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Molecular identification of Taenia hydatigena from domestic and free-living animals in Slovakia, Central Europe

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Júlia Halapy Jarošová at Institute of Parasitology of the Slovak Academy of Sciences
Júlia Halapy Jarošová
Daniela Antolová at Slovak Academy of Sciences
Daniela Antolová
Adriana Iglodyova at University of Veterinary Medicine in Košice
Adriana Iglodyova
Alžbeta Königová
Alžbeta Königová
Alžbeta Königová
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Taenia hydatigena is a cosmopolitan tapeworm that uses canids or felines as definitive hosts, while the larval stage (metacestode), formerly referred to as cysticercus tenuicollis, infects a wide variety of intermediate hosts, in particular ruminants. In the present study, we used partial nucleotide sequences of the cox1 and nad1 genes of T. hydatigena from different animal species to analyse the intraspecies genetic diversity of this economically important parasite. Twenty-four samples of metacestodes or adults of T. hydatigena from infected sheep, chamois, roe deer, fallow deer, wild boar, and dogs from Slovakia were collected and further analysed. Several haplotypes of T. hydatigena were identified with unique mutations that have not been previously recorded in Slovakia. Analysis of nucleotide polymorphism revealed the existence of 9 and 13 haplotypes, with relatively low nucleotide pairwise divergence ranging between 0.3–1.3 and 0.2–1.8% for the Hcox and Hnad haplotypes, respectively. In general, low nucleotide and high haplotype diversities in the overall population of T. hydatigena from the study indicate a high number of closely related haplotypes within the explored population; nucleotide diversity per site was low for cox1 (Pi = 0.00540) and slightly higher for nad1 (Pi = 0.00898). A molecular study confirmed the existence of genetic variation within T. hydatigena isolates from Slovakia. However, further investigations with more samples collected from different intermediate and definitive hosts are required in order to investigate the epidemiological significance of the apparent genetic differences observed in this study.
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Vol.:(0123456789)
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https://doi.org/10.1007/s00436-022-07481-z
HELMINTHOLOGY - ORIGINAL PAPER
Molecular identification ofTaenia hydatigena fromdomestic
andfree‑living animals inSlovakia, Central Europe
JúliaJarošová1· DanielaAntolová1· AdrianaIglodyová2· AlžbetaKönigová1· MichaelaUrdaDolinská1·
BronislavaVíchová1
Received: 30 September 2021 / Accepted: 6 March 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022
Abstract
Taenia hydatigena is a cosmopolitan tapeworm that uses canids or felines as definitive hosts, while the larval stage (meta-
cestode), formerly referred to as cysticercus tenuicollis, infects a wide variety of intermediate hosts, in particular ruminants.
In the present study, we used partial nucleotide sequences of the cox1 and nad1 genes of T. hydatigena from different animal
species to analyse the intraspecies genetic diversity of this economically important parasite. Twenty-four samples of meta-
cestodes or adults of T. hydatigena from infected sheep, chamois, roe deer, fallow deer, wild boar, and dogs from Slovakia
were collected and further analysed. Several haplotypes of T. hydatigena were identified with unique mutations that have not
been previously recorded in Slovakia. Analysis of nucleotide polymorphism revealed the existence of 9 and 13 haplotypes,
with relatively low nucleotide pairwise divergence ranging between 0.3–1.3 and 0.2–1.8% for the Hcox and Hnad haplo-
types, respectively. In general, low nucleotide and high haplotype diversities in the overall population of T. hydatigena from
the study indicate a high number of closely related haplotypes within the explored population; nucleotide diversity per site
was low for cox1 (Pi = 0.00540) and slightly higher for nad1 (Pi = 0.00898). A molecular study confirmed the existence of
genetic variation within T. hydatigena isolates from Slovakia. However, further investigations with more samples collected
from different intermediate and definitive hosts are required in order to investigate the epidemiological significance of the
apparent genetic differences observed in this study.
Keywords Taenia hydatigena· Metacestode· Cysticercus tenuicollis· cox1· nad1· Slovakia
Introduction
The cestode T. hydatigena is a cosmopolitan and wide-
spread tapeworm that resides in the small intestine of dogs
and other wild carnivores such as foxes, wolves, jackals,
lynx, raccoons, bears, and cats as definitive hosts. The lar-
val cysticercus appears in the peritoneal cavity of a variety
of intermediate hosts, including horses, small ruminants
(sheep, goats), and less frequently pigs, wild boar, or deer
(Murrell etal. 2005; Muku etal. 2020).
