Experimental cerebral and non-cerebral coenurosis caused by Taenia multiceps in laboratory animals

Document Type : Full paper (Original article)

Authors

1 Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

2 Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

3 Ph.D. Student in Pathology, Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran

Abstract

Background: Coenurosis, caused by the larval stage of Taenia multiceps, is a parasitic disease of considerable importance in veterinary medicine. Aims: This study aimed to evaluate whether rabbits, rats, and mice are susceptible to experimental infection with T. multiceps and can support the migration and/or development of its larval stage following oral inoculation with eggs obtained from adult worms derived from cerebral- and muscular-origin coenuri. Methods: The eggs derived from adult worms originating from cerebral and muscular coenuri, were orally inoculated to two groups of rabbits, rats and mice to trace the predilection sites of the larval stage of parasites. In addition, histopathological examinations were performed on brain and liver tissues from the experimentally infected animals. To identify the parasite in affected tissues based on mitochondrial DNA markers, PCR was performed, using primers targeting the CO1 and ND1 genes, followed by sequencing of the amplified products. Results: Necropsy and histopathological evaluation revealed no coenurus cyst formation in any of the examined tissues. However, eight infected rabbits displayed migratory tracks in the liver, together with histopathological lesions, including cell swelling and focal hemorrhages. Molecular analysis of liver samples confirmed the presence of T. multiceps DNA (CO1 and ND1 mitochondrial markers) in affected tissues. No histopathological changes or parasite remnants were detected in the tissues of infected rats and mice. Conclusion: Rabbits (Oryctolagus cuniculus) may serve as a potential animal model for studying certain aspects of coenurosis pathogenesis. However, further studies are necessary to clarify the role of host-specific factors, immune status, parasite strains, and infection methods in establishing experimental coenurosis.

