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Global epidemiology and molecular biology of Taenia multiceps: a comparative meta-analysis and in silico analysis study

Published online by Cambridge University Press:  12 August 2022

Ibrahim Abbas*
Affiliation:
Parasitology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
El-Sayed El-Alfy
Affiliation:
Parasitology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
Somaya Saleh
Affiliation:
Parasitology Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
Claudia Tamponi
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
Antonio Varcasia
Affiliation:
Department of Veterinary Medicine, University of Sassari, Sassari, Italy
*
Author for correspondence: Ibrahim Abbas, E-mail: ielsayed@mans.edu.eg

Abstract

In the present study, all published data on the epidemiology and molecular characters of Taenia multiceps were systematically collected from relevant databases (e.g. PubMed, Scopus, National Center for Biotechnology Information), and combined in various statistical and genetic analyses as a contribution to a better understanding of the epidemiology of this ubiquitous taeniid worldwide. While 5.8% of the key hosts (dogs) from various countries had T. multiceps, grey wolves displayed the highest prevalence (21.6%) among the definitive hosts. Small ruminants are the main intermediate hosts and carry the coenuri in various locations, but most commonly in the central nervous system (CNS). Cerebral coenuri were confirmed in 53% of sheep exhibiting neurological symptoms, and infected animals often had only a single coenurus in the brain. Sheep had a higher prevalence (8.8%) of CNS coenuri than goats (5.8%); however, extra-CNS coenuri were detected more frequently in goats than in sheep. In either case, the difference between sheep and goats was statistically insignificant. Analysis of 233 partial cytochrome oxidase subunit I nucleotide sections for T. multiceps revealed high haplotype and low nucleotide diversities. Fifty-one haplotypes were detected circulating in 6 geographic populations. China, Iran and Turkey had 2 major haplotypes, whereas Italy and Egypt shared 3. Haplotypes from Greece circulate worldwide, and displayed similar gene flow values when compared with the other populations. There were no distinct patterns for haplotype distribution in relation to the infected hosts or coenuri locations. The existence of genetic variants in T. multiceps was highlighted, but needs further studies.

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

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Footnotes

*

Equal contribution.

