Molecular Characterization of Echinococcus granulosus in South of Iran

Saeid Hosseinzadeh, Mehdi Fazeli, Arsalan Hosseini, Seyed Shahram Shekarforoush

Department of Basic Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.
Department of Food Hygiene, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.
Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran.

DOI: 10.4236/ojvm.2012.24032                

Abstract

The focus of present study was to determine the epidemiological and molecular aspects of different strains of cystic echinococcosis in Fars province, Iran. Liver and lung samples from 410 sheep, 206 goats and 315 cattle were collected. In cattle, the infestation rate was 18.1% (57/315), with 11.1% hepatic cysts and 7.0% pulmonary cysts. Out of all identified cysts, 31.4% of the hepatic and 31.8% of the pulmonary cysts were found fertile. Incidence rate of hydatid cyst infection in sheep was 15.5% (64/410) with 11.9% hepatic cysts and 3.6% pulmonary cysts, of which 24.5% and 20% of hepatic and pulmonary cysts were respectively identified as fertile. The infestation rate was 16.0% (33/206) in goat, in which 10.2% and 5.8% cysts were collected from liver and lung, correspondingly. The prevalence of fertile hepatic and pulmonary cysts was recorded as 23.8% and 16.7%, respectively. Genotyping the cystic materials using PCR showed that the most prominent strains responsible for cystic echinococcosis in the Fars province are G1 and G6/7, while no evidence of E. multilocularis was recorded. This information may give us some clues to find out more about strains distribution in different regions in Iran, which may finally use to find tools in the eradication program of the disease, here and elsewhere.

