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Cerebral and non-cerebral coenurosis: on the genotypic and phenotypic diversity of Taenia multiceps

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Abstract

We characterised the causative agents of cerebral and non-cerebral coenurosis in livestock by determining the mitochondrial genotypes and morphological phenotypes of 52 Taenia multiceps isolates from a wide geographical range in Europe, Africa, and western Asia. Three studies were conducted: (1) a morphological comparison of the rostellar hooks of cerebral and non-cerebral cysts of sheep and goats, (2) a morphological comparison of adult worms experimentally produced in dogs, and (3) a molecular analysis of three partial mitochondrial genes (nad1, cox1, and 12S rRNA) of the same isolates. No significant morphological or genetic differences were associated with the species of the intermediate host. Adult parasites originating from cerebral and non-cerebral cysts differed morphologically, e.g. the shape of the small hooks and the distribution of the testes in the mature proglottids. The phylogenetic analysis of the mitochondrial haplotypes produced three distinct clusters: one cluster including both cerebral isolates from Greece and non-cerebral isolates from tropical and subtropical countries, and two clusters including cerebral isolates from Greece. The majority of the non-cerebral specimens clustered together but did not form a monophyletic group. No monophyletic groups were observed based on geography, although specimens from the same region tended to cluster. The clustering indicates high intraspecific diversity. The phylogenetic analysis suggests that all variants of T. multiceps can cause cerebral coenurosis in sheep (which may be the ancestral phenotype), and some variants, predominantly from one genetic cluster, acquired the additional capacity to produce non-cerebral forms in goats and more rarely in sheep.

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References

  • Abuladze KI (1964) Taeniata of animals and man and diseases caused by them. In: Skrjabin KI (ed) Essentials of cestodology, vol IV. Israel Program for Scientific Translations, Jerusalem, p 530

    Google Scholar 

  • Afonso SMS, Mukaratirwa S, Hajovska K, Capece BPS, Cristòfol C, Arboix M, Neves L (2011) Prevalence and morphological characteristics of Taenia multiceps cysts (Coenurus cerebralis) from abattoir-slaughtered and experimentally infected goats. J Neuroparasitology 2:5. doi:10.4303/jnp/235532

    Article  Google Scholar 

  • Akbari M, Moazeni M, Oryan A, Sharifiyazdi H, 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

    Article  PubMed  Google Scholar 

  • Amrabadi O, Oryan A, Moazeni M, Sharifiyazdi H, Akbari M (2015) Comparison of cerebral and non-cerebral coenurosis by genetic markers of glycolytic enzyme (enolase) and mitochondrial sequences in sheep and goats. Vet Parasitol 214:333–336

    Article  CAS  PubMed  Google Scholar 

  • Avcioglu H, Yildirim A, Duzlu O, Inci A, Kapakin Terim KA, Balkaya I (2011) Prevalence and molecular characterization of bovine coenurosis from Eastern Anatolian region of Turkey. Vet Parasitol 176:59–64

    Article  CAS  PubMed  Google Scholar 

  • Baer JG (1926) Cestodes de Mammifères. Bulletin de la Société neuchâteloise des sciences naturelles 50:77–81

    Google Scholar 

  • Bowles J, McManus DP (1993) NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol 23:969–972

    Article  CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasit 54:165–173

    Article  CAS  Google Scholar 

  • Christodoulopoulos G (2007) Two rare clinical manifestations of coenurosis in sheep. Vet Parasitol 143:368–370

    Article  CAS  PubMed  Google Scholar 

  • Christodoulopoulos G, Theodoropoulos G, Petrakos G (2008) Epidemiological survey of cestode-larva disease in Greek sheep flocks. Vet Parasitol 153:368–373

    Article  CAS  PubMed  Google Scholar 

  • Christodoulopoulos G, Kassab A, Theodoropoulos G (2013) Occurrence of non-cerebral coenurosis in sheep. J Helminthol 87:125–127

    Article  CAS  PubMed  Google Scholar 

  • Christodoulopoulos G, Kassab A, Theodoropoulos G (2015) Characteristics of non-cerebral coenurosis in tropical goats. Vet Parasitol 211:216–222

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Corret F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890

    Article  Google Scholar 

  • Dinkel A, von Nickisch-Rosenegk M, Bilger B, Merli M, Lucius R, Romig T (1998) Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis as an alternative to necropsy. J Clin Microbiol 36:1871–1876

