Molecular and Immunological Characterization and Incidence Rate of Hydatid Cyst Isolated from Liver and Lungs for Human in Kurdistan Region, Iraq

Authors

  • Muslim babawat Duhok polytechnic university

DOI:

https://doi.org/10.22317/imj.v7i4.1256

Keywords:

Echinococcus granulosus; G1/G3 genotypes; human cystic echinococcosis; ELISA, immune response; Kurdistan region; Iraq

Abstract

Objective: This study aimed to identify characteristics, location, cyst stage, and species/genotypes of Echinococcus granulosus s.l. complex in humans from the Kurdistan region, Iraq. Surgical removal of 25 echinococcal cysts from 22 patients in Dohuk and Zakho cities (January 2020 to December 2022) was analyzed.

Methods: Characteristics of 22 surgically confirmed cystic echinococcosis (CE) cases, including anatomical site, cyst fertility, and patient
demographics, were examined. Molecular analysis using mitochondrial NAD5 gene confirmed genotypes G1 or G3 of E. granulosus s.s.,
indicating sheep–dog–human transmission.

Results: Liver (78.6% fertile, 21.4% sterile) and lungs (81.8% fertile, 18.2% sterile) were the most common anatomical sites for CE in females (59.1%) compared to males (40.9%). All analyzed samples belonged to genotypes G1 or G3. No statistically significant correlation was found between genotypes and variables such as fertility, location, and cyst stage.

Conclusion: The study underscores the prevalence of genotypes G1 or G3 in the E. granulosus s.l. complex, confirming sheep–dog–human transmission in Kurdistan, Iraq. Recommendations include monitoring and control programs in sheep and dog populations and public health education campaigns to reduce the risk of acquiring CE in humans.

References

Leder, K. Weller, P. F. (2003). Clinical manifestation and diagnosis of cystic and alveolar Echinococcosis. www.uptodate.com.

Yildiz, K. Gurcan, I. S. (2009). The Detection of Echinococcus granulosus Strains Using Larval Rostellar Hook Morphometry. Turk. Parazitol Dergisi.; 33 (2): 199–202.

EL-Shazly, A. M. Ranya. M. S. Usama, S. B. Tarek, S. Hytham, A. Z. (2010).

Evaluation of ELISA and IHAT in serological diagnosis of proven of human Hydatidosis. J. Egypt Soc. Parasitol; 40 (2): 531–538.

Thompson, R.C.A. The taxonomy, phylogeny and transmission of Echinococcus. Exp. Parasitol. 2008, 119, 439–446.

Gottstein, B.; Reichen, J. Hydatid lung disease (echinococcosis/hydatidosis). Clin. Chest Med. 2002, 23, 397–408.

Higuita, N.I.A.; Brunetti, E. and McCloskey, C. (2016). Cystic echinococcosis. Journal of clinical microbiology, 54(3): 518–523.

Morar R, Feldman C. Pulmonary echinococcosis. Euro Res J. 2003;21(6):1069–1077. DOI: 10.1183/09031936.03.00108403.

Chandrakesan, S. D., & Parija, S. C. (2003). Latex agglutination test (LAT) for antigen detection in the cystic fluid for the diagnosis of cystic echinococcosis. Diagnostic microbiology and infectious disease, 45(2), 123–126. https://doi.org/10.1016/S0732-8893(02)00479-0.

Saarma U, Gisalu I, Moks E, Varcasia A, Lavikainen A, Oksanen A, Sismek S, Resiuk V, Denegri G, Gonza LM. Rate T, Rinaldi L, Maravilli P. A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitol. 2009;136(3): 317–328. DOI: https://doi.org/10.1017/S0031182008005453.

Molan, A.L. & Baban, M.R. (1993). The prevalence of Echinococcus granulosus in stray dogs in Iraq. Jpn. J. med. Sci. Biol. Feb.; 46(1):29–35.

Saeed, I., kapel, c., saida, L.A., Willingham, L., Nanse, P. (2000). Epidemiology of Echinococcus granulosus in Erbil province. Northern Iraq, 1990–1998. Journal of Helminthology, vol. 74(issue1): 83–88.

