The significance of the cestode Joyeuxiella pasqualei (Cyclophyllidea: Dipylidiidae) for clinical practice and the welfare of cats
Main Article Content
Abstract
The cestode Joyeuxiella pasqualei is a common parasite of cats in Southern European countries, and due to the increasingly pronounced effects of global warming, there is a tendency for the spread and appearance of this parasite among carnivores in other parts of the European continent. The adult forms of the parasite are localized in the small intestines of definitive hosts (cats, dogs, foxes, wolves, and other carnivores). Cats become infected by ingesting primary hosts (coprophagic insects) and secondary intermediate hosts (reptiles and small mammals), which harbor the infective larval forms of the parasite (cysticercoids). In most infected animals, the disease progresses asymptomatically. An exception occurs in cases of high-intensity infections, where the adhesion of adult parasites to the intestinal mucosa leads to necrosis of the intestinal villi, invagination, and partial obstruction of the intestine, significantly compromising the health and well-being of cats. Successful treatment is achieved through the administration of praziquantel, and for prevention, it is necessary to prevent contact between cats and populations of intermediate hosts. Data on the etiopathogenesis, diagnosis, and control of this tapeworm are of particular importance for inexperienced diagnosticians, who, due to insufficient knowledge about J. pasqualei parasitism, can make significant errors in clinical diagnosis. Due to its significance for clinical practice and the welfare of cats, it is necessary to include this cestode in the differential diagnosis of intestinal invagination in cats and of other carnivore cestodes, which are species from the genera Diplopylidium and Dipylidium.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright of the published papers and grant to the publisher the right to publish the article, to be cited as its original publisher in case of reuse, and to distribute it in all forms and media. Articles will be distributed under the Creative Commons Attribution International License (CC BY 4.0).
References
Alagaili A.N., Mohammed O.B., Omer S.A. 2011. Gastrointestinal parasites and their prevalence in the Arabian red fox (Vulpes vulpes arabica) from the Kingdom of Saudi Arabia. Veterinary Parasitology, 180:336-339. https://doi.org/10.1016/j.vetpar.2011.03.038
Agrawal R.D., Pande B.P. 1979. Cysticercoid of Joyeuxiella pasqualei in the wall-lizard and its experimental development in kitten. Indian Journal of Helminthology, 31: 75-80.
Aleksić J., Stepanović P., Dimitrijević S., Gajić B., Bogunović D., Davidov I., Aleksić‑Agelidis A., Ilić T. 2020. Capillaria plica in red foxes (Vulpes vulpes) from Serbia: epidemiology and diagnostic approaches to urinary capillariosis in domestic carnivores. Acta Parasitologica, 65 (4): 954-962. https://doi.org/10.1007/s11686-020-00244-9
Al-Obaidi Q. 2012. Prevalence of Internal Helminthes in Stray Cats (Felis catus) in Mosul City, Mosul-Iraq. Journal of Animal and Veterinary Advances, 11 (15): 2732-2736. https://doi.org/10.3923/javaa.2012.2732.2736
Al-Rammahi H.M., Safa M.K., Hammadi A.K. 2014. Prevalence of intestinal helmintes in feral cats in Babylon province/Iraq, urban and rural locations. Mirror of Research in Veterinary Sciences and Animals, 3: 44-51. https://doi.org/10.22428/mrvsa. 2307-8073.2014. 00326.x
Al-Rubaie A.R.L., Mhaisen F.T., Al-Tae A.R.A. 2015. Survey of some gastrointestinal cestodes and nematodes from stray cats at Baghdad city, Iraq. American Journal of Biology and Life Sciences, 3: 246-253, 2015.
Arbabi M., Doroudgar A., Hoshyar H., Mobedi I. 2004. A survey of cestode infections of carnivores in the Kashar region. Journal of the Faculty of Veterinary Medicine, Tehran University 59: 289 – 293.
Arbabi M., Hooshyar H. 2009. Gastrointestinal parasites of stray cats in Kashan, Iran. Tropical Biomedicine, 26: 16-22. PMID: 19696723
Aydenizoz M. 1997. Konya Yöresi köpeklerindehelmintolojik arastimalar helminthological investigations of dogs in Konya province [in Turkish]. Acta Parasitologica Turcica, 2: 429-434.