Keywords

Hydatid Cyst; PCR; Echinococcus; Epidemiology

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. Euzeby, “The Epidemiology of Hydatidosis with Special Reference to the Mediterranean Area,” Parassitologia, Vol. 33, No. 1, 1991, pp. 25-39.
[2]	P. Schantz, “Echinococcus granulosus, E. multilocularis and E. vogli (Agents of Cystic, Alveolar, Polycystic Echinococcosis),” In: S. S. Long and C. G. Prober, Eds., Pediatrics Infectious Diseases, Churchill Livingstone, New York, 1997, pp. 1488-1492.
[3]	R. C. A. Thompson, “Echinococcosis,” In: S. H. Gillespie and R. Pearson, Eds., Principles and Practice of Clinical Parasitolog, Wiley, Sussex, 2001, pp. 595-612.
[4]	I. Mobedi, H. Madadi and F. Arfaa, “Camel ‘Camelus dromedarius’ Intermediate Host of Echinococcus granulosus in Iran,” The Journal of Parasitology, Vol. 56, No. 6, 1970, pp. 1255-1259. doi:10.2307/3277581
[5]	N. Moghaddar, A. Oryan and M. R. Hanifpour, “Helminthes Recovered from the Liver and Lungs Camel with Special Reference to Their Incidence and Pathogenesis in Shiraz, Islamic Republic of Iran,” The Indian Journal of Animal, Vol. 62, No. 11, 1992, pp. 1018-1023.
[6]	A. Oryan, N. Moghadar and S. N. S. Gaur, “Metacestodes of Sheep with Special Reference to Their Epidemiological Status, Pathogenesis and Economic Implications in Fars Province, Iran,” Veterinary Parasitology, Vol. 51, No. 3, 1994, pp. 231-240. doi:10.1016/0304-4017(94)90160-0
[7]	Hosseini S.H. and A. Eslami, “Morphological and Developmental Characteristics of Echinococcus granulosus Derived from Sheep, Cattle and Camels in Iran,” Journal of Helminthology, Vol. 72, No. 4, 1998, pp. 337-341. doi:10.1017/S0022149X00016709
[8]	D. Mehrabani, A. Oryan and S. M. Sadjjadi, “Prevalence of Echinococcus granulosus Infection in Stray Dogs and Herbivores in Shiraz, Iran,” Veterinary Parasitology, Vol. 86, No. 3, 1999, pp. 217-220. doi:10.1016/S0304-4017(99)00151-X
[9]	A. Dalimi, G. H. Motamedi, M. Hosseini, B. Mohammadian, H. Malaki, Z. Ghamari and F. Ghaffari-far, “Echinococcosis/hydatidosis in Western Iran,” Veterinary Parasitology, Vol. 105, No. 2, 2002, pp. 161-171. doi:10.1016/S0304-4017(02)00005-5
[10]	N. A. Ahmadi, “Hydatidosis in Camels (Camelus dromedarius) and Their Potential Role in the Epidemiology of Echinococcus granulosus in Iran,” Journal of Helminthology, Vol. 79, No. 2, 2005, pp. 119-125. doi:10.1079/JOH2005279
[11]	B. Bastani and F. Dehdashti, “Hepatic Hydatid Disease in Iran, with Review of the Literature,” Mount Sinai Journal, Vol. 62, No. 2, 1995, pp. 62-69.
[12]	N. A. Ahmadi and A. Dalimi, “Characterization of Echinococcus granulosus Isolates from Human, Sheep and Camel in Iran,” Infection, Genetics and Evolution, Vol. 6, No. 2, 2006, pp. 85-90. doi:10.1016/j.meegid.2005.01.005
[13]	L. A. E. Zhang, S. H. Hosseini and D. P. McManus, “Indication of the Presence of Two Distinct Strains of Echinococcus granulosus in Iran by Mitochondrial DNA Markers,” The American Journal of Tropical Medicine and Hygiene, Vol. 59, No. 1, 1998, pp. 171-174.
[14]	H. Per, S. Kumandas, H. Gumus and A. Kurtsov, Primary Soliter and Multiple Intracranial Cyst Hydatid Disease: Report of Five Cases,” Brain and Development, Vol. 31, No. 3, 2009, pp. 228-233. doi:10.1016/j.braindev.2008.03.009
[15]	P. R. Torgerson and D. D. Heath, “Transmission Dynamics and Control Options for Echinococcus granulosus,” Parasitology, Vol. 127, Suppl. S1, 2003, pp. S143-S158. doi:10.1017/S0031182003003810
[16]	J. Bowles, D. Blair and D. P. McManus, “Genetic Variants within the Genus Echinococcus Identified by Mitochondrial DNA Sequencing,” Molecular and Biochemical Parasitology, Vol. 54, No. 2, 1992, pp. 169-174. doi:10.1016/0166-6851(92)90109-W
[17]	M. Pearson, T. H. Le, L. H. Zhang, D. Blair, T. H. N., Dai and D. P. McManus, “Molecular Taxonomy and Strain Analysis in Echinococcus,” In: P. Craig and Z. Pawlowski, Eds., Cestode Zoonoses: Echinococcus and Cysticercosis. An Emergent and Global Problem, Nato Science Series, Vol. 341, IOS Press, Amsterdam, 2002, pp. pp. 205-219.
[18]	E. Sanchez, O. Caceres, C. Naquirel, D. Garcia, G. Patino, H. Silvia, A. C. Volotao and O. Fernandez, “Molecular Characterization of Echinococcus granulosus from Peru by Equencing of the Mitochondrial Cytochrome c Oxidase Subunit 1 Gene,” Memórias do Instituto Oswaldo Cruz, Vol. 105, No. 6, 2010, pp. 806-810.
[19]	M. F. Harandi, R. P. Hobbs, P. J. Adams, I. Mobedi, U. M. Morgan-Ryan and R. C. Thompson, “Molecular and Morphological Characterization of Echinococcus granulosus of Human and Animal Origin in Iran,” Parasitology, Vol. 125, No. 4, 2002, pp. 367-373.
[20]	R. C. Thompson and D. P. McManus, “Towards a Taxonomic Revision of the Genus Echinococcus,” Trends in Parasitology, Vol. 18, No. 10, 2002, pp. 452-457. doi:10.1016/S1471-4922(02)02358-9