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Main Subjects

References

Abbas, I; Tamponi, C; Madau, G; Cavallo, L; Varcasia, A and Scala, A (2024). Treatment and management of coenurosis by Taenia multiceps: field data from outbreaks in endemic regions and literature review. Parasit. Vectors. 17: 335.
Adalid-Peralta, L; Lopez-Roblero, A; Camacho-Vázquez, C; Nájera-Ocampo, M; Guevara-Salinas, A; Ruiz-Monroy, N; Melo-Salas, M; Morales-Ruiz, V; López-Recinos, D and Ortiz-Hernández, E (2021). Regulatory t cells as an escape mechanism to the immune response in taenia crassiceps infection. Front. Cell. Infect. Microbiol., 11: 630583.
Ahmadnia, S; Moazeni, M; Mohammadi-Samani, S and Alavi, AM (2014). Hydatid cyst formation in male Balb/c mice following the intraperitoneal injection of live protoscoleces and activated oncospheres: a comparative study. J. Parasit. Dis., 38: 77-80.
Akbari, M; Moazeni, M; Oryan, A; Sharifiyazdi, H and Amrabadi, O (2015). Experimental cerebral and non-cerebral coenurosis in goats: A comparative study on the morphological and molecular characteristics of the parasite. Vet. Parasitol., 211: 201-207.
Alvi, MA; Li, L; Ohiolei, JA; Qamar, W; Saqib, M; Tayyab, MH; Altaf, J; Ashfaq, K; Hassan, A and Jamal, M (2021). Hydatigera taeniaeformis in urban rats (Rattus rattus) in Faisalabad, Pakistan. Infect. Genet. Evol., 92: 104873.
Amrabadi, O; Oryan, A; Moazeni, M; Shari-Fiyazdi, H and Akbari, M (2019). Histopathological and molecular evaluation of the experimentally infected goats by the larval forms of Taenia multiceps. Iran. J. Parasitol., 14: 95-105.
Bariselli, S; Maioli, G; Pupillo, G; Calzolari, M; Torri, D; Cirasella, L; Luppi, A; Torreggiani, C; Garbarino, C and Barsi, F (2023). Identification and phylogenetic analysis of Taenia spp. parasites found in wildlife in the Emilia-Romagna region, northern Italy (2017-2022). Int. J. Parasitol. Parasites Wildl., 22: 20-27.
Betancourt, MA; de Aluja, AS; Sciutto, E; Hernández, M; Bobes, RJ; Rosas, G; Hernández, B; Fragoso, G; Hallal-Calleros, C And Aguilar, L (2012). Effective protection induced by three different versions of the porcine S3Pvac anticysticercosis vaccine against rabbit experimental Taenia pisiformis cysticercosis. Vaccine. 30: 2760-2767.
Bowles, J; Blair, D and McManus, DP (1992). Genetic variants within the genus Echinococcus granulosus identified by mitochon drial DNA sequencing. Mol. Biochem. Parasitol., 54: 165-174.
Bowles, J and McManus, D (1994). Genetic characterization of the Asian Taenia, a newly described taeniid cestode of humans. Am. J. Trop. Med. Hyg., 50: 33-44.
Christodoulopoulos, G; Dinkel, A; Romig, T; Ebi, D; Mackenstedt, U and Loos-Frank, B (2016). Cerebral and non-cerebral coenurosis: on the genotypic and phenotypic diversity of Taenia multiceps. Parasitol. Res., 115: 4543-4558.
Domínguez-Roldan, R; Pérez-Martínez, M; Rosetti, M; Arias-Hernández, D; Bernal-Fernández, G; Flores-Pérez, F and Hallal-Calleros, C (2018). High frequency of Taenia pisiformis metacestodes and high sex-associated susceptibility to cysticercosis in naturally infected wild rabbits. Parasitol. Res., 117: 2201-2206.
Flatt, RE and Campbell, WW (1974). Cysticercosis in rabbits: incidences and lesions of the naturally occurring disease in young domestic rabbits. Lab. Anim. Sci., 24: 914-918.
Flatt, RE and Moses, RE (1975). Lesions of experimental cysticercosis in domestic rabbits. Lab. Anim. Sci., 25: 162-167.
Gomez-Puerta, LA; Vargas-Calla, A; Garcia-Leandro, M; Jara-Vila, J; Rojas-Anticona, W; Pacheco, JI; Angulo-Tisoc, JM; Silva, W and Gonzalez, AE (2023). Identification of wild rodents as intermediate hosts for Hydatigera taeniaeformis in Peru. Parasitol. Res., 122: 1915-1921.
Gunyakti Kilinc, S; Celik, F; Kesik, HK and Simsek, S (2020). In silico analysis of the biodiversity and conservation status of mitochondrial cytochrome C oxidase subunit 1 (CO1) gene of Taenia multiceps. Acta Parasitol., 65: 852-858.
Gururaj, K; Pawaiya, RS; Gangwar, NK; Mishra, AK; Singh, DD; Andani, D; Paul, S; Sharma, N; Shivasharanappa, N and Rahal, A (2019). Comparative molecular characterization and phylogenetic analysis of cerebral and non-cerebral coenurosis in Indian goats. Vet. Parasitol. Reg. Stud. Reports. 15: 100266.