Abdullah, A. M. (2010). Epidemiological, comparative enzymatic and total protein content of hydatid cyst of E. granulosus isolated from sheep and goats in Duhok province, Kurdistan Region /Iraq. M.Sc. Thesis, College of Education, University of Duhok.

Molan, A.L. & Saida, L.A. (1989). Echinococcosis in Iraq: Prevalence of Echinococcus granulosus in stray dogs in Erbil province/Iraq, Jpn J med Sci Biol., 42(4):137–141.

McManus, D.P. (2006). Molecular discrimination of Taeniid cestodes. Parasitol. Int., 55:31–37.

Thompson, R.C.A. (2008). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119:439–446.

Nakao, M., McManus, D.P., Schantz, P.M., Craig, P.S., Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology, 134: 713–722.

Nakao, M., Li, T., Han, X., Ma, X., Xiao, N., Qiu, J.,Wang, H., Yanagida, T., Mamutia, W., Wen, H., Moro, P. L.,Giraudoux, P., Craig, P. S. & Ito, A. (2010). Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. Int J Parasitol., 40(3): 379–385.

Moro, P. & Schantz, P.M. (2009). Echinococcosis: a review. International Journal of Infectious Diseases, 13: 125–133.

Siracusano, A., teggi, A. & Ortona, E. (2009). Human cystic echinococcosis: Old problem and new prospective.Interdisiplinary Perspectives on Infectious disease.Vol. 2009, Article ID 474368, 7 pages. DOI: 10.1155/2009/474368.

Bowles, J., Blair, D. and McManus, D.P. (1994). Molecular genetics characterization of the cervid strain (Northern form) of Echinococcus granulosus. Parasitology, 109: 215–221.

Bowles, J., Blair, D. and McManus, D. P. (1995). Molecular phylogeny of the genus Echinococcus. Parasitol., 110: 317–328.

Budke, C. M., Deplazes, P. and Torgerson, P. R. (2006). Global socioeconomic impact of cystic Echinococcosis. Emerging Infectious Diseases, 12(2):296–303.

OIE (2008). Echinococcosis/hydatidiosis. OIE Terrestrial manual 2008. Chapter 2.1.4:175–189.

Pour, A. A., Hosseini, S. H, & Shayan, P. (2010).Comparative genotyping of Echinococcus granulosus infecting buffalo in Iran using cox1 gene. Parasitol Res. DOI 10.1007/s00436-010-2170-x.

Moro, P. & Schantz, P.M. (2009). Echinococcosis: a review. International Journal of Infectious Diseases, 13: 125–133.

Zhang, L., Eslami, A., Hosseini, S. H. & McManus, D.P. (1998). (Indication of the presence of two distinct strains of Echinococcus granulosus in Iran byMitochondrial DNA Markers. Am. J. Trop. Med. Hyg., 59(1): 171–174.

Ergin, S., Saribas, S., Yuksel, P., Zengin, K., Midilli, K., Ergin, S, et al. (2010). Genotypiccharacterization of Echinococcus granulosus isolated from human in Turkey. African Journal ofMicrobiology Research, 4 (7): 551–555.

Ghaffar, N. M. (2008). Prevalence of hydatidosis in livestock slaughtered at Duhok Abattoir, Kurdistan Region /Iraq. M.Sc. Thesis, College of Sciences/ University of Duhok.

Al-Qaoudy, K.M., Abdel-Hafez, S.K., Craig, P.S. (2003). Canine Echinococcosis in northern Jordan: increased prevalence and dominance of sheep/ dogstrain, 90(3):187–91.

Carmona C, Perdomo R, Carbo A, Alvarez C, Monti J, Grauert R, et al. Risk factors associated with human cystic echinococcosis in Florida, Uruguay: Results of a mass screening study using ultrasound and serology. Am J Trop Med Hyg 1998; 58:599–605.