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dinkel A, Njoroge EM, Zimmermann A, Wälz M, Zeyhle E, Elmahdi IE, Mackenstedt U, Romig T (2004) A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, with reference to the epidemiological situation in eastern Africa. Int J Parasitol 34:645–653

    Article  CAS  PubMed  Google Scholar 

  • Gaiger SH (1907) Coenurus serialis found in two goats in India. J Trop Vet Sci 2:316–321

    Google Scholar 

  • Gubányi A (1995) Morphometries of taeniid tapeworms I. Multivariate analysis of distance measurements of the rostellar hooks. Parasit hung 28:21–41

    Google Scholar 

  • Hall MC (1910) The gid parasite and allied species of the genus Multiceps. I. Historical review. Dept Agric Buro Anim Ind Bull 125:1–68

    Google Scholar 

  • Hall MC (1916) A new and economically important tapeworm, Multiceps gaigeri, from the dog. J Am Vet Med Assoc 50:214–223

    Google Scholar 

  • Hall MC (1920) The adult taenioid cestodes of dogs and cats, and of related carnivores in North America. Proc US Nat Hist Mus 55:1–94

    Article  Google Scholar 

  • Ing MB, Schantz PM, Turner JA (1998) Human coenurosis in North America: case reports and review. Clin Infect Dis 27:519–523

    Article  CAS  PubMed  Google Scholar 

  • Kheirandish R, Sami M, Azizi S, Mirzaei M (2012) Prevalence, predilection sites and pathological findings of Taenia multiceps coenuri in slaughtered goats from south-east Iran. Onderstepoort J Vet 79(1):5. doi:10.4102/ojvr.v79i1.436

    Article  Google Scholar 

  • Lavikainen A, Iwaki T, Haukisalmi V, Konyaev SV, Casiraghi M, Dokuchaev NE, Galimberti A, Halajian A, Henttonen H, Ichikawa-Seki M, Itagaki T, Krivopalov AV, Meri S, Morand S, Näreaho A, Olsson GE, Ribas A, Terefe Y, Nakao M (2016) Reappraisal of Hydatigera taeniaeformis (Batsch, 1786) (Cestoda: Taeniidae) sensu lato with description of Hydatigera kamiyai n. sp. Int J Parasitol 46:361–374

    Article  PubMed  Google Scholar 

  • Linscott AJ et al (2015) Manual of clinical microbiology, vol 2, 11th edn. American Society for Microbiology, Washington, pp 2310–2316

    Google Scholar 

  • Loos-Frank B (2000) An up-date of Verster’s (1969) ‘Taxonomic revision of the genus Taenia Linnaeus’ (Cestoda) in table format. Syst Parasitol 45:155–183

    Article  CAS  PubMed  Google Scholar 

  • Nakao M, Lavikainen A, Iwaki T, Haukisalmi V, Konyaev S, Oku Y, Okamoto M, Ito A (2013) Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. Int J Parasitol 43:427–437

    Article  CAS  PubMed  Google Scholar 

  • Ortlepp RJ (1938) South African helminths. Pt II. Some taenias from large wild carnivores. Onderstepoort J Vet 10:253–278

    Google Scholar 

  • Oryan A, Nazifi S, Sharifiyazdi H, Ahmadnia S (2010) Pathological, molecular, and biochemical characterization of Coenurus gaigeri in Iranian native goats. J Parasitol 96:961–967

    Article  CAS  PubMed  Google Scholar 

  • Oryan A, Akbari M, Moazeni M, Amrabadi OR (2014) Cerebral and non-cerebral coenurosis in small ruminants. Trop Biomed 31:1–16

    CAS  PubMed  Google Scholar 

  • Popov NP (1937) Cenuroz myshc ovec. Ucennye Zapisi Kazanskogo Gosudarstvennogo Zooveterinarnogo Instituta 47:353–363

    Google Scholar 

  • Rostami S, Beech RN, Salavati R, Baneshi MR, Kamyabi H, Harandi MF (2013) Morphometric analysis of larval rostellar hooks in Taenia multiceps of sheep in Iran and its association with mitochondrial gene variability. Iran J Parasitol 8:579–585

    PubMed  PubMed Central  Google Scholar 

  • Scala A, Varcasia A (2006) Updates on morphobiology, epidemiology and molecular characterization of coenurosis in sheep. Parassitologia 48:61–63

    CAS  PubMed  Google Scholar 

  • Schmidt GD (1970) How to know the tapeworms. WM. C. Brown Company Publishers, Dubuque Iowa, pp 13–15