Hallal-Calleros, C; Morales-Montor, J; Orihuela-Trujillo, A; Togno-Peirce, C; Murcia-Mejía, C; Bielli, A; Hoffman, KL and Flores-Pérez, FI (2016). Taenia pisiformis cysticercosis induces decreased prolificacy and increased progesterone levels in rabbits. Vet. Parasitol., 229: 50-53.
Haq, SU; Malik, MA; Alshammari, A; Yameen, AB; Wakid, MH; Alvi, MA; Kabli, AM; Saqib, M; Qamar, W; Sajid, MS and Gao, F (2024). Genetic variation and population structure of Taenia multiceps (Coenurus cerebralis) based on mitochondrial cox1 gene: A comprehensive global analysis. Infect. Genet. Evol., 125: 105676.
Hidifira, AM; Alvares-Saraiva, AM; Perez, EC; Spadacci-Morena, DD; de Araujo, RS and Lallo, MA (2023). Increased susceptibility to encephalitozoonosis associated with mixed Th1/Th2 profile and M1/M2 profile in mice immunosuppressed with cyclophosphamide. Exp. Parasitol., 254: 108606.
Huang, X; Chen, L; Yang, Y; Gu, X; Wang, Y; Lai, W; Peng, X and Yang, G (2015). Expression, tissue localization and serodiagnostic potential of Taenia multiceps acidic ribosomal protein P2. Parasit. Vectors. 8: 1-9.
Huang, X; Xu, J; Wang, Y; Guo, C; Chen, L; Gu, X; Lai, W; Peng, X and Yang, G (2016). GP50 as a promising early diagnostic antigen for Taenia multiceps infection in goats by indirect ELISA. Parasit. Vectors. 9: 1-8.
Ito, A; Nakaya, K; Sako, Y; Nakao, M and Ito, M (2001). NOD-scid mouse as an experimental animal model for cysticercosis. Southeast Asian J. Trop. Med. Public Health. 32: 85-89.
Jenkins, DJ; Urwin, NA; Williams, TM; Mitchell, KL; Lievaart, JJ and Armua-Fernandez, MT (2014). Red foxes (Vulpes vulpes) and wild dogs (dingoes (Canis lupus dingo) and dingo/domestic dog hybrids), as sylvatic hosts for Australian Taenia hydatigena and Taenia ovis. Int. J. Parasitol. Parasites Wildl., 3: 75-80.
Jiménez, L; Díaz-Zaragoza, M; Hernández, M; Navarro, L; Hernández-Ávila, R; Encarnación-Guevara, S; Ostoa-Saloma, P and Landa, A (2023). Differential protein expression of Taenia crassiceps ORF strain in the murine cysticercosis model using resistant (C57BL/6) mice. Pathogens. 12: 678.
Kandil, O; Nassar, SA; Nasr, SM; Fahmy, HA; Mahmoud, MS; El Nemaky, AH; Shalaby, HA and Abdelrahman, KA (2013). Biochemical and histopathological changes in balb/C mice-as an experimental animal model-infected with Taenia saginata oncospheres. Glob. Vet., 11: 528-533.
Labuschagne, J; Frean, J; Parbhoo, K; Mutyaba, D; Pillay, T; Boughan, S and Nkala, H (2022). Disseminated human subarachnoid coenurosis. Trop. Med. Infect. Dis., 7: 405.
Lavikainen, A; Haukisalmi, V; Lehtinen, MJ; Henttonen, H; Oksanen, A and Meri, S (2008). A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data. Parasitology. 135: 1457-1467.
Li, W; Liu, B; Yang, Y; Ren, Y; Wang, S; Liu, C; Zhang, N; Qu, Z; Yang, W and Zhang, Y (2018). The genome of tapeworm Taenia multiceps sheds light on understanding parasitic mechanism and control of coenurosis disease. DNA Research. 25: 499-510.
Li, WH; Yang, Y; Zhang, NZ; Wang, JK; Liu, YJ; Li, L; Yan, HB; Jia, WZ and Fu, B (2021). Comparative transcriptome analyses of the developmental stages of Taenia multiceps. Front. Vet. Sci., 8: 677045.
Liu, Y; Guo, C; Dong, X; Gu, X; Xie, Y; Lai, W; Peng, X and Yang, G (2019). Molecular characterisation and expression analysis of two heat-shock proteins in Taenia multiceps. Parasit. Vectors. 12: 1-10.
Mamuti, W; Yamasaki, H; Sako, Y; Nakaya, K; Nakao, M; Lightowlers, MW and Ito, A (2002). Usefulness of hydatid cyst fluid of Echinococcus granulosus developed in mice with secondary infection for serodiagnosis of cystic echinococcosis in humans. Clin. Vaccine Immunol., 9: 573-576.
Moazeni, M; Larki, S; Oryan, A and Saharkhiz, MJ (2014a). Preventive and therapeutic effects of Zataria multiflora methanolic extract on hydatid cyst: An in vivo study. Vet. Parasitol., 205: 107-112.
Moazeni, M; Larki, S; Saharkhiz, MJ; Oryan, A; Ansary Lari, M and Mootabi Alavi, A (2014b). In vivo study of the efficacy of the aromatic water of Zataria multiflora on hydatid cysts. Antimicrob. Agents Chemother., 58: 6003-6008.
Mohammadi, P; Zakian, A; Farjanikish, G; Yeganeh, FF; Raisi, A and Samadipoor, M (2021). Clinical report of Coenurosis cerebralis outbreak in Lori sheep. Comp. Clin. Path., 30: 729-733.
O'Reilly, A; McCowan, C; Hardman, C and Stanley, R (2002). Taenia serialis causing exophthalmos in a pet rabbit. Vet. Ophthalmol., 5: 227-230.