Zhang W, McManus DP. Recent advances in the immunology and diagnosis of echinococcosis. FEMS Immunol Med Microbiol 2006; 47:24–4.

Yazgan S, Gursoy S, Usluer O, Ucvet A. Hydatid cyst with intracavitary fungal ball: Does it require lung resection? J Res Med Sci 2015; 20:204–5.

Nasrieh MA, Abdel Hafez SK. Echinococcus granulosus in Jordan: Assessment of various antigenic preparations for use in the serodiagnosis of surgically confirmed cases using enzyme immuno assays and the indirect haemagglutination test. Diagn Microbiol Infect Dis 2004; 48:117–23.

Iacona A, Pini C, Vicari G. Enzyme-linked immunosorbent assay (ELISA) in the serodiagnosis of hydatid disease. Am J Trop Med Hyg 1980; 29:95–102.

Craig PS, Rogan MT, Allan JC, Gillespie S, Hawkey P. Hydatidosis and cysticercosis-larval cestodes. Medical Parasitology: A Practical Approach. New York, USA: Oxford University Press Inc.; 1995. p. 209–37.

Maddison SE, Slemenda SB, Schantz PM, Fried JA, Wilson M, Tsang VC. A specific diagnostic antigen of Echinococcus granulosus with an apparent molecular weight of 8 kDA. Am J Trop Med Hyg 1989; 40:377–83.

Pearce E J, Scott P A and Sher A. Immune regulation in parasitic infection and disease. In Paul WE (ed). Fundamental immunology.4th ed. Philadelphia, Lippincott-Ravean publishers; 1999.

Siracusano A, Ortona E and Rigano R. Molecular and cellular tools in human cystic echinococcosis:Current Drug Targets Immune,Endocrine and Metabolic Disorders,2002; 2:235–45.

Zhang W, Ross A and MacManus D. Mechanisms of immunity in hydatid disease: Implications for vaccine development. J Immunol, 2008; 181: 6679–85.

Zhang W, Li J and Mcmanus DP. Concepts in immunology and diagnosis of hydatid disease. ClinMicrobol Rev, 2003; 16:18–36.

Rigano R, Profumo E, Bruschi F, Carulli G, Azzara AJ, Iopplo S. et al. Modulation of human immune response by Echinococcus granulosus antigen B and its possible role in evading host defenses. Infect. Immune; 2001; 69:288–96.

Virginio V, Taroco L, Ramose A, Ferreira A, Zaha A, Ferreira H and et al. Effect of protoscoleces and AgB from Echinococcus granulosus on human neutrophils: Possible implications on the parasites immune evasion mechanisms. Parasitol Res, 2006; 100: 935–42.

Rigano R, Buttari B, Profumo E, Ortona E, Delunado F, Margutti P, Mattei V et al. Echinococcus granulosus antigen B impairs human dendertic cell differentiation and polarizes immature dendertic cell maturation towards a Th2 cell response. Infect Immun, 2007; 75: 1667–78.

Dematteis S, Rottenberg M and Baz A. Cytokine response and outcome of infection depends on the infective dose of parasites in experimental infection by Echinococcus granulosus. Parasite Immunol, 2003; 25: 189–98.

Al-Qaoud K and Abdel Hafez S. Humoral and cytokine response during protection of mice against secondary hydatidosis caused by Echinococcus granulosus. Parasitol Res, 2005; 98: 54–60.

Obwaller A, Schneider R, Walochnik J, Gollackner B, Deutz A, Janitschke K et al. Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology, 2004; 128: 569–75.

Thompson RC, Boxell AC, Ralston BJ, Constantine CC, Hobbs R P, Shury T et al. Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitol, 2006; 132: 439–47.

Roratto PA, Bartholomei-Santos ML, Gutierrez AM, Kamenetzky L, Rosenzvit MC and Zaha A.Detection of genetic polymorphism among and within Echinococcus granulosus strains byheteoduplex analysis of a microsatelliate from the U1snRNA genes.Genet Mol Res, 2006; 5: 542–52.