Taenia hydatigena eggs are passed with the faeces of
canids and are accidentally ingested by intermediate hosts
during grazing on contaminated pasture. Subsequently, the
eggs hatch in the small intestine, and the hexacanth embryos
migrate to various organs. Within 7–10days after infec-
tion, the migrating larvae can be found mostly in the liver
parenchyma causing traumatic hepatitis in young animals
(Blažek etal. 1985; Murat 2005). The mature cysticerci are
usually found in the omentum, mesentery, peritoneum, and
visceral surface of the liver and less frequently in the pleura
and pericardium. However, lungs, kidneys, brain, ovaries,
uterus, and uterine tubes have been described as unusual
locations of the T. hydatigena metacestode (Gomez-Puerta
etal. 2015). It has been observed that metacestodes are not
as harmful in the peritoneal space as they are if located in
the liver (Kaufmann 2013).
Studies have demonstrated that cysticercosis caused by
the T. hydatigena metacestode are of veterinary importance,
and infection can cause serious economic losses in livestock
Section Editor: Bruno Gottstein
* Bronislava Víchová
vichova@saske.sk
1 Institute ofParasitology, Slovak Academy ofSciences,
04001Košice, Slovakia
2 University ofVeterinary Medicine andPharmacy inKošice,
04181Košice, Slovakia
/ Published online: 12 March 2022
Parasitology Research (2022) 121:1345–1354
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... T. hydatigena is a widespread cestode that uses canids or felines as definitive hosts, while the larval stage appears in the peritoneal cavity of a wide variety of intermediate hosts, including horses; small ruminants (sheep, goats); and less frequently pigs, wild boar, or deer [61,62]. Eggs of this tapeworm are passed with the faeces of canids and are occasionally ingested by intermediate hosts during grazing on contaminated pasture [63]. Accidentally swallowed eggs from which larvae hatch in the 10 [63]. ...
... Eggs of this tapeworm are passed with the faeces of canids and are occasionally ingested by intermediate hosts during grazing on contaminated pasture [63]. Accidentally swallowed eggs from which larvae hatch in the 10 [63]. The similar structure of the stomach in the chamois and the European bison may also explain the presence of DNA of this helminth in the studied population. ...
Molecular Identification of Selected Cervid Helminths in Supplementarily Fed European Bison Population
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... We identified adult forms of T. hydatigena mainly in wolves and larval stages of the same parasite species in the wild boar, a common prey of wolf packs in Italy. This parasite species has already been reported in wolves from Italy (Gori et al., 2015;Poglayen et al., 2017) and in wild boar from Estonia (Järvis et al., 2007), Slovakia (Jarošová et al., 2022), Poland (Filip et al., 2019), Germany (Barutzki et al., 1991) and Spain (De La Muela et al., 2001). T. hydatigena has been frequently reported in Italian wild boars from central Italy by Di Nicola et al. (2015) and by Paoletti et al. (2019), and in southern Italy by Sgroi et al. (2020). ...
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The recent expansion of the habitat of several wildlife species, comprising anthropized areas, is a relevant risk factor for many zoonotic diseases and should be considered in national and regional sanitary monitoring systems. We evaluated adult intestinal Taenia spp. parasites isolated from wild carnivores and cystic larval forms isolated from wild mammals analysed at the Istituto Zooprofilattico Sperimentale della Lombardia ed Emilia-Romagna (IZSLER) as part of the regional wildlife sanitary surveillance plan. Then, we assessed parasite species through molecular analysis (multiplex PCR followed by ribosomal 12S subunit gene sequencing) in order to update the epidemiological situation on Taeniids infection in the Emilia-Romagna wildlife, reporting the prevalence of each isolated species. The most commonly isolated species was Taenia serialis, which we detected in both wolves and foxes as definitive hosts and in roe deer as intermediate host. More attention on the distribution of Taeniids in wildlife should be paid, considering their potential zoonotic role: several Taenia spp. (Taenia solium, Taenia multiceps, Taenia serialis, Taenia brauni, Taenia glomerulatus) are known for causing coenurosis in humans, with possible severe or fatal outcomes.