[21]	A. Varcasia, S. Canu, M. W. Lightowlers, A. Scala and G. Garippa, “Molecular Characterization of Echinococcus granulosus Strains in Sardinia,” Parasitology Research, Vol. 98, No. 3, 2006, pp. 273-277. doi:10.1007/s00436-005-0059-x
[22]	A. Dinkel, E. M. Njoroge, A. Zimmermann, M. W?lz, E. Zeyhle, I. E. Elmahdi, U. Mackenstedt and T. Romig, “A PCR System for Detection of Species and Genotypes of the Echinococcus granulosus-Complex, with Reference to the Epidemiological Situation in Eastern Africa,” International Journal for Parasitology, Vol. 34, No. 5, 2004, pp. 645-653. doi:10.1016/j.ijpara.2003.12.013
[23]	A. Obwaller, R. Schneider, J. Walochnik, B. Gollackner, A. Deutz, K. Janitschke, H. Asp?ck and H. Auer “Echinococcus granulosus Strain Differentiation Based on Sequence Heterogeneity in Mitochondrial Genes of Cytochrome c Oxidase-1 and NADH Dehydrogenase-1,” Parasitology, Vol. 128, No. 5, 2004, pp. 569-575. doi:10.1017/S0031182004004871
[24]	R. Schneider, B. Gollackner, B. Edel, K. Schmid, F. Wrba, G. Tucek, J. Walochnik and H. Auer, “Development of a New PCR Protocol for the Detection of Species and Genotypes (Strains) of Echinococcus in formalin-Fixed, Paraffin-Embedded Tissues,” International Journal for Parasitology, Vol. 38, No. 8-9, 2008, pp. 1065-1071. doi:10.1016/j.ijpara.2007.11.008
[25]	M. Nakao, Y. A. Tetsuya, O. B. Munehiro, K. A. Jenny, N. A. Agathe, S. A. Yasuhito and I. A. Akira, “State-of-the-Art Echinococcus and Taenia: Phylogenetic Taxonomy of Human-Pathogenic Tapeworms and Its Application to Molecular Diagnosis,” Infection, Genetics and Evolution, Vol. 10, No. 4, 2010, pp. 444-452. doi:10.1016/j.meegid.2010.01.011
[26]	J. Eckert and P. Deplazes, “Biological, Epidemiological, and Clinical Spects of Echinococcosis, a Zoonosis of Increasing Concern,” Clinical Microbiology Reviews, Vol. 17, No. 1, 2004, pp. 107-135. doi:10.1128/CMR.17.1.107-135.2004
[27]	I. Abbasi, A. Branzburg, M. Campos-Ponce, S. K. Abdel Hafez, F. Raoul, P. S. Craig and J. Hamburger, “Copro-Diagnosis of Echinococcus granulosus Infection in Dogs by Amplification of a Newly Identified Repeated DNA Sequence,” The American Journal of Tropical Medicine and Hygiene, Vol. 69, No. 3, 2003, pp. 324-230.
[28]	S. Stefanic, B. S. Shaikenov, P. Deplazes, A. Dinkel, P. R. Torgerson and A. Mathis, “Polymerase Chain Reaction for Detection of Patent Infections of Echinococcus granulosus (‘Sheep Strain’) in Naturally Infected Dogs,” Parasitology Research, Vol. 92, No. 4, 2004, pp. 347-351. doi:10.1007/s00436-003-1043-y
[29]	A. Naidich, D. P. McManus, S. G. Canova, A. M. Gutierrez, W. Zhang, E. A. Guarnera and M. C. Rosenzvit, “Patent and Pre-Patent Detection of Echinococcus granulosus Genotypes in the Definitive Host,” Molecular and Cellular Probes, Vol. 20, No. 1, 2006, pp. 5-10. doi:10.1016/j.mcp.2005.08.001
[30]	M. Rostami-Nejad, M. Nazemalhosseini, Z. Nochi, M. F. Harandi, K. Cheraghipour, G. R. Mowlavi and M. R. Zali, “Echinococcus granulosus Strain Differentiation in Iran Based on Sequence Heterogenecity in the Mitochondrial 12S rRNA gene,” Journal of Helminthology, Vol. 82, No. 4, 2008, pp. 343-347. doi:10.1017/S0022149X0804594X
[31]	M. Sharbatkhori, H. Mirhendi, M. F. Harandi, M., Rezaeian, M. Mohebali, M. Eshraghian, H. Rahimi and E. B. Kia, “Echinococcus granulosus Genotypes in Livestock of Iran Indicating High Frequency of G1 Genotype in Camels,” Experimental Parasitology, Vol. 124, No. 4, 2010, pp. 373-379. doi:10.1016/j.exppara.2009.11.020
[32]	J. Sambrook, E. F. Fritsch and T. Maniatis, “Molecular Cloning, a Laboratory Manual,” 2nd Edition, Cold Spring Harbor Laboratory Press, New York, 1989.
[33]	M. M. Siles-Lucas and B. B. Gottstein, “Molecular Tools for the Diagnosis of Cystic and Alveolar Echinococcosis,” Tropical Medicine & International Health, Vol. 6, No. 6, 2001, pp. 463-475. doi:10.1046/j.1365-3156.2001.00732.x
[34]	P. Kern, P. Frosch, M. Helbig, J. G. Wechsler, S. Usadel, K. Beckh, R. Kunz, R. lucius and M. Frosch, “Diagnosis of Echinococcus multilocularis Infection by Reverse-Transcription Polymerase Chain Reaction,” Gastroenterology, Vol. 109, No. 2, 1995, pp. 596-600. doi:10.1016/0016-5085(95)90350-X
[35]	P. Myjak, W. Nahorski, H. Pietkiewicz, M. von Nickisch-Rosenegk, J. Stolarczyk, E. Kacprzak, I. Felczak-Korzybska, B. Szostakowska and R. Lucius, “Molecular Confirmation of Human Alveolar Echinococcosis in Poland,” Clinical Infectious Diseases, Vol. 37, No. 8, 2003, pp. 121-125. doi:10.1086/378296
[36]	D. P. McManus and R. C. A. Thompson, “Molecular Epidemiology of Cystic Echinococcosis,” Parasitology, Vol. 127, Suppl. S1, 2003, pp. S37-S51. doi:10.1086/378296
[37]	M. Arbabi, J. Massoud, A. Dalimi-Asl and S. M. Sadjjadi, “Prevalence of Hydatidosis in Slaughtered Animals in Hamedan,” Journal of Shahed Universty, Vol. 5, 1998, pp. 57-61.