Genetic characterisation of Echinococcus granulosus sensu lato infecting ruminants in the Republic of North Macedonia L.

PDF (English)
Publicado: Dec 18, 2025
DOI: https://doi.org/10.12681/jhvms.40892
L Rashikj
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0000-0002-9617-5811
J Stefanovska
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0000-0003-1598-7146
I Djadjovski
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
Z Popova Hristovska
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0009-0007-0521-7603
B Xhekaj
Faculty of Agriculture and Veterinary, University of Prishtina, Prishtina, Kosovo
https://orcid.org/0000-0003-2757-0591
A Trajchovski
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0000-0002-9891-6345
B Chapkunovska
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0009-0005-2533-5768
M Jurhar Pavlova
Faculty of Medicine, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia ABSTRACT:
https://orcid.org/0009-0003-9557-1454
A Cvetkovikj
Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Skopje, Republic of North Macedonia
https://orcid.org/0000-0002-6582-7020
Resumen

This study aimed to characterize Echinococcus genotypes infecting ruminants in North Macedonia and estimate their epidemiological significance and possible public health implications. Samples from 69 ruminants were collected between 2021 and 2022, with one cyst per animal analyzed for genetic diversity through amplification and sequencing of the cytochrome c oxidase 1 (cox1) mitochondrial gene. Using the neighbor-joining method, phylogenetic analysis of the sequenced data was performed using MAFFT for sequence alignment, trimming, and tree construction with MEGAX. Phylogenetic analysis identified two major genotypes: G1 and G3. Among the samples, 38/61 sheep (62.3%) were G1, and 23/61 sheep (37.7%) were G3. Both G1 and G3 genotypes were detected in 4/8 isolates (50%) in cattle. This study provides the first molecular characterization of Echinococcus granulosus (s.s.) genotypes (G1 and G3) in North Macedonian ruminants. The predominance of these highly zoonotic genotypes highlights significant public health risks and underscores the urgent need for integrated surveillance programs targeting both animal and human populations. These findings provide essential baseline data for implementing targeted control strategies in this endemic region.

Article Details
  • Sección
  • Research Articles
Creative Commons License

Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial 4.0.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Descargas
Los datos de descargas todavía no están disponibles.
Biografía del autor/a
B Xhekaj, Faculty of Agriculture and Veterinary, University of Prishtina, Prishtina, Kosovo

Betim's affiliation is: Faculty of Agriculture and Veterinary, University of Prishtina, Prishtina, Kosovo

Kosovo is not in the list of countries and can't be selected.