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Cestodes in Eurasian wolves (Canis lupus lupus) and domestic dogs (Canis lupus familiaris) in Switzerland
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Molecular characterization of Cysticercus tenuicollis isolates from sheep in the Nile Delta, Egypt and a review on Taenia hydatigena infections worldwide
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The predator–prey-transmitted cestode Taenia hydatigena infects a wide range of definitive and intermediate hosts all over the world. Domestic and sylvatic cycles of transmission are considered as well. The parasite has considerable economic importance, particularly in sheep. Here, the molecular characters of T. hydatigena cysticerci in sheep from the Nile Delta, Egypt were investigated for the first time. For this purpose, 200 sheep carcasses and their offal were inspected at the municipal abattoir, Dakahlia governorate, Egypt. Cysticerci of T. hydatigena were collected and molecularly characterized employing the mitochondrial 12S rRNA gene. Cysticerci were found in 42 (21%) sheep, mostly attached to the omenti, mesenteries and livers. After molecular confirmation, nine isolates were sequenced displaying six different haplotypes. Analysis of the T. hydatigena 12S rRNA nucleotide sequences deposited in GenBank revealed 55 haplotypes out of 69 isolates, displaying high haplotype (0.797) and low nucleotide (0.00739) diversities. For the Tajima D neutrality index, a negative value (−2.702) was determined, indicating the population expansion of the parasite. Additionally, global data summarized in this study should be useful to set up effective control strategies against this ubiquitous parasite.
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Αcute visceral cysticercosis caused by Taenia hydatigena in lambs: ultrasonographic findings
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A new molecular nomenclature for Taenia hydatigena: Mitochondrial DNA sequences reveal sufficient diversity suggesting the assignment of major haplotype divisions
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Cysticercosis caused by the metacestode larval stage of Taenia hydatigena formerly referred to as Cysticercus tenuicollis is a disease of veterinary importance that constitutes a significant threat to livestock production worldwide, especially in endemic regions due to condemnation of visceral organs and mortality rate of infected young animals. While the genetic diversity among parasites is found to be potentially useful in many areas of research including molecular diagnostics, epidemiology and control, that of T. hydatigena across the globe remains poorly understood. In this study, analysis of the mitochondrial DNA (mtDNA) of adult worms and larval stages of T. hydatigena isolated from dogs, sheep, and a wild boar in China showed that the population structure consists of two major haplogroups with very high nucleotide substitutions involving synonymous and non-synonymous changes. Compared with other cestodes such as Echinococcus spp., the genetic variation observed between the haplogroups is sufficient for the assignment of major haplotype or genotype division as both groups showed a total of 166 point-mutation differences between the 12 mitochondrial protein-coding sequences. Preliminary analysis of a nuclear protein-coding gene (pepck) did not reveal any peculiar changes between both groups which suggests that these variants may only differ in their mitochondrial makeup.
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Molecular Identification of Taenia hydatigena from Sheep in Khartoum, Sudan
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The cestode Taenia hydatigena uses canids, primarily dogs, as definitive hosts, while the metacestode larval stage cysticercus infects a range of intermediate hosts, including domestic animals such as goats, sheep, and pigs. Cysticercosis due to T. hydatigena has large veterinary and economic drawbacks. Like other taeniids, e.g., Echinococcus, intraspecific variation is found among the members of the genus Taenia. In Africa, few studies are available on the epidemiology and distribution of T. hydatigena, and even fewer studies are available on its genetic variation. In this study, we molecularly identified 11 cysticerci from sheep in Sudan and demonstrated the genetic variation based on the NADH dehydrogenase subunit 1 (nad1) and cytochrome c oxidase subunit 1 (cox1) mitochondrial genes. The isolates were correctly identified as T. hydatigena with more than 99% similarity to those in the GenBank database. Low diversity indices and insignificant neutrality indices were observed, with 3 and 2 haplotypes for the nad1 and cox1 genes, respectively. The results suggest the presence of unique T. hydatigena haplotypes in Sudan, as haplotypes with 100% similarity were not found in the GenBank database. With few available studies on the genetic variation of T. hydatigena in Africa, this report represents the first insights into the genetic variation of T. hydatigena in Sudan and constitutes useful data.
