In the modern world, country borders do not represent boundaries for the transmission of pathogens. This is also true for parasites that may travel with animals, particularly pets. Dogs and cats are moving across countries more than ever before as a result of adoption, commerce and travels with owners. In addition, climate change supports the establishment of parasites, particularly those transmitted by invertebrate intermediate hosts and vectors, into areas which were previously considered non-enzootic. Therefore, it is important for veterinarians to keep a vigilant eye on such parasitic infections in dogs and cats, be able to recognise compatible signs and feel confident in ordering specific diagnostic tests. This article presents parasites prevalently reported as imported from one European country to another. Furthermore, common clinical manifestations and diagnostic tests are summarised and the preventive measures that should be advised to pet owners are discussed. Raising awareness among veterinary practitioners and pet owners about the risk of parasites spreading in new areas is imperative for controlling and delaying globalisation of important, and potentially lethal, parasitic diseases.

In the ever-evolving global landscape, boundaries of various kinds are shifting or even dissolving altogether. This transformation finds its roots in a nexus of environmental, climatic, socioeconomic, geopolitical and behavioural changes. A striking illustration of this occurrence lies in the propagation and exchange of pathogens across diverse regions, ecosystems and countries. This phenomenon finds application in the importation of pet animal parasites, some of zoonotic importance, from enzootic areas to areas free of these infections among European countries. Parasites considered ‘exotic’ enter non-enzootic European countries via pet animals that serve as a Trojan horse, occasionally find suitable conditions to thrive locally and eventually become enzootic (Trees and Ridge, 2016).

Indeed, the number of travelling dogs and cats is steadily increasing. Pets travel with owners for holidays and tourism, when adopted and rehomed in a different country and in the form of trade from breeding facilities located in a different country than that of purchase. Pet movements have been facilitated because of discontinuation of quarantine restrictions and regulations that were previously in force – primarily for rabies control – in many European countries including Norway, Sweden, Finland, Ireland, the UK, Cyprus and Malta (Hunter, 2016). Over the years, quarantine was replaced in many European countries by the ‘Pet Travel Scheme’, which allows dogs and other pets to move between European Union countries and certain non-European Union countries with specific health checks, microchipping, vaccinations and documentation. However, the documentation that is needed in most countries (eg administration of praziquantel for Echinococcus spp. control or negative serological examination for Leishmania spp.) clearly does not cover all possible parasitic infections and leave room for the import of new parasites (Diakou, 2017).

Register now to continue reading

Thank you for visiting UK-VET Companion Animal and reading some of our peer-reviewed content for veterinary professionals. To continue reading this article, please register today.