References

Abbas, I, El-Alfy, ES, Janecek-Erfurth, E and Strube, C (2021) Molecular characterization of Cysticercus tenuicollis isolates from sheep in the Nile Delta, Egypt and a review on Taenia hydatigena infections worldwide. Parasitology 148, 913933.CrossRefGoogle Scholar
Abuladze, KI (1964) Taeniata of animals and man and the diseases caused by them (in Russian). In Skrjabin, KI (ed.), Essentials of Cestodology. Jerusalem: Israel Program for Scientific Translocations, p. 530.Google Scholar
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. Veterinary Parasitology 211, 201207.CrossRefGoogle ScholarPubMed
Al-Riyami, S, Ioannidou, E, Koehler, AV, Hussain, MH, Al-Rawahi, AH, Giadinis, ND, Lafi, SQ, Papadopoulos, E and Jabbar, A (2016) Genetic characterisation of Taenia multiceps cysts from ruminants in Greece. Infection Genetics and Evolution 38, 110116.CrossRefGoogle ScholarPubMed
Amer, S, ElKhatam, A, Fukuda, Y, Bakr, LI, Zidan, S, Elsify, A, Mohamed, MA, Tada, C and Nakai, Y (2017) Prevalence and identity of Taenia multiceps cysts ‘Coenurus cerebralis’ in sheep in Egypt. Acta Tropica 176, 270276.CrossRefGoogle ScholarPubMed
Amrabadi, O, Oryan, A, Moazeni, M, Sharifiyazdi, H and Akbari, M (2015) Comparison of cerebral and non-cerebral coenurosis by genetic markers of glycolytic enzyme (enolase) and mitochondrial sequences in sheep and goats. Veterinary Parasitology 214, 333336.CrossRefGoogle ScholarPubMed
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. Iranian Journal of Parasitology 14, 95105.Google ScholarPubMed
Avcioglu, H, Yildirim, A, Duzlu, O, Inci, A, Terim, KAK and Balkaya, I (2011) Prevalence and molecular characterization of bovine coenurosis from Eastern Anatolian region of Turkey. Veterinary Parasitology 176, 5964.CrossRefGoogle ScholarPubMed
Bondareva, VI (1963) Coenurus invasion in domestic and wild animals (in Russian). Alma-Aty: Academy of Sciences of the Kazach SSR Publishing house, p. 356.Google Scholar
Christodoulopoulos, G, Kassab, A and Theodoropoulos, G (2013) Occurrence of non-cerebral coenurosis in sheep. Journal of Helminthology 87, 125127.CrossRefGoogle ScholarPubMed
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. Parasitology Research 115, 45434558.CrossRefGoogle ScholarPubMed
Deplazes, P, Eichenberger, RM and Grimm, F (2019) Wildlife transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates. International Journal for Parasitology: Parasites and Wildlife 9, 342358.Google ScholarPubMed
Edwards, GT and Herbert, IV (1982) Preliminary investigations into the immunization of lambs against infection with Taenia multiceps metacestodes. Veterinary Parasitology 9, 211216.CrossRefGoogle ScholarPubMed
Evangelisti, MA, Deiana, R, Melosu, V, Burrai, GP, Ballocco, I, Varcasia, A, Scala, A and Manunta, ML (2018) Relationships among neuroscore, magnetic resonance imaging features, and intracranial pressure in sheep affected by slow-growing brain lesions. Veterinary Radiology & Ultrasound 59, 305311.CrossRefGoogle ScholarPubMed
Fu, YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915925.Google ScholarPubMed
Gasser, RB, Zhu, X and McManus, DP (1999) NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). International Journal for Parasitology 29, 19651970.CrossRefGoogle ScholarPubMed
Giadinis, ND, Psychas, V, Polizopoulou, Z, Papadopoulos, E, Papaioannou, N, Komnenou, A, Thomas, AL, Petridou, EJ, Kritsepi-Konstantinou, M, Lafi, SQ and Brellou, GD (2012) Acute coenurosis of dairy sheep from 11 flocks in Greece. New Zealand Veterinary Journal 60, 247253.CrossRefGoogle ScholarPubMed
Godara, R, Katoch, R, Yadav, A, Khajuria, JK and Borkataki, S (2011 a) Coenurosis in small ruminants: an overview. Veterinary Practitioner 12, 102105.Google Scholar
Godara, R, Borah, MK, Sharma, RL and Jangir, BL (2011 b) Caprine coenurosis with special reference to hepatic coenurosis. Comparative Clinical Pathology 20, 277280.CrossRefGoogle Scholar
Goeze, JAE (1780) Das Drehen der Schafe. Neue oeconomische Nachrichten der patriotriotischen Gesellschaft in Schlesien 1, 2127.Google Scholar
Gökçe, E, Beytut, E, Tașcİ, GT, Uzlu, E, Kİrmİzİgül, AH and Erdoğan, HM (2013) An outbreak of coenurosis in a cattle farm. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 19(suppl. A), 199202.Google Scholar
Gururaj, K, Pawaiya, RS, Gangwar, NK, Mishra, AK, Singh, DD, Andani, D, Paul, S, Sharma, N, Shivasharanappa, N, Rahal, A, Chaturvedi, VK, Kumar, A and Sharma, DK (2019) Comparative molecular characterization and phylogenetic analysis of cerebral and non-cerebral coenurosis in Indian goats. Veterinary Parasitology: Regional Studies and Reports 15, 100266.Google ScholarPubMed
Hall, MC (1916) A new and economically important tapeworm, Multiceps gaigeri, from the dog. Journal of the American Veterinary Medical Association 50, 214223.Google Scholar