    Google Scholar 

  • Schuster RK, Sivakumar S, Wieckowsky T (2010) Non-cerebral coenurosis in goats. Parasitol Res 107:721–726

    Article  PubMed  Google Scholar 

  • Schuster RK, Sivakumar S, Wieckowsky T, Reiczigel J (2015) Abattoir survey on extra-cerebral coenurosis in goats. Helminthologia 52:303–309

    Article  Google Scholar 

  • Sharma DK, Chauhan PPS (2006) Coenurosis status in Afro-Asian Region—a review. Small Ruminant Res 64:197–202

    Article  Google Scholar 

  • Smith MC, Sherman DM (2009) Goat medicine, 2nd edn. Ames, IA, Wiley-Blackwell, Oxford, pp 85–256

    Book  Google Scholar 

  • Soulsby EJL (1982) Helminths, arthropods & protozoa of domesticated animals, 7th edn. Bailliére Tindall & Cassell, London, pp 117–119

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson RC (2008) The taxonomy, phylogeny and transmission of Echinococcus. Exp Parasitol 119:439–446

    Article  CAS  PubMed  Google Scholar 

  • Varcasia A, Lightowlers MW, Cattoli G, Cancedda GM, Canu S, Garippa G, Scala A (2006) Genetic variation within Taenia multiceps in Sardinia, Western Mediterranean (Italy). Parasitol Res 99:622–626

    Article  CAS  PubMed  Google Scholar 

  • Varcasia A, Jia WZ, Yanb HB, Manunta ML, Pipia AP, Garippa G, Scala A, Schuster RK (2012) Molecular characterization of subcutaneous and muscular coenurosis of goats in United Arab Emirates. Vet Parasitol 190:604–607

    Article  CAS  PubMed  Google Scholar 

  • Varcasia A, Pipia AP, Arru D, Pes AM, Tamponi C, Dore F, Garippa G, Scala A (2013) Morphological and molecular characterization of bovine coenurosis in Sardinia, Italy. Parasitol Res 112:2079–2082

    Article  CAS  PubMed  Google Scholar 

  • Verster A (1969) A taxonomic revision of the genus Taenia Linnaeus 1758 s. str. Onderstepoort J Vet 36:3–58

    CAS  Google Scholar 

  • von Nickisch-Rosenegk M, Lucius R, Loos-Frank B (1999) Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. J Mol Evol 48:586–596

    Article  Google Scholar 

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Acknowledgments

This work was supported by a research grant awarded to Prof. G. Christodoulopoulos from the Department of Aridland Agriculture of the University of United Arab Emirates; the authors gratefully acknowledge.

Also, the authors acknowledge the help of their colleague Professor Ahmed Kassab for hosting the Egyptian part of their experiment in the facilities of the Department of Anatomy and Embryology of the Faculty of Veterinary Medicine, Benha University (Moshtohor, Toukh 13736, Egypt); this contribution was essential to their study.

The graph of the proglottid (Fig. 1) has been adapted from a pattern of a stained mature proglottid of a taenia derived from a non-cerebral coenurus cyst of a goat. The graph was made by the artist Eunomia Dimitriadi, who is also a veterinarian. The authors would like to express their thanks to Eunomia for this prestigious artwork.

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Authors and Affiliations

  1. Department of Parasitology, University of Hohenheim, Emil-Wolff-Str. 34, 70599, Stuttgart, Germany

    Georgios Christodoulopoulos, Anke Dinkel, Thomas Romig, Dennis Ebi, Ute Mackenstedt & Brigitte Loos-Frank

  2. Clinical Veterinary Medicine Department, School of Veterinary Medicine, University of Thessaly, P.O. Box 199, GR-43100, Karditsa, Greece

    Georgios Christodoulopoulos

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  1. Georgios Christodoulopoulos
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  2. Anke Dinkel
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  6. Brigitte Loos-Frank
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Correspondence to Georgios Christodoulopoulos.

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All investigations complied with the current laws of the countries in which they were performed. All animals were handled by trained and experienced veterinary staff following the recommendations of European Council Directive 86/609/EC for the protection of animals used for experimental purposes.

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The authors declare that they have no conflicts of interest.

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Christodoulopoulos, G., Dinkel, A., Romig, T. et al. Cerebral and non-cerebral coenurosis: on the genotypic and phenotypic diversity of Taenia multiceps . Parasitol Res 115, 4543–4558 (2016). https://doi.org/10.1007/s00436-016-5246-4

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