Citas
Alvarez Rojas CA, Mathis A, Deplazes P (2018) Assessing the contamination
of food and the environment with Taenia and Echinococcus
eggs and their zoonotic transmission. Curr Clin Microbiol Rep
:154–163.
Bart JM, Morariu S, Knapp J, Ilie MS, Pitulescu M, Anghel A, et al.
(2006) Genetic typing of Echinococcus granulosus in Romania.
Parasitol Res 98(2):130–137.
Bosco A, Alves LC, Cociancic P, Amadesi A, Pepe P, Morgoglione ME,
et al (2021) Epidemiology and spatial distribution of Echinococcus
granulosus in sheep and goats slaughtered in a hyperendemic
European Mediterranean area. Parasit Vectors 14(1):421. Bonelli
P, Loi F, Cancedda MG, Peruzzu A, Antuofermo E, Pintore E, et al
(2020) Bayesian analysis of three methods for diagnosis of cystic
echinococcosis in sheep. Pathogens 9(10):1–9.
Bonelli P, Serra E, Dei Giudici S, Peruzzu A, Crotti S, Danesi P, et al
(2024) Molecular phylogenetic analysis of Echinococcus granulosus
sensu lato infecting sheep in Italy. Acta Trop 252:105782.
Breyer I, Georgieva D, Kurdova R, Gottstein B (2004) Echinococcus
granulosus strain typing in Bulgaria: The G1 genotype is predominant
in intermediate and definitive wild hosts. Parasitol Res
(2):127–130.
Budke CM, Casulli A, Kern P, Vuitton DA (2017) Cystic and alveolar
echinococcosis: Successes and continuing challenges. PLoS Negl
Trop Dis 11(4):e0005363.
Casulli A, Siles-Lucas M, Tamarozzi F (2019) Echinococcus granulosus
sensu lato. Trends Parasitol 35(8):663–664.
Casulli A, Massolo A, Saarma U, Umhang G, Santolamazza F, Santoro
A (2022) Species and genotypes belonging to Echinococcus
granulosus sensu lato complex causing human cystic echinococcosis
in Europe (2000–2021): A systematic review. Parasit Vectors
(1):109. Chaligiannis I, Maillard S, Boubaker G, Spiliotis M,
Saratsis A, Gottstein B, et al (2015) Echinococcus granulosus infection
dynamics in livestock of Greece. Acta Trop 150:64–70.
Cucher MA, Macchiaroli N, Baldi G, Camicia F, Prada L, Maldonado
L, et al (2016) Cystic echinococcosis in South America: Systematic
review of species and genotypes of Echinococcus granulosus sensu
lato in humans and natural domestic hosts. Trop Med Int Health
(2):166– 175.
Dărăbuș G, Bușe A, Oprescu I, Morariu S, Mederle N, Ilie M, et al
(2022) Investigation on descriptive epidemiology, geographical
distribution, and genotyping of Echinococcus granulosus s.l. in
bovine from Romania. Vet Sci 9(12):678.
Debeljak Z, Boufana B, Interisano M, Vidanovic D, Kulisic Z, Casulli
A (2016) First insights into the genetic diversity of Echinococcus
granulosus sensu stricto (s.s.) in Serbia. Vet Parasitol 223:57–62.
Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF,
Romig T, et al (2017) Global distribution of alveolar and cystic
echinococcosis. Adv Parasitol 95:315–493.
Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, World Health Organization
(2001) WHO/OIE manual on echinococcosis in humans
and animals: A public health problem of global concern. World
Organisation for Animal Health. Accessed March 2021.
Espinoza S, Salas AM, Vargas A, Freire V, Diaz E, Sánchez G, et al.
(2014) Detection of the G3 genotype of Echinococcus granulosus
from hydatid cysts of Chilean cattle using COX1 and ND1 mitochondrial
markers. Parasitol Res 113(1):139–147.
Felsenstein J (1985) Confidence limits on phylogenies: An approach
using the bootstrap. Evolution (N Y) 39(4):783–791.
Haleem S, Niaz S, Qureshi NA, Ullah R, Alsaid MS, Alqahtani AS,
et al (2018) Incidence, risk factors, and epidemiology of cystic
echinococcosis: A complex socioecological emerging infectious
disease in Khyber Pakhtunkhwa, province of Pakistan. Biomed
Res Int. 5042430:15.
Hodžić A, Alić A, Spahić A, Harl J, Beck R (2022) Genetic diversity
of Echinococcus granulosus sensu lato from animals and humans
in Bosnia and Herzegovina. Parasit Vectors 15(1).
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Mammalian
Protein Metabolism. Elsevier, pp 21–132.
Jesudoss Chelladurai JRJ, Quintana TA, Johnson WL, Schmidt C, Righter
