Molecular Characterization of Echinococcus granulosus Isolated from Clinical Samples of Patients Diagnosed with Hydatid Cysts in Eastern Türkiye
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Abstract
Background: We aimed to investigate the genetic diversity and population structure of Echinococcus granulosususing various cyst materials fromtheparasiteobtained from humansineastern Türkiye.
Methods: We used cyst samples from 61 patients diagnosed with hydatid cysts by the Department of Thoracic Surgery and Department of Radiology at Atatürk University Faculty of Medicine between 2019 and 2023. Microscopic examination of protoscolex in cyst samples was performed, and, if available, the patients' ELISA IgG results were obtained from the hospital automation system. Two primer pairs revealed DNA regions specific to E. granulosus (12S rRNA and mt-COX1). Sequence analysis was performed on samples found positive for mt-COX1 PCR, and a phylogenetic tree was constructed from the resulting data.
Results: The rate of scolex in microscopic examination was 31/61 (50.8%), and the ELISA IgG positivity rate was 36/51 (70.6%). As a result of PCR analysis of 12S rRNA and mt-COX1 gene regions of 61 cyst samples, positivity was determined in 48 (78.7%) samples. As a result of PCR product sequence analysis, it was found that all samples were of the E. granulosus sensu stricto (G1, G3) genotype. Lung cyst alone was detected in 25 (40.9%) cases, while only liver cyst was detected in 15 (24.6%) cases. In 13 (21.3) cases, cysts were present in both the lungs and the liver.
Conclusion: The genotype of E. granulosus isolates obtained from cyst material from patients diagnosed with hydatid cysts in Erzurum and surrounding provinces was a domestic sheep strain (G1, G3).
1. Woolsey ID, Miller AL. Echinococcus granulosus sensu lato and Echinococcus multilocularis: A review. Res Vet Sci. 2021; 135: 517-522.
2. Sarkari B, Rezaei Z. Immunodiagnosis of human hydatid disease: Where do we stand? World J Methodol. 2015; 5 (4): 185-95.
3. Deplazes P, Rinaldi L, Rojas CA, et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol. 2017; 95: 315–493.
4. Kurt A, Avcioglu H, Guven E, et al. Molecular characterisation of Echinococcus multilocularis and Echinococcus granulosus from cysts and formalin-fixed paraffin-embedded tissue samples of human isolates in northeastern Turkey. Vector Borne Zoonotic Dis. 2020;20 (8); 593-602.
5. Yağmur Y, Akbulut S. Epidemiology of Hidatid Disease. Turkiye Klinikleri J Gen Surg-Special Topics. 2010; 3(2): 6-8.
6. Romig T, Ebi D, Wassermann M. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol. 2015;213(3-4): 76-84.
7. Siles-Lucas M, Casulli A, Conraths F, et al. Laboratory diagnosis of Echinococcus spp. in human patients and infected animals. Adv Parasitol. 2017; 96: 159-257,
8. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al. Serological diagnosis and follow-up of human cystic echinococcosis: a new hope for the future? Biomed Res Int. 2015;1: 428205.
9. Lissandrin R, Tamarozzi F, Piccoli L, et al. Factors influencing the serological response in hepatic Echinococcus granulosus infection. Am J Trop Med Hyg. 2016; 94(1): 166-71.
10. Akkaş Ö, Özgökçe M, Aydemir S, et al. (2023). Genotyping of Echinococcus granulosus human isolates obtained from the puncture, aspiration, injection, and re-aspiration (PAIR) process in Türkiye. Iran J Parasitol. 2023;18(4): 427-434.
11. Dinkel A, Njoroge EM, Zimmermann A, et al. A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, concerning the epidemiological situation in eastern Africa. Int J Parasitol. 2004;34(5): 645-53.
12. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992; 54(2): 165-73.
13. Tamarozzi F, Mariconti M, Covini I, et al. [Rapid diagnostic tests for the serodiagnosis of human cystic echinococcosis]. Bull Soc Pathol Exot. 2017; 110(1): 20-30. [Article in French].
14. Kinkar L, Laurimäe T, Acosta-Jamett G, et al. Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. Int J Parasitol. 2018; 48(9-10): 729-742.
15. Demirci E, Altun E, Çalik M, et al. [Hydatid cyst cases with different localisation: Region of Erzurum]. Türkiye Parazitol. Derg. 2015; 39(2): 103-7.
16. Aslan MH, Kurt A, Vural MK. Investigation of Indirect Hemagglutination (IHA) test results in a patient with early diagnosis of Cystic Echinococcosis. Van Medical Journal. 2019; 26(2): 158-161.