Baker M.K., Lange L., Vester A., van der Plaat S. 1989. A survey of helminths in domestic cats in the Pretoria area of Transvaal. Part 1: The prevalence and comparison of burdens of helminths in adult and juvenile cats. Journal of the South African Veterinary Association, 60: 139-142. PMID: 2634770
Barutzki D., Schaper R. 2003. Endoparasites in dogs and cats in Germany 1999-2002. Parasitology Research, 90: 148-150. https://doi.org/10.1007/s00436-003-0922-6
Beddard F.E. 1913. Contributions to the anatomy and systematic arrangement of the cestoidea. 10. On two species of tapeworms from Genetta dongolana. Proceedings of the Zoological Society of London, 1913: 549-571.
Bezerra-Santos M.A., Mendoza-Roldan J.A., Lia R.P., Annoscia G., Schuster R., Varcasia A., Sgroi G., Modry D., Otranto D. 2022. Description of Joyeuxiella pasqualei (Cestoda: Dipylidiidae) from an Italian domestic dog, with a call for further research on its first intermediate host. Parasitology, 149 (13): 1769-1774. https://doi.org/10.1017/S0031182022001342
Blagburn B.L., Todd K.S. 1986. Exotic cestodiasis (Joyeuxiella pasqualei) in a cat. Feline Practitioners, 16 (2): 8-11.
Borji H., Razmi G., Ahmadi A., Karami H., Yaghfoori S., Abedi V. 2011. A survey on endoparasites and ectoparasites of stray cats from Mashhad (Iran) and association with risk factors. Journal of Parasitology Diseases, 35: 202-206. https://doi.org/10.1007/s12639-011-0057-0
Bowman D.D., Hendrix C.M., Lindsay D.S., Barr S.C. 2002. The cestodes in feline clinical parasitology, Ames, Iowa State University Press, pp. 183-232.
Calvete C., Lucientes J., Castillo J.A., Estrada R., Gracia M.J., Peribáñez M.A., Ferrer M. 1998. Gastrointestinal helminth parasites in stray cats from the mid-Ebro Valley, Spain. Veterinary Parasitology, 75 (2–3): 235-240. https://doi.org/10.1016/s0304-4017(97)00182-9
Changizi E., Mobedi I., Salimi-Bejestani M.R., Rezaei-Doust A. 2007. Gastrointestinal helminthic parasites in stray cats (Felis catus) from north of Iran. Iranian Journal of Parasitology, 2 (4): 25-29.
Dalimi A., Sattari A., Motamedi G. 2006. A study on intestinal helminthes of dogs, foxes and jackels in the western part of Iran. Veterinary Parasitology, 142: 129-133. https://doi.org/10.1016/j.vetpar.2006.06.024
Daoud I.S., Al-Tae A.R.A., Salman Y.J. 1988. Prevalence of gastrointestinal helminthes in cats from Iraq. Journal of Biological Sciences Research, 19: 363-368.
Das S.S., Kumar D., Srikrishnan R. 2011. Joyeuxiella pasqualei in a wild cat in Puducherry. Journal of Veterinary Parasitology, 25: 90-91. Print ISSN: 0971-6157
Deshmukh A.L. 1990. Joyeuxiella domestica sp. N. (Cestoda: Dipylidiidae) from the domestic cat, Felis domesticus (Carnivora) in India. Helminthology, 27: 233-238.
Diakou A., Di Cesare A., Accettura P.M., Barros L., Iorio R., Paoletti B., Frangipane di Regalbono A., Halos L., Beugnet F., Traversa D. 2017. Intestinal parasites and vector-borne pathogens in stray and free-roaming cats living in continental and insular Greece. PLoS Neglected Tropical Diseases, 11 (1): e0005335. https://doi.org/10.1371/journal.pntd.0005335
Diamare V. 1893. Note su cestodi. [Note on cestodes]. Bollettino della Società dei naturalisti in Napoli, 7: 9-13. (In Italian)
Dorchies P., Franc M., Lahite J.D., Berthonneau M.D. 1980. Traitment du teniasis du chien et du chat par le praziquantel. Revista de Medicina Veterinaria, 131: 409-411.