D, Howey E (2024) Cystic echinococcosis in cattle and sheep
caused by Echinococcus granulosus sensu stricto genotypes G1
and G3 in the USA. Parasit Vectors 17(1):128.
Khan S, Cable J, Masud N, Hailer F, Younus M, Hussain N, et al (2025)
Epidemiological and genotypic assessment of cystic echinococcosis
in ruminant populations of Northern Punjab, Pakistan: A neglected
zoonotic disease. Parasitol Res 124(1):7.
Kinkar L, Laurimäe T, Sharbatkhori M, Mirhendi H, Kia EB, Ponce-Gordo
F, et al. (2017) New mitogenome and nuclear evidence on the
phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus
granulosus sensu stricto. Infect Genet Evol 52:52–58.
Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli
A, et al. (2018a) Distinguishing Echinococcus granulosus sensu
stricto genotypes G1 and G3 with confidence: A practical guide.
Infect Genet Evol 64:178–184.
Kinkar L, Laurimäe T, Acosta-Jamett G, Andresiuk V, Balkaya I, Casulli
A, et al. (2018b) Global phylogeography and genetic diversity of the
zoonotic tapeworm Echinococcus granulosus sensu stricto genotype
G1. Int J Parasitol 48(9):729–742.
Kinkar L, Laurimäe T, Balkaya I, Casulli A, Zait H, Irshadullah M, et
al. (2018c) Genetic diversity and phylogeography of the elusive,
but epidemiologically important Echinococcus granulosus sensu
stricto genotype G3. Parasitol 145(12):1613–1622.
Küçükyağlıoğlu A, Uslu U (2022) Prevalence and economic significance
of hidatidosis in cattle slaughtered at an abattoir in Konya, Turkey.
Turkiye Parazitoloji Dergisi 46(3):207–212.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular
evolutionary genetics analysis across computing platforms.
Mol Biol Evol 35(6):1547–1549.
Larrieu E, Gavidia CM, Lightowlers MW (2019) Control of cystic
echinococcosis: Background and prospects. Zoonoses Public Health
:889–899.
Nakao M, Yanagida T, Okamoto M, Knapp J, Nkouawa A, Sako Y, et
al. (2010) State-of-theart Echinococcus and Taenia: Phylogenetic
taxonomy of human-pathogenic tapeworms and its application to
molecular diagnosis. Infect Genet Evol 10(4):444–452.
Nungari L, Mbae C, Gikunju J, Mulinge E, Kaburu T, Zeyhle E,
Magambo J. (2019) Prevalence and genotyping of Echinococcus
species from livestock in Kajiado County, Kenya. Biomed Res Int
:4798906.
Oudni-M’rad M, M’rad S, Ksia A, Lamiri R, Mekki M, Nouri A, et
al. (2016) First molecular evidence of the simultaneous human
infection with two species of Echinococcus granulosus sensu lato:
Echinococcus granulosus sensu stricto and Echinococcus canadensis.
Parasitol Res 115:1065–1069.
Raissi V, Etemadi S, Sohrabi N, Raiesi O, Shahraki M, Salimi-Khorashad
A, et al. (2021) Molecular characterization and phylogeny of Taenia hydatigena and Echinococcus granulosus from Iranian sheep
and cattle based on COX1 gene. Curr Microbiol 78(4):1202–1207.
Roinioti E, Papathanassopoulou A, Theodoropoulou I, Simsek S,
Theodoropoulos G (2016) Molecular identification of Echinococcus
granulosus isolates from ruminants in Greece. Vet Parasitol
:138–144.
Romig T, Ebi D, Wassermann M (2015) Taxonomy and molecular epidemiology
of Echinococcus granulosus sensu lato. Vet Parasitol
(3–4):76–84.
Rashikj L, Cvetkovikj A, Nikolovski M, Cvetkovikj I, Stefanovska J
(2022) Cystic echinococcosis in slaughtered cattle and sheep from
Republic of North Macedonia. Mac Vet Rev 45(1):35–41.
Saitou N, Nei M (1987) The neighbor-joining method: A new method
for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425.
Thompson RC (2017) Biology and systematics of Echinococcus. Adv
Parasitol 95:65–109. Thompson RC (2020) The molecular epidemiology
of Echinococcus infections. Pathogens 9:1–9.
Torgerson PR, Budke CM (2003) Echinococcosis – an international
public health challenge. Res Vet Sci 74(3):191–202.
Umhang G, Richomme C, Bastid V, Boucher JM, Peytavin De Garam C,
Itié-Hafez S, et al (2020) National survey and molecular diagnosis
of Echinococcus granulosus sensu lato in livestock in France, 2012.
Parasitology 147(6):667–672.