17. Aydın Y, Altuntaş B, Eroğlu A, et al. Treatment approach for pulmonary alveolar echinococcosis. Türk Gögüs Kalp Dama. 2017; 25(2): 223-229.
18. Manterola C, Vial M, Melo A, et al. Viability and fertility of human hepatic hydatid cysts. World J Surg. 2006;30: 227-232.
19. Thompson R. Biology and systematics of Echinococcus. Adv Parasitol. 2017;95 : 65-109,
20. Cucher MA, Macchiaroli N, Baldi G, et al. 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. 2016; 21(2): 166-75.
21. Rostami S, Torbaghan SS, Dabiri S, et al. Genetic characterisation of Echinococcus granulosus from a large number of formalin-fixed, paraffin-embedded tissue samples of human isolates in Iran. Am J Trop Med Hyg. 2015; 92(3): 588-94.
22. Alvi MA, Ohiolei JA, Saqib M, et al. Echinococcus granulosus (sensu stricto)(G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA. Parasite Vectors. 2020; 13(1):347.
23. Pednekar RP, Gatne ML, Thompson RA, et al. Molecular and morphological characterisation of Echinococcus from food-producing animals in India. Vet Parasitol. 2009;165 (1-2): 58-65.
24. Casulli A, Massolo A, Saarma U, et al. Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000–2021): a systematic review. Parasite Vectors. 2022; 15(1):109.
25. Kargar S, Dalimi A, Eslami G, et al. "Cystic Echinococcosis in Central Iran: G1 and G6 genotypes in patients. Surg Infect (Larchmt). 2022; 23 (5): 451-457.
26. Erdoğan E, Ozkan B, Mutlu F, et al. [Molecular characterisation of Echinococcus granulosus isolates obtained from different hosts]. Mikrobiyol Bul. 2017; 51(1): 79-86.
27. Orsten S, Boufana B, Ciftci T, et al. Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitol Res. 2018; 117: 1257-1263.
28. Hamamcı B, Açıkgöz G, Çetinkaya Ü, et al. Molecular genotyping of Echinococcus granulosus sensu stricto from human Echinococcal cysts in Hatay, Türkiye. Exp Parasitol. 2023; 245:108454.
29. Santucciu C, Bonelli P, Peruzzi A, et al. Genetic Characterisation of Echinococcus granulosus Sensu Stricto Isolated from Human Cysts from Sardinia, Italy. Diseases. 2023; 11(3): 91.
30. Khan A, Naz K, Ahmed H, et al. Knowledge, attitudes and practices related to cystic echinococcosis endemicity in Pakistan. Infect Dis Poverty. 2018; 7(1):4.
31. Hallaç Keser S, Selek A, Ece D, et al. Review of hydatid cyst with a focus on cases with unusual locations. Turk Patoloji Derg. 2017;33(1): 30-36.
2. Sarkari B, Rezaei Z. Immunodiagnosis of human hydatid disease: Where do we stand? World J Methodol. 2015; 5 (4): 185-95.
3. Deplazes P, Rinaldi L, Rojas CA, et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol. 2017; 95: 315–493.
4. Kurt A, Avcioglu H, Guven E, et al. Molecular characterisation of Echinococcus multilocularis and Echinococcus granulosus from cysts and formalin-fixed paraffin-embedded tissue samples of human isolates in northeastern Turkey. Vector Borne Zoonotic Dis. 2020;20 (8); 593-602.
5. Yağmur Y, Akbulut S. Epidemiology of Hidatid Disease. Turkiye Klinikleri J Gen Surg-Special Topics. 2010; 3(2): 6-8.
6. Romig T, Ebi D, Wassermann M. Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Vet Parasitol. 2015;213(3-4): 76-84.
7. Siles-Lucas M, Casulli A, Conraths F, et al. Laboratory diagnosis of Echinococcus spp. in human patients and infected animals. Adv Parasitol. 2017; 96: 159-257,
8. Manzano-Román R, Sánchez-Ovejero C, Hernández-González A, et al. Serological diagnosis and follow-up of human cystic echinococcosis: a new hope for the future? Biomed Res Int. 2015;1: 428205.
9. Lissandrin R, Tamarozzi F, Piccoli L, et al. Factors influencing the serological response in hepatic Echinococcus granulosus infection. Am J Trop Med Hyg. 2016; 94(1): 166-71.
10. Akkaş Ö, Özgökçe M, Aydemir S, et al. (2023). Genotyping of Echinococcus granulosus human isolates obtained from the puncture, aspiration, injection, and re-aspiration (PAIR) process in Türkiye. Iran J Parasitol. 2023;18(4): 427-434.
11. Dinkel A, Njoroge EM, Zimmermann A, et al. A PCR system for detection of species and genotypes of the Echinococcus granulosus-complex, concerning the epidemiological situation in eastern Africa. Int J Parasitol. 2004;34(5): 645-53.
12. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992; 54(2): 165-73.
13. Tamarozzi F, Mariconti M, Covini I, et al. [Rapid diagnostic tests for the serodiagnosis of human cystic echinococcosis]. Bull Soc Pathol Exot. 2017; 110(1): 20-30. [Article in French].
14. Kinkar L, Laurimäe T, Acosta-Jamett G, et al. Global phylogeography and genetic diversity of the zoonotic tapeworm Echinococcus granulosus sensu stricto genotype G1. Int J Parasitol. 2018; 48(9-10): 729-742.
15. Demirci E, Altun E, Çalik M, et al. [Hydatid cyst cases with different localisation: Region of Erzurum]. Türkiye Parazitol. Derg. 2015; 39(2): 103-7.
16. Aslan MH, Kurt A, Vural MK. Investigation of Indirect Hemagglutination (IHA) test results in a patient with early diagnosis of Cystic Echinococcosis. Van Medical Journal. 2019; 26(2): 158-161.
17. Aydın Y, Altuntaş B, Eroğlu A, et al. Treatment approach for pulmonary alveolar echinococcosis. Türk Gögüs Kalp Dama. 2017; 25(2): 223-229.
18. Manterola C, Vial M, Melo A, et al. Viability and fertility of human hepatic hydatid cysts. World J Surg. 2006;30: 227-232.
19. Thompson R. Biology and systematics of Echinococcus. Adv Parasitol. 2017;95 : 65-109,
20. Cucher MA, Macchiaroli N, Baldi G, et al. 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. 2016; 21(2): 166-75.
21. Rostami S, Torbaghan SS, Dabiri S, et al. Genetic characterisation of Echinococcus granulosus from a large number of formalin-fixed, paraffin-embedded tissue samples of human isolates in Iran. Am J Trop Med Hyg. 2015; 92(3): 588-94.
22. Alvi MA, Ohiolei JA, Saqib M, et al. Echinococcus granulosus (sensu stricto)(G1, G3) and E. ortleppi (G5) in Pakistan: phylogeny, genetic diversity and population structural analysis based on mitochondrial DNA. Parasite Vectors. 2020; 13(1):347.
23. Pednekar RP, Gatne ML, Thompson RA, et al. Molecular and morphological characterisation of Echinococcus from food-producing animals in India. Vet Parasitol. 2009;165 (1-2): 58-65.
24. Casulli A, Massolo A, Saarma U, et al. Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000–2021): a systematic review. Parasite Vectors. 2022; 15(1):109.
25. Kargar S, Dalimi A, Eslami G, et al. "Cystic Echinococcosis in Central Iran: G1 and G6 genotypes in patients. Surg Infect (Larchmt). 2022; 23 (5): 451-457.
26. Erdoğan E, Ozkan B, Mutlu F, et al. [Molecular characterisation of Echinococcus granulosus isolates obtained from different hosts]. Mikrobiyol Bul. 2017; 51(1): 79-86.
27. Orsten S, Boufana B, Ciftci T, et al. Human cystic echinococcosis in Turkey: a preliminary study on DNA polymorphisms of hydatid cysts removed from confirmed patients. Parasitol Res. 2018; 117: 1257-1263.
28. Hamamcı B, Açıkgöz G, Çetinkaya Ü, et al. Molecular genotyping of Echinococcus granulosus sensu stricto from human Echinococcal cysts in Hatay, Türkiye. Exp Parasitol. 2023; 245:108454.
29. Santucciu C, Bonelli P, Peruzzi A, et al. Genetic Characterisation of Echinococcus granulosus Sensu Stricto Isolated from Human Cysts from Sardinia, Italy. Diseases. 2023; 11(3): 91.
30. Khan A, Naz K, Ahmed H, et al. Knowledge, attitudes and practices related to cystic echinococcosis endemicity in Pakistan. Infect Dis Poverty. 2018; 7(1):4.
31. Hallaç Keser S, Selek A, Ece D, et al. Review of hydatid cyst with a focus on cases with unusual locations. Turk Patoloji Derg. 2017;33(1): 30-36.
| Files | ||
| Issue | Vol 20 No 4 (2025) | |
| Section | Original Article(s) | |
| Keywords | ||
| Echinococcus granulosus Hydatid cyst Genotype mt-Cox1 Phylogenesis | ||
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How to Cite
1.
Yılmaz A, Aydın H, Akkaş Önder, Aydın Y, Eren S, Uslu H. Molecular Characterization of Echinococcus granulosus Isolated from Clinical Samples of Patients Diagnosed with Hydatid Cysts in Eastern Türkiye. Iran J Parasitol. 2025;20(4):534-543.