El-Azazi O.M.E., Abdou N.E., Khalil A., Al-Batel M.K., Henedi A..AR, Tahrani LMA. 2016. Cestodes and nematodes recorded in stray cats in Kuwait. Global Veterinaria, 16: 111-118. https://doi.org/10.5829/idosi.gv.2016.16.01.10282
ESCCAP Guideline 01. 2021. Worm control in dogs and cats. Sixth Edition, Worcestershire, United Kingdom, pp. 42.
Farrow C.S. 2003. Small intestinal disease. In Veterinary diagnostic imagining – the dog and cat. St Louis, Mosby, pp. 614-642.
Fuhrmann O. 1935. Rectification de nomenclature [Correction of nomenclature]. Annals of Parasitology, 13: 386. (In French)
Gajić B., Bogunović D., Stevanović J., Kulišić Z., Simeunović P., Stanimirović Z. 2014. Canine and feline thelaziosis caused by Thelazia callipaeda in Serbia. Acta Veterinaria-Beograd, 64: 447-455. https://doi.org/10.2478/acve-2014-0042
Gajić B., Bugarski-Stanojević V., Penezić A., Kuručki M., Bogdanović N., Ćirović D. 2019. First report of eyeworm infection by Thelazia callipaeda in gray wolf (Canis lupus) from Serbia. Parasitology Research, 118 (12): 3549-3553. https://doi.org/10.1007/s00436-019-06519-z
Galán-Puchades M.T., Mas-Coma S., Valero M.A., Fuentes M.V. 2021. First data on the helminth community of the smallest living mammal on earth, the Etruscan Pygmy Shrew, Suncus etruscus (Savi, 1822) (Eulipotyphla: Soricidae).Animals,11 (7): 2074. https://doi.org/10.3390/ani11072074
Gianelli A., Capelli, G., Joachim A., Hinney B., Losson B., Kirova Z., Magalie R.M. Papadopoulus E., Farkas R. 2017. Lungworms and gastrointestinal parasites of domestic cats: a European perspective. International Journal of Parasitology, 47: 517-528. https://doi.org/10.1016/j.ijpara.2017.02.003
Hadži-Milić M., Ilić T., Stepanović P., Đorđević J., Dimitrijević S. 2016. Serbia: Another endemic region for canine ocular thelaziosis. Medycyna Weterynaryjna, 72 (9): 558-563. https://doi.org/ 10.21521/mw.5561
Hosseini S.M., Moshrefi A.H., Esfandiyari A., Youssefi M.R., Nassiri A. 2020. First report of Joyeuxiella spp. infection in Eurasian Lynx and its histopathology study from Iran: a case report. Iranian Journal of Parasitology, 15 (2): 282-286. PMID: 32595721; PMCID: PMC7311823
Ilić T., Becskei Zs., Petrović T., Polaček V., Ristić B., Milić S., Stepanović P., Radisavljević K., Dimitrijević S. 2016. Endoparasitic fauna of red foxes (Vulpes vulpes) and golden jackals (Canis aureus) in Serbia. Acta Parasitologica, 61 (2): 389-396. https://doi.org/ 10.1515/ap-2016-00
Ilić T., Becskei Zs., Tasić A., Stepanović P., Radisavljević K., Đurić B., Dimitrijević S. 2016a. Red foxes (Vulpes vulpes) as reservoirs of respiratory capillariosis in Serbia. Journal of Veterinary Research, 60: 153-157. https://doi.org/ 10.1515/jvetres-2016-0022
Ilić T., Kulišić Z., Antić N., Radisavljević K., Dimitrijević S. 2017. Prevalence of zoonotic intestinal helminths in pet dogs and cats in the Belgrade area. Journal of Applied Animal Research, 45 (1): 204-208. https://doi.org/ 10.1080/09712119.2016.1141779
Ilić T., Mandić M., Stepanović P., Dimitrijević S. 2015. Respiratorna kapilarioza pasa i mačaka – klinički, parazitološki i epidemiološki značaj. Veterinarski glasnik, 69 (5-6): 417-428. https://doi.org/ 10.2298/VETGL1506417I