De La Rue M L, Dinkel A Mackenstedt U and Roming T. New data on Echinococcus spp. In Southern Brazil. Rev Inst Med Trop S. Paulo, 2006; 48: 103–4.

Gottestein B. Molecular and immunological diagnosis of echinococcosis. Clin Microbiol Rev; 1992; 5:248–61.

Mehlhorn H.Parasitology. Berlin: Springer-verlag Berlin Heiderg, 2001.

Santolamazza, F.; Santoro, A.; Possenti, A.; Cacciò, M.S.; Casulli, A. A validated method to identify Echinococcus granulosus sensu lato at species level. Infect. Genet. Evol. 2020, 85, 104575.

Kinkar, L.; Laurimäe, T.; Acosta-Jamett, G.; Andresiuk, V.; Balkaya, I.; Casulli, A. Distinguishing Echinococcus granulosus sensu stricto genotypes G1 and G3 with confidence: A practical guide. Infect. Genet. Evol. 2018, 64, 178–184.

Al-Jobbory, S. H. H. (2005). SeroParasitological Identification of Human Hydatidosis in Space Occupying Lesions in Mosul. M.Sc. Thesis, Coll. Med. Mosul.

Shehatha, J. Alward, M. Saxena, P. Konstantinov, I. E. (2008). Surgical Management of Cardiac Hydatidosis. Tex. Heart. Inst. J.; 36(1): 72–73.

AL-Barwari, S. E. Saeed, I. S. Khalid, W. AL-Harmini, K. I. (1991). Human Hydatidosis in Arbil, N. Iraq. J. Islam Acade Scien; 4 (4): 330 –335.

Abu-Hasan, Daragmeh, M. Adwan, K. Al-Qaoud, K. and Abdel-Hafez, S. (2001). Human cystic echinococcosis in the West Bank of Palestine: surgical incidence and sero-epidemiological study. Parasitol. Res. 88 (2): 107 –112.

Fahim, F. Al-Salamah, S. M. (2007). Cystic echinococcosis in Central Saudi Arabia: A 5-year experience. Turk. J. Gastroenterol; 18 (1): 22 –27.

Ranjbar-bahadori, S.; Lotfollahzadeh, S.; Vaezi, G.; Eslami, A. Epidemiological study of the human cystic echinococcosis in Iran. Res. J. Parasitol. 2008, 3, 130–136.

Al-Bosely, A.R.I. Studies on epidemiology and some enzyme activities in laminated and germinal layers of hydatid cysts isolated from different intermediate hosts in Zakho, Duhok Province, Kurdistan Region of Iraq. Master’s Thesis, University of Zakho, Zakho, Iraq, 2013.

Khan, A.; Ahmed, H.; Simsek, S.; Liu, H.; Yin, J.; Wang, Y.; Shen, Y.; Cao, J. Molecular characterization of human Echinococcus isolates and the first report of E. canadensis (G6/G7) and E. multilocularis from the Punjab Province of Pakistan using sequence analysis. BMC Infect. Dis. 2020, 20, 262.

Molan, A.L. Epidemiology of hydatidosis and echinococcosis in Theqar Province, Southern Iraq. Jpn. J. Med. Sci. Biol. 1993, 46, 29–35.

Al Saeed, A.T.M.; Almufty, K.S.A. Human hydatidosis in Duhok–Kurdistan Region–North of Iraq. Med. J. Babylon 2016, 13, 125–133.

Saida, L.A.; Nouraddin, A.S. Epidemiological study of cystic echinococcosis in Man and slaughtered Animals in Erbil province, Kurdistan Regional-Iraq. Tikrit J. Pure Sci. 2011, 16, 45–50.

Saghafipour, A.; Divband, M.; Farahani, L.Z.; Parsa, H.H.; Fard, H.G. Epidemiology, burden, and geographical distribution of cystic echinococcosis in Central Iran. Int. J. One Health 2020, 6, 17–22.

Lotfi, M. (2004). Diagnosis and Treatment of hydatid cyst of the liver. Pakistan J. Surgery; 8: 109-114.