Heath, DD, Parmeter, SN and Osborn, PJ (1980) An attempt to immunise dogs against Taenia hydatigena. Research in Veterinary Science 29, 388389.CrossRefGoogle ScholarPubMed
Hegglin, D, Bontadina, F, Contesse, P, Gloor, S and Deplazes, P (2007) Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Functional Ecology 21, 552560.CrossRefGoogle Scholar
Henke, SE, Pence, DB and Bryant, FC (2002) Effect of short-term coyote removal on populations of coyote helminths. Journal of Wildlife Diseases 38, 5467.Google ScholarPubMed
Hoberg, EP (2002) Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859866.CrossRefGoogle ScholarPubMed
Hoberg, EP (2006) Phylogeny of Taenia: species definitions and origins of human parasites. Parasitology International 55, 2330.CrossRefGoogle ScholarPubMed
Hoberg, EP, Jones, A, Rausch, RL, Eom, KS and Gardner, SL (2000) A phylogenetic hypothesis for species of the genus Taenia (Eucestoda: Taeniidae). Journal of Parasitology 86, 8998.CrossRefGoogle ScholarPubMed
Hoberg, EP, Alkire, NL, Queiroz, AD and Jones, A (2001) Out of Africa: origins of the Taenia tapeworms in humans. Proceedings of the Royal Society of London. Series B: Biological Sciences 268, 781787.CrossRefGoogle ScholarPubMed
Hunter, JP, Saratzis, A, Sutton, AJ, Boucher, RH, Sayers, RD and Bown, MJ (2014) In meta-analyses of proportion studies, funnel plots were found to be an inaccurate method of assessing publication bias. Journal of Clinical Epidemiology 67, 897903.CrossRefGoogle ScholarPubMed
Kaartinen, S, Luoto, M and Kojola, I (2009) Carnivore-livestock conflicts: determinants of wolf (Canis lupus) depredation on sheep farms in Finland. Biodiversity and Conservation 18, 3503.CrossRefGoogle Scholar
Kheirandish, R, Sami, M, Azizi, S and Mirzaei, M (2012) Prevalence, predilection sites and pathological findings of Taenia multiceps coenuri in slaughtered goats from south-east Iran. Onderstepoort Journal of Veterinary Research 79, 15.CrossRefGoogle ScholarPubMed
Kilinc, SG, 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 Parasitologica 65, 852858.CrossRefGoogle Scholar
Lange, PNA, Lelieveld, G and De Knegt, HJ (2021) Diet composition of the golden jackal Canis aureus in south-east Europe – a review. Mammal Review 51, 207213.CrossRefGoogle Scholar
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, 14571467.CrossRefGoogle ScholarPubMed
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.CrossRefGoogle Scholar
Leske, NG (1780) Von dem Drehen der Schafe und dem Blasenbandwurme im Gehirne derselben, als der Ursache dieser Krankheit. Müller in Komm, 1–4.Google Scholar
Ligios, C, Viglietti, A, Carta, P, Dexter, G, Simmons, MM and Agrimi, U (2004) Clinicopathological findings in sheep from Sardinia showing neurological signs of disease. Veterinary Record 154, 365370.CrossRefGoogle ScholarPubMed
Lymbery, AJ (2017) Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Advances in Parasitology 95, 111145.CrossRefGoogle ScholarPubMed
Maddison, DR, Swofford, DL and Maddison, WP (1997) NEXUS: an extensible file format for systematic information. Systematic Biology 46, 590621.CrossRefGoogle ScholarPubMed
Mohammadi, P, Zakian, A, Farjanikish, G, Yeganeh, FF, Raisi, A and Samadipoor, M (2021) Clinical report of Coenurosis cerebralis outbreak in Lori sheep. Comparative Clinical Pathology 30, 729733.CrossRefGoogle Scholar
Murai, É and Sugár, L (1979) Taeniid species in Hungary (Cestoda, Taeniidae). I. Cysticercosis, coenurosis and hydatidosis of wild ungulates. Parasitologia Hungarica 12, 4152.Google Scholar
Oryan, A, Nazifi, S, Sharifiyazdi, H and Ahmadnia, S (2010) Pathological, molecular, and biochemical characterization of Coenurus gaigeri in Iranian native goats. Journal of Parasitology 96, 961967.CrossRefGoogle ScholarPubMed
Oryan, A, Akbari, M, Moazeni, M and Amrabadi, OR (2014) Cerebral and non-cerebral coenurosis in small ruminants. Tropical Biomedicine 31, 116.Google ScholarPubMed
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 Ruminant Research 132, 4449.CrossRefGoogle Scholar
Ozmen, O, Sahinduran, S, Haligur, M and Sezer, K (2005) Clinicopathologic observations on Coenurus cerebralis in naturally infected sheep. Schweizer Archiv für Tierheilkunde 147, 129134.CrossRefGoogle ScholarPubMed
Pintus, D, Varcasia, A, Dessì, G, Tamponi, C, Manunta, ML, Carboni, GA, Cancedda, MG, Ligios, C and Scala, A (2018) Atypical outbreak of acute coenurosis by Taenia multiceps in a sheep flock. Parasitology Research 117, 19851988.CrossRefGoogle Scholar
Polizopoulou, SZ, Giadinis, DN, Papahristou, A and Papaioannou, N (2016) Neurological diseases of small ruminants in Greece: a retrospective study in 114 flocks. Acta Veterinaria-Beograd 66, 160171.CrossRefGoogle Scholar
Popov, NP (1937) Cenuroz myshc ovec. Ucennye Zapisi Kazanskogo Gosudarstvennogo Zooveterinarnogo Instituta 47, 353363.Google Scholar