Oryan, A; Moazeni, M; Amrabadi, O; Akbari, M and Sharifiyazdi, H (2015). Comparison of distribution pattern, pathogenesis and molecular characteristics of larval stages of Taenia multiceps in sheep and goats. Small. Rumin. Res., 132: 44-49.
Oryan, A; Nazifi, S; Sharifiyazdi, H and Ahmadnia, S (2010). Pathological, molecular, and biochemical characterization of Coenurus gaigeri in Iranian native goats. J. Parasitol., 96: 961-967.
Owiny, JR (2001). Cysticercosis in laboratory rabbits. J. Am. Assoc. Lab. Anim. Sci., 40: 45-48.
Peng, SY; Chu, TH; Wang, IC; Chung, WC; Yu, KW; Tsaihong, JC; Huang, JC and Fan, PC (2009). Infection of normal C3H/HeN mice with Taenia saginata asiatica oncospheres. Res. Vet. Sci., 86: 261-266.
Philipo, V; Lupindu, AM and Nzalawahe, JS (2024). Epidemiology and molecular identification of Coenurus cerebralis in sheep and goats in Mpwapwa District, Tanzania: Factors to consider in control plans. Vet. Med. Int., 1: 5055115.
Remesar, S; Castro-Scholten, S; Jiménez-Martín, D; Camacho-Sillero, L; Morrondo, P; Rouco, C; Gómez-Guillamón, F; Cano-Terriza, D and García-Bocanegra, I (2021). Spatiotemporal monitoring of Cysticercus pisiformis in European wild rabbit (Oryctolagus cuniculus) in Mediterranean ecosystems in southern Spain. Prev. Vet. Med., 197: 105508.
Rickard, M and Coman, B (1977). Studies on the fate of Taenia hydatigena and Taenia ovis larvae in rabbits, and cross-immunity with Taenia pisiformis larvae. Int. J. Parasitol., 7: 257-267.
Rosa, DR; David, AH; Emmanuel, DG; Edda, S; Virginio, AF; Ivan, FP and Claudia, HC (2022). Decreased embryo implantation in rabbits infected with Taenia pisiformis. Parasitol. Res., 121: 3689-3692.
Soulsby, EJL (1968). Helminths, arthropods and protozoa of domesticated animals.
Tamarozzi, F; Kibona, T; de Glanville, WA; Mappi, T; Adonikamu, E; Salewi, A; Misso, K; Maro, V; Casulli, A and Santoro, A (2022). Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities. Parasit. Vectors. 15: 396.
Tas, A; Sen, I; Hatipoglu, F; Ari, HH; Risvanli, A; Salykov, R; Ozdal, N; Samsaliev, M; Tolomusev, S and Abdimanap Uulu, N (2024). Surgical removal of Coenurus cerebralis cysts located in the brain of sheep. J. Appl. Anim. Res., 52: 2292362.
Thakre, B; Joseph, JP; Kumar, B; Brahmbhatt, N and Gamit, K (2019). Taeniasis in a German shepherd pup: A case report. Ind. J. Vet. Sci. Biotech., 15: 83-84.
Toral-Bastida, E; Garza-Rodriguez, A; Jimenez-Gonzalez, DE; Garcia-Cortes, R; Avila-Ramirez, G; Maravilla, P and Flisser, A (2011). Development of Taenia pisiformis in golden hamster (Mesocricetus auratus). Parasit. Vectors. 4: 1-4.
Tsotetsi-Khambule, A; Njiro, S; Katsande, T and Harrison, L (2018). Risk factors associated with taeniosis-cysticercosis in rural farming communities in Gauteng Province, South Africa. Trop. Anim. Health Prod., 50: 1951-1955.
Varcasia, A; Tamponi, C; Ahmed, F; Cappai, MG; Porcu, F; Mehmood, N; Dessì, G and Scala, A (2022). Taenia multiceps coenurosis: a review. Parasit. Vectors. 15: 84.
Wang, ZX; Chen, X; Han, L; Liu, HD; Guo, JH; Zhao, Y and Sun, XL (2021). Generation and application of a monoclonal antibody against the 18-kDa oncosphere antigen of Taenia pisiformis. Exp. Parasitol., 224: 108096.
Worley, DE (1974). Quantitative studies on the migration and development of Taenia pisiformis larvae in laboratory rabbits. Lab. Anim. Sci., 24: 517-522.
Yu, J; Fu, J; Liu, H; Kang, C; Wang, Z; Jin, Y; Wu, S; Li, T; Yang, R and Jin, M (2024). Application of recombinant lactic acid bacteria (LAB) live vector oral vaccine in the prevention of F4+ enterotoxigenic Escherichia coli. Vaccines. 12: 304.
Zhang, XY; Jian, YN; Ma, LQ; Li, XP and Karanis, P (2018). A case of coenurosis in a wild rabbit (Lepus sinensis) caused by Taenia serialis metacestode in Qinghai
Tibetan Plateau Area, China. Korean J. Parasitol., 56: 195.
Zhang, LQ; Yen, Y; Zheng, YL and Liu, DC (2007). Meiotic restriction in emmer wheat is controlled by one or more nuclear genes that continue to function in derived lines. Sex Plant Reprod., 20: 159-166.
Zhu, GQ; Li, L; Ohiolei, JA; Wu, YT; Li, WH; Zhang, NZ; Fu, BQ; Yan, HB and Jia, WZ (2019). A multiplex PCR assay for the simultaneous detection of Taenia hydatigena, T. multiceps, T. pisiformis, and Dipylidium caninum infections. BMC Infect. Dis., 19: 1-7.

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