Wani, N. A. Kosar, T. L. Khan, A. Q. Ahmad, S. S. (2010). Multidetector-row Computed tomography in cerebral hydatid cyst. J. Neurosci. Rural Pract. 1(2): 112–114.

Arda, B. Yamazhan, T. Demirpolat, G. (2009). Prevalence of Echinococcus granulosus detected using enzyme immunoassay and abdominal ultrasonography in a group of students staying in a state dormitory in Turkey. Turk. J. Med. Sci; 39 (5): 791–794.

Al-sakee, H. M. A. Al-barzanjy, Z. K. A. Baker. H. M. (2004). Prevalence of antihydatid Antibodies in Erbil community: an epidemulogical approach. Z. J. M. S. 8; 79–85

Khalf, M.S.; AlTaie, L.H.; AlFaham, M.A. The incidence of hydatid cyst in human in baghdad governorate. IOSR J. Pharm. Biol. Sci. 2014, 9, 11–14.

Salem, O.A.; Schneegans, F.; Chollet, J.Y.; Jemli, M.H. Epidemiological studies on Echinococcosis and characterization of human and livestock hydatid cysts in Mauritania. Iran. J. Parasitol. 2011, 6, 49–57.

Tamarozzi, F.; Akhan, O.; Cretu, C.M.; Vutova, K.; Akinci, D.; Chipeva, R.; Ciftci, T.; Constantin, C.M.; Fabiani, M.; Golemanov, B.; et al. Prevalence of abdominal cystic echinococcosis in rural Bulgaria, Romania, and Turkey: A cross-sectional, ultrasound-based, population study from the HERACLES project. Lancet Infect. Dis. 2018, 18, 769–778.

Piccoli, L.; Bazzocchi, C.; Brunetti, E.; Mihailescu, P.; Bandi, C.; Mastalier, B.; Cordos, I.; Beuran, M.; Popa, L.G.; Meroni, V.; et al. Molecular characterization of Echinococcus granulosus in South-Eastern Romania: Evidence of G1–G3 and G6–G10 complexes in humans. Clin. Microbiol. Infect. 2013, 19, 578–582.

Possenti, A.; Manzano-Román, R.; Sánchez-Ovejero, C.; Boufana, B.; La Torre, G.; Siles-Lucas, M.; Casulli, A. Potential risk factors associated with human cystic echinococcosis: Systematic review and meta-analysis. PLoS Negl. Trop. Dis. 2016, 10, e0005114.

Alvarez Rojas, C.A.; Romig, T.; Lightowlers, M.W. Echinococcus granulosus sensu lato genotypes infecting humans—Review of current knowledge. Int. J. Parasitol. 2014, 44, 9–18.

Ahmed, B.D.; Mero, W.M.S.; Salih, A.M.; Xiao, N.; Casulli, A.; Abdo, J.M. Molecular characterization of Echinococcus granulosus isolated from human hydatid cyst using mitochondrial Cox1 gene sequencing in Dohuk Province–Kurdistan Region, Iraq. Sci. J. Univ. Zakho 2013, 1, 72–80.

Hassan, H.F.; Fadhil, M.H.; Fadhil, Z.H. Molecular characterization of Echinococcus granulosus isolated from human and domestic animals in Kirkuk, Iraq. Anim. Res. Int. 2016, 13, 2544–2547.

Alsaady, H.A.M.; Al-Quzweeni, H.A.N. Molecular study of Echinococcus granulosus in Misan Province, South of Iraq. Indian J. Public Health Res. Dev. 2019, 10, 1046–1050.

Mahdi, Z.M.S.; Al-Hamairy, A.K.; Al-Rubaiey, H.M. Genotyping of Echinococcus granulosus isolates from human, sheep and cattles hydatid cysts in some Central Euphrates Provinces, Iraq. Med.-Leg. Update 2020, 20, 570–575.