Ilić T., Nišavić U., Gajić B., Nenadović K., Ristić M., Stanojević D., Dimitrijević S. 2021. Prevalence of intestinal parasites in dogs from public shelters in Serbia. Comparative Immunology, Microbiology and Infectious Diseases, 76: 101653. https://doi.org/ 10.1016/j.cimid.2021.101653
Ilić T., Petrović T., Stepanović P., Bogunović D., Gajić B., Kulišić Z., Ristić M., Hadži Milić M., Dimitrijević S. 2020. Zoonotic helminthosis of domestic and wild carnivores in the epizootiologic territory of Serbia. Archives of Veterinary Medicine, 13 (1): 5-28. https://doi.org/ 10.46784/e-avm.v13i1.238
Ilić T., Rogošić M., Gajić B., Aleksić J. 2021. Urinary capillariosis in dogs. Veterinarski glasnik, 75 (1): 20-32. https://doi.org/ 10.2298/VETGL191009003I
Ilić T., Savić S., Dimitrijević S. 2012. Epizootiološko-epidemiološki značaj parazitskih infekcija divljih kanida. Veterinarski glasnik, 66, 3-4: 299-309. https://doi.org/ 10.2298/VETGL1204299I
Ilić T., Ignjatović N., Jovanović M.N., Davitkov D., Nenadović K. 2023. Epidemiological and clinical importance of canine dioctophymosis. Archives of Veterinary Medicine, 16 (1): 17-36. https://doi.org/ 10.46784/e-avm.v16i1.319
Jones A. 1983. A revision of the cestode genus Joyeuxiella Fuhrmann, 1935 (Dilepididae: Dipylidiinae). Systematic Parasitology, 5: 203-213. https://doi.org/ 10.1007/BF00009352
Jovanović MN, Despotović D, Stepanović P, Rajković M, Ilić T, Clinical-parasitological and epidemiological review of the nematode Acanthocheilonema reconditum. Veterinarski Glasnik, 77 (1): 1-15, 2023. https://doi.org/ 10.2298/VETGL220307008J
Kozlov D.P. 1977. Key to the helminths of carnivorous mammals of the USSR. Nauka, Moscow, p. 274.
Knaus M., Abu-Madi M.A., Ibarra-Velarde F., Kok D.J., Kusi I., Postoli R., Chester S.T., Rosentel J, Alva R., Irwin J., Visser M., Winter R., Rehbein S. 2014. Efficacy of a novel topical fipronil, (S)-methoprene, eprinomectin and praziquantel combination against naturally acquired intestinal nematode and cestode infections in cats. Veterinary Parasitology, 202: 18-25. https://doi.org/10.1016/j.vetpar.2014.02.035
Knaus M., Kusi I., Rapti D., Xhaxhiu D., Winter R., Visser M., Rehbein S. 2011. Endoparasites of cats from the Tirana area and the first report on Aelurostrongylus abstrusus (Railliet, 1898) in Albania. Wiener Klin Wschrift, 123, 1: 31-35. https://doi.org/10.1007/s00508-011-1588-1
Kulišić Z, Pavlović I, Nikolić A, Veljović T, Kokoškov N, Sikimić P (1992). Paraziti digestivnog trakta pasa na području Beograda. Zbornik kratkih sadržaja V Savetovanja veterinara Srbije, Kopaonik, 90.
Lalošević V, Lalošević D, Čapo I, Simin V, Galfi A, Traversa D (2013). High infection rate of zoonotic Eucoleus aerophilus infection in foxes from Serbia. Parasite 20: 1-5.
Lažetić V., Ilić T., Ilić V., Dimitrijević S. 2012. Parazitske bolesti mačaka na beogradskom području sa posebnim osvrtom na zoonoze. Arhiv Veterinarske Medicine, 5 (2): 53-66. UDK 619:636.8(497.1 lBeograd)
Lindquist W.D., Austin E.R. 1981. Exotic parasitism in a Siamese cat. Feline Practitioners, 11: 9-11.
Lopez-Neyra C.R. 1927. Considérations sur le genre Dipylidium Leuckart. Bulletin de la Société de pathologie exotique, 20: 434-440.
