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Description of Joyeuxiella pasqualei (Cestoda: Dipylidiidae) from an Italian domestic dog, with a call for further research on its first intermediate host

Published online by Cambridge University Press:  27 September 2022

Marcos Antonio Bezerra-Santos
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
Jairo Alfonso Mendoza-Roldan
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
Riccardo Paolo Lia
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
Giada Annoscia
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
Rolf Schuster
Affiliation:
Department of Parasitology, Central Veterinary Research Laboratory, Dubai
Antonio Varcasia
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
Giovanni Sgroi
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
David Modry
Affiliation:
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budějovice, Czech Republic Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences, Prague, Czech Republic
Domenico Otranto*
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy Department of Pathobiology, Faculty of Veterinary Science, Bu-Ali Sina University, Hamedan, Iran
*
Author for correspondence: Domenico Otranto, E-mail: [email protected]

Abstract

Although Joyeuxiella pasqualei is frequently detected in cats from Mediterranean Europe, information on its biology is still scarce. This cestode is relatively less frequently reported in dogs, possibly because it is often misdiagnosed with the better-known Dipylidium caninum. The occurrence of J. pasqualei proglottids in a dog living in a closed environment triggered us to delve into the biology of this cestode by collecting biological samples from lizards and a road-killed cat. Two reptile species, Podarcis siculus (Lacertidae), and Tarentola mauritanica (Geckonidae) were also collected in the garden and its surroundings. In addition, experimental infections with eggs obtained from gravid proglottids were performed in laboratory mice, and Tenebrio molitor (Coleoptera: Tenebrionidae) beetles. Proglottids from the dog's feces and adult cestodes detected at necroscopy of a cat were morphologically identified as J. pasqualei. Two out of 13 T. mauritanica collected in the garden had natural infections of J. pasqualei cysts in the liver and attached to the intestine. All P. siculus lizards and experimentally infected rodents and beetles were negative. DNA sequences obtained from J. pasqualei showed the highest nucleotide similarities with Versteria sp., Echinococcus sp., Raillietina sonini, Taenia polyacantha and D. caninum. Data herein provided show the inability of rodents to become infected by direct ingestion of gravid proglottids, suggesting a need for an invertebrate first intermediate host in the life cycle. Thus, more research study is advocated to better understand the biology of J. pasqualei such as its first intermediate host and its mechanism of transmission in reptiles and rodents.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Alagaili, AN, Mohammed, OB and Omer, SA (2011) Gastrointestinal parasites and their prevalence in the Arabian red fox (Vulpes vulpes arabica) from the Kingdom of Saudi Arabia. Veterinary Parasitology 180, 336339.CrossRefGoogle ScholarPubMed
Baer, JG (1924) Contribution a la faune helminthologique Sud-Africaine. Annales de Parasitologie 2, 239247 (in French).Google Scholar
Barutzki, D and Schaper, R (2003) Endoparasites in dogs and cats in Germany 1999–2002. Parasitology Research 90, S148S150.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle ScholarPubMed
Bowman, DD, Hendrix, CM, Lindsay, DS and Barr, SC (2002) Feline Clinical Parasitology. USA: Iowa State University. A Blackwell Science Company, USA, pp. 375400.CrossRefGoogle Scholar
Calvete, C, Lucientes, J, Castillo, JA, Estrada, R, Gracia, MJ, Peribáñez, MA and Ferrer, M (1998) Gastrointestinal helminth parasites in stray cats from the mid-Ebro Valley, Spain. Veterinary Parasitology 75, 235240.CrossRefGoogle ScholarPubMed
Dalimi, A, Sattari, A and Motamedi, G (2006) A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Veterinary Parasitology 142, 129133.CrossRefGoogle Scholar
El-Azazy, OM, Abdou, NMI, Khalil, AI, AL-Batel, MK, Henedi, AR and Tahrani, MA (2016) Cestodes and nematodes recorded in stray cats in Kuwait. Global Veterinaria 16, 111118.Google Scholar