Vural, G.; Baca, A.U.; Gauci, C.G.; Bagci, O.; Gicik, Y.; Lightowlers, M.W. Variability in the Echinococcus granulosus cytochrome C oxidase1 mitochondrial gene sequence from livestock in Turkey and a re-appraisal of the G1–3 genotype cluster. Vet. Parasitol. 2008, 154, 347–350.

Kurt, A.; Avcioglu, H.; Guven, E.; Balkaya, I.; Oral, A.; Kirman, R.; Bia, M.M.; Akyuz, M. Molecular characterization 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, 593–602.

Parsa, F.; Haghpanah, B.; Pestechian, N.; Salehi, M. Molecular epidemiology of Echinococcus granulosus strains in domestic herbivores of Lorestan, Iran. Jundishapur J. Microbiol. 2011, 4, 123–130.

Arbabi, M.; Pirestani, M.; Delavari, M.; Hooshyar, H.; Abdoli, A.; Sarvi, S. Molecular and morphological characterizations of Echinococcus granulosus from human and animal isolates in Kashan, Isfahan Province, Iran. Iran. J. Parasitol. 2017, 12, 177–187.

Issa, H.S.; Abdel-Hafez, S.K.; Hijjawi, N.S.; Al-Qaoud, K.M. Molecular characterization of Echinococcus granulosus sensu stricto cysts of domestic ruminants in Jordan. Jordan J. Biol. Sci. 2018, 11, 301–306.

Metwally, D.M.; Qassim, L.E.; Al-Turaiki, I.M.; Almeer, R.S.; El-Khadragy, M.F. Gene-based molecular analysis of COX1 in Echinococcus granulosus cysts isolated from naturally infected livestock in Riyadh, Saudi Arabia. PLoS ONE 2018, 13, e0195016.

Al-Hizab, F.A.; Mohamed, N.S.; Wassermann, M.; Hamouda, M.A.; Ibrahim, A.M.; Ghareeb, W.R.; Abdel-Raheem, S.M.; Romig, T.; Omer, R.A. Three species of Echinococcus granulosus sensu lato infect camels on the Arabian Peninsula. Parasitol. Res. 2021, 120, 2077–2086.

Casulli, A.; Massolo, A.; Saarma, U.; Umhang, G.; Santolamazza, F.; Santoro, A. Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000–2021): A systematic review approach. Parasites Vectors 2022, 15, 109.

Morar R and Feldman C. Pulmonary echinococosis. Eur Respir J, 2003; 21: 1069–77.

Ghorbanalinezhad E, Assmar M, Piazak N and Khabiri A. Development of new ELISA kit for the diagnosis of hydatid osis in humans. Iran J Pub Health, 2001; 30: 67–70.

Kanwar J R, Kanwar R K, Grewal A S and Vinayak V K. Significance of detection of immune- complexed 8 KDa hydatid-specific antigen for Imunodiagnosis of hydatidosis. FEMS Immmunol Microbil, 1994; 9: 231–36.

Chematai A K, Bowry T R and Ahmad Z. Evaluation of five immunodiagnostic techniques in ehinococcosis patients. Bull World Health Organ, 1981; 59: 767–72.

Kuroo MS. Hydatid disease:Current status and recent advances.Ann Saudi Med,2002; 22: 56–4.

Manson PE and Bell DR. Mansons Tropical Disease, Baillier Tindall, 1987.

Craig P S. Immunodiagnosis of Echinococcus granulosus and a comparison of techniques for diagnosis of canine echinococcosis. In Anderson F L, Ouhelli H and Kachani M (eds). Compendium on cystic echinococcosis in Africa and in Middle Eastern countries with special reference to Morocco. Provo, USA, Bringham Young University. 1997.

Mehlhorn H.Parasitology. Berlin: Springer-verlag Berlin Heiderg, 2001.

Downloads

Published

2024-01-03

How to Cite

babawat, M. (2024). Molecular and Immunological Characterization and Incidence Rate of Hydatid Cyst Isolated from Liver and Lungs for Human in Kurdistan Region, Iraq. Iraq Medical Journal, 7(4). https://doi.org/10.22317/imj.v7i4.1256