Millan J., Casanova J.C. 2007. Helminth parasites of the endangered Iberian lynx (Lynx pardinus) and sympatric carnivores. Journal of Helminthology, 81:377-380. https://doi.org/10.1017/S0022149X07869203
Millan J., Casanova J.C. 2009. High prevalence of helminth parasites in feral cats in Majorca Island (Spain). Parasitology Research, 106:183-188. https://doi.org/10.1007/s00436-009-1647-y
Minnaar W.N., Krecek R.C. 2001. Helminths in dogs belonging to people in a resource-limited urban community in Gauteng, South Africa. Onderstepoort Journal of Veterinary Research, 68: 111-117. PMID: 11585088
Miquel J., Swiderski Z., Marchand B. 2005. Spermatological characters in the Dipylidiidae Stiles, 1896 (Cestoda, Cyclophyllidea). Acta Parasitologica, 50: 65-73. Corpus ID: 59401679
Mohamed S.I., Haroun E.M., Yousif M., Mursal W.I., Abdelsalam E.B. 2021. Prevalence and pathology of some internal parasites in stray cats (Felis catus) in Khartoum North Town, Sudan. American Journal of Research Communication, 9: 13-33.
Nabavi R., Manouchehri Naeini K., Nozhat Zebardast N., Hashemi H. 2014. Epidemiological study of gastrointestinal helminthes of canids in Chaharmahal and Bakhtiari Province of Iran. Iranian Journal of Parasitology, 9: 276-281. PMID: 25848396; PMCID: PMC438605
Öter K., Bilgin Z., Tinar R., Tüzer E. 2011. Tapeworm Infections in stray dogs and cats in Istanbul, Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi, 17: 595-599.
Papazoglou L.G., Diakou A., Patsikas M.N., Anagnostou T., Vagiatis I., Papastefanou A., Kosmas P. 2006. Intestinal pleating associated with Joyeuxiella pasqualei infection in a cat. Veterinary Record, 159 (19): 634. https://doi.org/10.1136/vr.159.19.634
Papazoglou L.G., Patsikas M.N., Rallis T. 2003. Intestinal foreign bodies in dogs and cats. Compendium: continuing education for veterinarians, 25: 830-844.
Pavlović J. Joyeuxiella pasqualei – kliničko parazitološki osvrt i značaj za dobrobit mačaka. Diplomski rad, Fakultet vetrinarske medicine, Univerzitet u Beogradu, str. 1-36, 2023.
Pavlović I, Kulišić Z (1994). Prevalencija askarida kod lisica i pasa na području Beograda. Zbornik kratkih sadržaja VII Savetovanja veterinara Srbije, Zlatibor, 28.
Pavlović I, Kulišić Z, Milutinović M (1997). Rezultati parazitološkog ispitivanja peščanih igrališta za decu u užem centru Beograda. Vet Glasnik 51: 61-65.
Pavlović I., Tasić A (2023). Coccidiosis of pet cats in Belgrade area during 2021. II. International Istanbul current scientific studies, February 8-9, Istanbul, Turkey, 910. ISBN: 978-625-8254-14-3.
Pavlović I., Terzin V. 2012. The influence of the new strategy to resolve the problem of ownerless dogs and cats in Belgrade on the preservation of environmental conditions. Book of Abstracts for the International Scientific Conference on Innovative Strategies and Technologies in Environment Protection, Beograd, 44-46.
Rehbein S., Capári B., Duscher G., Keidane D., Kirkova Z., Petkevičius S., Rapti D., Wagner A., Wagner T., Chester S.T., Rosentel J., Tielemans E., Visser M., Winter R., Kley K., Knaus M. 2014. Efficacy against nematode and cestode infections and safety of a novel topical combination of fipronil, (S)-methoprene, eprinomectin and praziquantel in domestic cats under field conditions in Europe. Veterinary Parasitology, 202: 10-17. https://doi.org/10.1016/j.vetpar.2014.02.032
Ristić M., Dimitrijević S., Višnjić A., Bogunović D., Gajić B., Stojanović M., Ilić T. 2020. Dogs from public city parks as a potential source of pollution of the environment and risk factor for human health. Indian Journal of Animal Sciences. 90 (4): 35-42.
Sanchis Moronis G. Parasitofauna del zorro rojo (Vulpes vulpes) en la comunidad Valenciana [Helminthfauna of the Red fox (Vulpes vulpes) in the Valencia community] [in Spanish]. Thesis Murcia University, 271 pp, 2015.