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Estimation of some biochemical parameters and trace elements in sheep infested with Taenia hydatigena cysts in Sulaymaniyah province/Iraq
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This study was carried out in Sulaymaniyah province, Iraq to estimate the concentration of some biochemical parameters and trace elements in the serum of sheep infected with the metacestodes of Taenia hydatigena. The present study included the measurement of some biochemical parameters as total protein, albumin and globulin and evaluation of trace elements as zinc, copper and iron using automatic analyzer and spectrophotometer respectively. For this purpose, up to 40 serum samples from sheep infected with T. hydatigena cysts and 10 serum samples from non-infected group had been used. The findings of the current study showed significant elevated levels in both total protein and globulin compared to non-infected group, where the total protein and globulin levels were 8.04 ± 0.275 g/dl and 5.90 ± 0.321 g/dl respectively, compared to the non-infected group 6.686 ± 0.409 g/dl and 4.124 ± 0.479 g/dl respectively. While, the mean serum albumin in infected sheep was significantly decreased 2.14 ± 0.224 g/dl compared to non-infected one 2.562 ± 0.152 g/dl. About the results of trace elements, the serum Cu was significantly increased in infected group 1.42 ± 0.466 mg/L compared to non-infected one 0.90 ± 0.171 mg/L, while the mean serum Zn concentration was significantly decreased in infected group 0.37 ± 0.230 mg/L compared to non-infected group 0.70 ± 0.108 mg/L. Although, the mean serum Fe of infected sheep 1.42 ± 0.388 mg/L was slightly lower than non-infected one 1.26 ± 0.490 mg/L, statistically there was no significant difference between them. It was concluded that T. hydatigena cysts had significant effects on serum total protein, globulin, Zn and Cu.
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First molecular description, phylogeny and genetic variation of Taenia hydatigena from Nigerian sheep and goats based on three mitochondrial genes
Article
Full-text available
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Background: Cysticercosis caused by the metacestode larval stage of Taenia hydatigena is a disease of veterinary and economic importance. A considerable level of genetic variation among isolates of different intermediate hosts and locations has been documented. Generally, data on the genetic population structure of T. hydatigena is scanty and lacking in Nigeria. Meanwhile, similar findings in other cestodes like Echinococcus spp. have been found to be of epidemiological importance. Our aim, therefore, was to characterize and compare the genetic diversity of T. hydatigena population in Nigeria based on three mitochondrial DNA markers as well as to assess the phylogenetic relationship with populations from other geographical regions. Methods: In the present study, we described the genetic variation and diversity of T. hydatigena isolates from Nigerian sheep and goats using three full-length mitochondrial genes: the cytochrome c oxidase subunit 1 (cox1), NADH dehydrogenase subunit 1 (nad1), and NADH dehydrogenase subunit 5 (nad5). Results: The median-joining network of concatenated cox1-nad1-nad5 sequences indicated that T. hydatigena metacestodes of sheep origin were genetically distinct from those obtained in goats and this was supported by high FST values of nad1, cox1, and concatenated cox1-nad1-nad5 sequences. Genetic variation was also found to be higher in isolates from goats than from sheep. Conclusions: To the best of our knowledge, the present study described the genetic variation of T. hydatigena population for the first time in Nigeria using full-length mitochondrial genes and suggests the existence of host-specific variants. The population indices of the different DNA markers suggest that analysis of long mitochondrial DNA fragments may provide more information on the molecular ecology of T. hydatigena. We recommend that future studies employ long mitochondrial DNA sequence in order to provide reliable data that would explain the extent of genetic variation in different hosts/locations and the biological and epidemiological significance.
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Massive Taenia hydatigena Cysticercosis in a Wild Boar (Sus scrofa) from Italy
Article
Full-text available
  • Aug 2019
Purpose Taenia hydatigena cysticercosis, due to Cysticercus tenuicollis, is a parasitic disease infecting domestic and wild animals worldwide causing economic and productive losses. Nonetheless, little attention has been paid to the role of the wild ungulates in the epidemiology of this disease. In the last years, the increasing population of wild boars in Europe has raised the attention of researchers on their role in the spreading of several infections, including those caused by cestodes. Herein, we report the description of a massive infection due to T. hydatigena cysticercosis in a wild boar from southern Italy. Methods An adult female boar was examined during the hunting season 2018 within the regional project “Piano Emergenza Cinghiali in Campania”. A complete necropsy was performed on the boar carcass and all viscera were examined to determine number and location of the cysts. Morphological and molecular analyses of the cysts were performed to confirm the C. tenuicollis identity. Results The boar examined has revealed an impressive massive infection with 265 cysts. Measurements of the large and small larval hooks showed a mean of length as 200.3 µm and 136.8 µm, respectively. Molecular analysis of Cox1 and ND1 mitochondrial genes confirmed the C. tenuicollis identity. Conclusions Our findings suggest that wild boar could be involved in the epidemiology of T. hydatigena, due to the significant amount of boar raw offal available to definitive hosts (i.e., hunting dogs, foxes and wolves), during the hunting seasons.