Rostami, S, Salavati, R, Beech, RN, Sharbatkhori, M, Babaei, Z, Saedi, S and Harandi, MF (2013 a) Cytochrome c oxidase subunit 1 and 12S ribosomal RNA characterization of Coenurus cerebralis from sheep in Iran. Veterinary Parasitology 197, 141151.CrossRefGoogle ScholarPubMed
Rostami, S, Beech, RN, Salavati, R, Baneshi, MR, Kamyabi, H and Harandi, MF (2013 b) Morphometric analysis of larval rostellar hooks in Taenia multiceps of sheep in Iran and its association with mitochondrial gene variability. Iranian Journal of Parasitology 8, 579585.Google ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 32993302.CrossRefGoogle ScholarPubMed
Scala, A and Varcasia, A (2006) Updates on morphobiology, epidemiology and molecular characterization of coenurosis in sheep. Parassitologia 48, 6163.Google ScholarPubMed
Scala, A, Cancedda, GM, Varcasia, A, Ligios, C, Garippa, G and Genchi, C (2007) A survey of Taenia multiceps coenurosis in Sardinian sheep. Veterinary Parasitology 143, 294298.CrossRefGoogle ScholarPubMed
Schuster, RK, Sivakumar, S, Wieckowsky, T and Reiczigel, J (2015) Abattoir survey on extra-cerebral coenurosis in goats. Helminthologia 52, 303309.CrossRefGoogle Scholar
Scott, PR (2012) Diagnosis and treatment of coenurosis in sheep. Veterinary Parasitology 189, 7578.CrossRefGoogle ScholarPubMed
Sharma, DK and Chauhan, PPS (2006) Coenurosis status in Afro-Asian region: a review. Small Ruminant Research 64, 197202.CrossRefGoogle Scholar
Sharma, M, Fomda, BA, Mazta, S, Sehgal, R, Singh, B and Malla, N (2013) Genetic diversity and population genetic structure analysis of Echinococcus granulosus sensu stricto complex based on mitochondrial DNA signature. PLoS ONE 8, e82904.CrossRefGoogle ScholarPubMed
Sikandar, A, Adil, M, Zaneb, H, Arshad, M, Ali, HM and Khan, MA (2018) Concurrent cerebral and extra-cerebral caprine coenurosis: a case report. Pakistan Journal of Life and Social Sciences 16, 5558.Google Scholar
Tajima, F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.CrossRefGoogle ScholarPubMed
Tan, L, Wang, AB, Zheng, SQ, Zhang, XL, Huang, CJ and Liu, W (2018) Molecular characterization and phylogenetic analysis of Taenia multiceps from China. Acta Parasitologica 63, 721727.CrossRefGoogle ScholarPubMed
Varcasia, A, Lightowlers, MW, Cattoli, G, Cancedda, GM, Canu, S, Garippa, G and Scala, A (2006) Genetic variation within Taenia multiceps in Sardinia, western Mediterranean (Italy). Parasitology Research 99, 622626.CrossRefGoogle ScholarPubMed
Varcasia, A, Jia, WZ, Yan, HB, Manunta, ML, Pipia, AP, Garippa, G, Scala, A and Schuster, RK (2012) Molecular characterization of subcutaneous and muscular coenurosis of goats in United Arab Emirates. Veterinary Parasitology 190, 604607.CrossRefGoogle ScholarPubMed
Varcasia, A, Pipia, AP, Arru, D, Pes, AM, Tamponi, C, Dore, F, Garippa, G and Scala, A (2013) Morphological and molecular characterization of bovine coenurosis in Sardinia, Italy. Parasitology Research 112, 20792082.CrossRefGoogle ScholarPubMed
Varcasia, A, Tamponi, C, Tosciri, G, Pipia, AP, Dore, F, Schuster, RK, Kandil, OM, Manunta, ML and Scala, A (2015) Is the red fox (Vulpes vulpes) a competent definitive host for Taenia multiceps? Parasites and Vectors 8, 491496.CrossRefGoogle ScholarPubMed
Varcasia, A, Pipia, AP, Dessì, G, Zidda, A, Tamponi, C, Pau, M, Scala, A and Boufana, B (2016) Morphology and genetic variability within Taenia multiceps in ruminants from Italy. Veterinary Parasitology 223, 181185.CrossRefGoogle ScholarPubMed
Varcasia, A, Tamponi, C, Ahmed, F, Cappai, MG, Porcu, F, Mehmood, N, Dessì, G and Scala, A (2022) Taenia multiceps coenurosis: a review. Parasites and Vectors 15, 84.CrossRefGoogle ScholarPubMed
Vasileiou, NGC, Fthenakis, GC and Papadopoulos, E (2015) Dissemination of parasites by animal movements in small ruminant farms. Veterinary Parasitology 213, 5660.CrossRefGoogle ScholarPubMed
Verster, A (1969) A toxonomic revision of the genus Taenia Linnaeus, 1758 S. str. Onderstepoort Journal of Veterinary Research 36, 358.Google ScholarPubMed
Wallace, BC, Dahabreh, IJ, Trikalinos, TA, Lau, J, Trow, P and Schmid, CH (2012) Closing the gap between methodologists and end-users: R as a computational back-end. Journal of Statistical Software 49, 115.CrossRefGoogle Scholar
Wang, CR, Qiu, JH, Zhao, JP, Xu, LM, Yu, WC and Zhu, XQ (2006) Prevalence of helminthes in adult dogs in Heilongjiang Province, the People's Republic of China. Parasitology Research 99, 627630.CrossRefGoogle ScholarPubMed
Willis, JM and Herbert, IV (1984) Some factors affecting the eggs of Taenia multiceps: their transmission onto pasture and their viability. Annals of Tropical Medicine & Parasitology 78, 236242.CrossRefGoogle ScholarPubMed
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