Santana-Hernández K.M., Rodríguez-Ponce E. 2019. Definitive and paratenic hosts for Joyeuxiella pasqualei in Gran Canaria: a new host record for Spain. Conference: XXI Congreso de la Sociedad Española de Parasitología, e inter Europeo de Parasitología, Poster Presentation, July 03-05, Pontevedra, Spain. https://doi.org/10.13140/RG.2.2.25202.86722
Schuster R., Montag A. 2000. Joyeuxiella pasqualei – an unusual tapeworm in an indigenous domestic cat. Kleintierpraxis, 45 (11): 867-870.
Schuster R.K., Thomas K., Sivakumar S., O’Donovan D. 2009. The parasite fauna of stray domestic cats (Felis catus) in Dubai, United Arab Emirates. Parasitology Research, 105: 125-134. https://doi.org/10.1007/s00436-009-1372-6
Schuster R.K., Mustafa M.B., Baskar J.V., Rosentel J., Chester S.T., Knaus M. 2016. Efficacy of a topical combination of fipronil, (S)-methoprene, eprinomectin and praziquantel (Broadline®) against naturally acquired infections with cestodes of the genus Joyeuxiella in cats. Parasitology Research, 115: 2679-2684. https://doi.org/10.1007/s00436-016-5016-3
Schuster R.K. 2020. Cestodes of the genera Diplopylidium and Joyeuxiella (Eucestoda: Dipylidiiae) – a review of historical data, species inventory and geographical distribution. Scientia Parasitologica, 21 (1-2): 1-17. ISSN 1582-1366
Soulsby E.J.L. 1968. Cestodes. In helminths, arthropods and protozoa of domesticated animals. 6th ed. London, Baillière, Tindall and Cassell, pp. 88-141.
Stepanović P., Despotović D., Dimitrijević S., Ilić T. 2020. Clinical-parasitological screening for respiratory capillariosis in cats in urban environments, Helminthologia, 57 (4): 322-334. https://doi.org/10.2478/helm-2020-0046
Stepanović P., Ilić T., Krstić N., Dimitrijević S. 2015. Efficiency of modified therapeutic protocol in the treatment of some varieties of canine cardiovascular dirofilariasis. Bulletin of Veterinary Institute in Pulawy, 59: 505-509. https://doi.org/10.1515/bvip-2015-0075
Supperer R., Hinaidy H.K. 1986. Contribution to the parasite infestation of dogs and cats in Austria. Deutsche Tierärztliche Wochenschrift, 93: 383-386. PMID: 3536404
Symeonidou I., Gelasakis A.I., Arsenopoulos K., Angelou A., Beugnet F., Papadoupoulos E. 2018. Feline gastrointestinal parasitism in Greece: emergent zoonotic species and associated risk factors. Parasites & Vectors, 11 (1): 227. https://doi.org/10.1186/s13071-018-2812-x
Talbot N. 1970. Parásitos helmintos y artrópodos del gato doméstico en Papua y Nueva Guinea. Australian Veterinary Journal, 46: 370-372. https://doi.org/10.1111/j.1751-0813.1970.tb15575.x
Tielemans E., Manavella C., Chester S.T., Visser M. 2014. Efficacy of a novel topical combination of fipronil, S-methoprene, eprinomectin and praziquantel against induced infections of Echinococcus multilocularis. Veterinary Parasitology, 202: 26-29. https://doi.org/10.1016/j.vetpar.2014.02.034
Waab H., Gomez J., Nunez T. 2014. Parasite communitis in stray cat populations from Lisbon. Portugal. Journal of Helminthology, 88: 389-395. https://doi.org/10.1017/S0022149X1300031X
Witenberg G. 1932. On the cestode subfamily Dipylidiinae Stiles. Zeitschrift Fur Parasitenkunde, 4: 541-584.
Yaman M., Ayaz E., Gül A., Muz M.N. 2006. Hatay ilinde bakisiyapilan kedi köpeklerde helmint enfeksiyonlari [Investigation of helminth infections of cats and dogs in the Hatay province]. Türkiye Parazitoloji Dergisi [Acta Parasitologica Turcica] [in Turkish] 30: 200-204. PMID: 17160852