Galán-Puchades, MT, Mas-Coma, S, Valero, MA and Fuentes, MV (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, 2074.CrossRefGoogle Scholar
Haralabidis, ST, Papazachariadou, MG, Koutinas, AF and Rallis, TS (1988) A survey on the prevalence of gastrointestinal parasites of dogs in the area of Thessaloniki, Greece. Journal of Helminthology 62, 4549.CrossRefGoogle ScholarPubMed
Hasegawa, M, Kishino, H and Yano, T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160174.CrossRefGoogle Scholar
Jones, A (1983) A revision of the cestode genus Joyeuxiella Fuhrmann, 1935 (Dilepididae: Dipylidiinae). Systematic Parasitology 5, 203213.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Millán, J and Casanova, JC (2007) Helminth parasites of the endangered Iberian lynx (Lynx pardinus) and sympatric carnivores. Journal of Helminthology 81, 377380.CrossRefGoogle ScholarPubMed
Millán, J and Casanova, JC (2009) High prevalence of helminth parasites in feral cats in Majorca Island (Spain). Parasitology Research 106, 183188.CrossRefGoogle Scholar
Minnaar, WN, Krecek, RC and Fourie, LJ (2002) Helminths in dogs from a peri-urban resource-limited community in Free State Province, South Africa. Veterinary Parasitology 107, 343349.CrossRefGoogle ScholarPubMed
Nabavi, R, Manouchehri Naeini, K, Zebardast, N and Hashemi, H (2014) Epidemiological study of gastrointestinal helminthes of canids in Chaharmahal and Bakhtiari Province of Iran. Iranian Journal of Parasitology 9, 276281.Google ScholarPubMed
Ortlepp, RJ (1933) Joyeuxia fuhrmanni Baer, 1924, a hitherto unrecorded cestode parasite of the domesticated cat in South Africa. Onderstepoort Journal of Veterinary Science and Animal Industry 1, 9798.Google Scholar
Papadopoulos, H, Himonas, C, Papazahariadou, M and Antoniadou-Sotiriadou, K (1997) Helminths of foxes and other wild carnivores from rural areas in Greece. Journal of Helminthology 71, 227231.CrossRefGoogle Scholar
Papazoglou, LG, Diakou, A, Patsikas, MN, Anagnostou, T, Vagiatis, I, Papastefanou, A and Kosmas, P (2006) Intestinal pleating associated with Joyeuxiella pasqualei infection in a cat. Veterinary Record 159, 634635.CrossRefGoogle ScholarPubMed
Petersen, N (1986) Dissection on a micro scale. The Science Teacher 53, 1921.Google Scholar
Poon, RWS, Tam, EWT, Lau, SKP, Cheng, VCC, Yuen, KY, Schuster, RK and Woo, PCY (2017) Molecular identification of cestodes and nematodes by cox1 gene real-time PCR and sequencing. Diagnostic Microbiology and Infectious Disease 89, 185190.CrossRefGoogle ScholarPubMed
Sanchis-Monsonís, G, Fanelli, A, Martínez-Carrasco, C and Tizzani, P (2020) The typical cestodes of the red fox in eastern areas of the Iberian Peninsula have a grouped distribution. Veterinary Parasitology 283, 109168. doi: 10.1016/j.vetpar.2020.109168CrossRefGoogle ScholarPubMed
Schmidt, GD (1986) Handbook of Tapeworm Identification. Boca Raton, FL, USA: CRC Press Inc, p. 33431.Google Scholar
Schuster, RK (2020) Cestodes of the genera Diplopylidium and Joyeuxiella (Eucestoda: Dipylidiiae) – a review of historical data, species inventory and geographical distribution. Scientific Parasitology 21, 117.Google Scholar
Schuster, R and Montag, A (2000) Joyeuxiella pasqualei ein ungewöhnlicher Bandwurm bei einer einheimischen Hauskatze. Kleintierpraxis 45, 867870.Google Scholar
Schuster, RK, Thomas, K, Sivakumar, S and O'Donovan, D (2009) The parasite fauna of stray domestic cats (Felis catus) in Dubai, United Arab Emirates. Parasitology Research 105, 125134.CrossRefGoogle ScholarPubMed
Schuster, RK, Mustafa, MB, Baskar, JV, Rosentel, J, Chester, ST and 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, 26792684.CrossRefGoogle ScholarPubMed
Symeonidou, I, Gelasakis, AI, Arsenopoulos, K, Angelou, A, Beugnet, F and Papadopoulos, E (2018) Feline gastrointestinal parasitism in Greece: emergent zoonotic species and associated risk factors. Parasites and Vectors 11, 227. doi: 10.1186/s13071-018-2812-xCrossRefGoogle ScholarPubMed
Waap, H, Gomes, J and Nunes, T (2014) Parasite communities in stray cat populations from Lisbon, Portugal. Journal of Helminthology 88, 389395.CrossRefGoogle ScholarPubMed
Witenberg, G (1932) On the cestode subfamily Dipylidiinae Stiles. Zeitschrift für Parasitenkunde 4, 541584.CrossRefGoogle Scholar