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Identification of Tapeworm Species in Genetically Characterised Grey Wolves Recolonising Central Europe
Article
  • Feb 2021
PurposeRestored role of the grey wolf in ecological networks of newly recolonized areas can be studied via surveys of parasite communities of this predator. As helminths circulating in multi-host systems, the tapeworms directly reflect wolves’ diet, while some species are also important from the One Health perspective. The Czech experienced centuries of wolves’ absence, however, now it is situated on the crossroad of recolonising wolves’ populations, which is opening questions of their role in ecological networks in this area and thus in sylvatic cycles of heteroxenous parasites.Methods Five wolf carcasses from this area were obtained and genetic affinity to a particular population was inspected. Tapeworms isolated from wolves’ intestines during necropsies were molecularly identified based on sequences of COI marker.ResultsThree wolf haplotypes (w1, w2, w14) correspond with the dominance of haplogroup 1 (w1, w2) within Central European lowland population and haplogroup 2 (w14) within the Carpathian population. Two Taenia spp. were revealed: T. krabbei in Central European population wolves and T. hydatigena in an individual from Carpathian population.Conclusions The results serve as a base for future monitoring and studies of the recolonising wolf population and its impact on ecosystems in the studied area to contribute to the hypothesis about differentiation of parasite communities in particular wolf population and higher parasite diversity and richness in established populations in comparison to newly settled ones.
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Preliminary information on the prevalence and molecular description of Taenia hydatigena isolates in Pakistan based on mitochondrial cox1 gene
Article
  • Jul 2020
  • INFECT GENET EVOL
Taenia hydatigena is a cestode of veterinary importance. Infection with the metacestode larval stage results in cysticercosis, which poses a serious challenge to the livestock industry worldwide. Globally, there are numerous reports on cysticercosis caused by T. hydatigena in sheep and goat but a lack of data on the prevalence and genetic diversity exists for Pakistan. We designed this study to provide an insight into the disease status as well as investigate the genetic variation among the recovered isolates based on the mitochondrial cox1 gene. In this study, we examined small ruminants (sheep and goats) slaughtered in Faisalabad in eastern Punjab province of Pakistan for T. hydatigena metacestodes and described the population structure and genetic variation using the cytochrome c oxidase subunit 1 (cox1) mitochondrial gene. Overall, a prevalence of 4.40% (goat =4.67% sheep = 4.07%) from a total of 2225 small ruminant carcasses (sheep = 983, goats = 1242) was observed. Based on the NCBI BLAST search and Bayesian phylogeny, the identity of all isolates was confirmed via their nucleotide sequences. The diversity indices indicated a high haplotype and a low nucleotide diversity with 43 haplotypes from 98 isolates. The results also show the existence of unique haplotypes of T. hydatigena in Pakistan as demonstrated by the significant negative values of Tajima's D and Fu's Fs neutrality test suggesting a recent population expansion. The median-joining network of the partial cox1 sequence dataset showed the existence of two main haplotypes detected in both sheep and goat populations. This study shows that the prevalence of cycticercosis due to T. hydatigena is below 5% in sheep and goats in Faisalabad, Punjab, Pakistan. The molecular analysis of the partial cox1 gene also indicates a high degree of genetic variation with the existence of rare haplotypes. These findings represent a preliminary report on the prevalence and genetic variation of T. hydatigena in Pakistan and serve as baseline information for future studies on the prevalence and population structure of T. hydatigena in the country.
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Molecular and Morphological Characterization of Cysticercus tenuicollis in Red Deer (Cervus elaphus) from Turkey
Article
  • Jun 2019
Introduction Cysticercus tenuicollis, the metacestode stage of Taenia hydatigena has a worldwide distribution and is particularly common in rural areas and developing countries. In rare cases, T. hydatigena infection may result in the death of its host due to severe damage or secondary bacterial infections. Generally, when multiple cysts are attached to the liver, it causes economic losses. The infection can be detected using morphological, histopathological and more recently, molecular investigations. Methods In the present study, we describe molecular and morphological characterization of C. tenuicollis detected in a 3 month-old female red deer (Cervus elaphus) during necropsy. Cystic samples were stained with haematoxylin–eosin (HE) and Masson’s trichrome stain for histopathological examination, and molecular characterization of the complete mitochondrial cytochrome c oxidase subunit 1 (cox1) gene region was performed. Purpose This study provides the first morphological, histopathological, and molecular data on C. tenuicollis isolated from red deer in Turkey.
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