Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T05:52:49.001Z Has data issue: false hasContentIssue false

Molecular characterization of Echinococcus granulosus in livestock of Al-Madinah (Saudi Arabia)

Published online by Cambridge University Press:  01 June 2020

N.M. AL-Mutairi
Affiliation:
Faculty of Science, Taibah University, Al-Madinah, Saudi Arabia
H.A. Taha
Affiliation:
Faculty of Science, Ain Shams University, Cairo, Egypt
A.H. Nigm*
Affiliation:
Faculty of Science, Ain Shams University, Cairo, Egypt
*
Author for correspondence: A.H. Nigm, E-mail: ahmednigm@sci.asu.edu.eg

Abstract

Echinococcus granulosus is the causative agent of cystic echinococcosis, which has serious impacts on human and/or animal health, resulting in significant economic losses. Echinococcus granulosus comprises a number of intra-specific variants or strains at the genetic level. In Saudi Arabia, few studies were performed on genetic variations in Echinococcus species. Therefore, the present study aimed to investigate the phenotypic and genetic characterization of hydatid cysts harboured by sheep and camels in Al-Madinah Al-Munawarah. Samples of hydatid cysts were collected from local sheep (n = 25) and camels (n = 8). The morphological criteria of protoscoleces were investigated. To investigate the molecular characterization, random amplified polymorphic DNA polymerase chain reaction (RAPD-PCR), single-stranded conformation polymorphism (SSCP) were carried out. DNA was extracted from individual fertile cysts and subjected to RAPD-PCR analysis (using five arbitrary primers) and PCR amplification of cytochrome c oxidase I (cox1) and 12S ribosomal ribonucleic acid (12S rRNA) genes. The PCR products were subjected to SSCP analysis for genetic discrimination in E. granulosus isolates. In addition, partially sequencing of the mitochondrial DNA cox1 genes was achieved for assessing the phylogenetic positions of collected isolates using some global published sequence data of cox1 genes. The rostellar hooks of camel and local sheep isolates show remarkable variability in their dimensions. Five distinct SSCP patterns were identified in the 12S rRNA gene, showing intraspecific variations in E. granulosus of camels and local sheep. Sequencing of (cox1) genes of both local sheep and camels exhibit high similarity with those of the same gene (E. granulosus sensu stricto) published in NCBI BLAST.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Baki, AS, Almalki, E and Al-Quarishy, S (2018) Prevalence and characterization of hydatidosis in Najdi sheep slaughtered in Riyadh city, Saudi Arabia. Saudi Journal of Biological Sciences 25(7), 13751379.CrossRefGoogle ScholarPubMed
Abu-Eshy, SA (1998) Some rare presentations of hydatid cyst (Echinococcus granulosus). Journal of the Royal College of Surgeons of Edinburgh 43(5), 347352.Google Scholar
Adewunmi, OA and Basilingappa, HM (2004) Primary ovarian hydatid disease in the Kingdom of Saudi Arabia. Saudi Medical Journal 25(11), 16971700.Google ScholarPubMed
Ahmad, G, Nizami, WA and Saifullah, M (2001) Analysis of potential antigens of protoscolices isolated from pulmonary and hepatic hydatid cyst of Bubalus bubalis. Comparative Immunology, Microbiology and Infectious Diseases 24, 91110.CrossRefGoogle Scholar
Ahmadi, N (2004) Using morphometry of the larval rostellar hooks to distinguish Iranian strains of Echinococcus granulosus. Annals of Tropical Medicine & Parasitology 98, 211220.CrossRefGoogle ScholarPubMed
Ahmadi, N, Dalimi, A and Ahmadi, NA (2006) Characterization of Echinococcus granulosus isolates from human, sheep and camel in Iran. Infection, Genetics and Evolution 6(2), 8590.CrossRefGoogle ScholarPubMed
Al-Malki, JS and Degheidy, NS (2013) Epidemiological studies of hydatidosis among slaughtered sheep and human in Taif, Saudi Arabia. Assiut Veterinary Medicine Journal 59(139), 4550.Google Scholar
Al-Mofleh, IA, Al-Rashed, RS, Ayoola, EA, Al-Faleh, FZ, Al-Amri, SM, Al-Rikabi, AC, Al-Sohaibani, MO and Reyes, AH (2000) Hepatic granulomas in an Arab population: a retrospective study from a teaching hospital in Riyadh. Saudi Journal of Gastroenterology 6, 4146.Google Scholar
Al-Olayan, EM, Metwally, DM, Fouad, D, Omer, SA and Helmi, H (2014) Molecular characterization of camel, sheep and goat Echinococcus granulosus isolates in Riyadh, Saudi Arabia. Mitteilungen Klosterneuburg 64(9), 194212.Google Scholar
Almalki, E, Al-Quarishy, S and Abdel-Baki, AS (2017) Assessment of prevalence of hydatidosis in slaughtered Sawakny sheep in Riyadh city, Saudi Arabia. Saudi Journal of Biological Sciences 24(7), 15341537.CrossRefGoogle ScholarPubMed
Almeida, FB, Rodrigues-Silva, R and Neves, RH (2007) Intraspecific variation of Echinococcus granulosus in livestock from Peru. Veterinary Parasitology 143(1), 5058.CrossRefGoogle ScholarPubMed
Amer, OH, Haouas, N, Al-Hathal, EA, El-Shikh, I and Ashankyty, I (2018) Cystic echinococcosis in slaughtered animals in Ha'il, Northwestern Saudi Arabia. Japanese Journal of Veterinary Research 66(4), 289296.Google Scholar
Amini-Bavil-Olyaee, S, Alavian, SM, Adeli, A, Sarrami-Forooshani, R and Sabahi, F (2006) Hepatitis B virus genotyping, core promoter, and precore/core mutations among Afghan patients infected with hepatitis B: a preliminary report. Journal of Medical Virology 78, 358364.CrossRefGoogle ScholarPubMed
Bhattacharya, D, Bera, AK, Bera, BC, Pan, D and Das, SK (2008) Molecular appraisal of Indian animal isolates of Echinococcus granulosus. Indian Journal of Medical Research 127, 383387.Google ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165174.CrossRefGoogle ScholarPubMed
Eckert, J, Thompson, RC, Michael, SA, Kumaratilake, LM and El-Sawah, HM (1989) Echinococcus granulosus of camel origin: development in dogs and parasite morphology. Parasitology Research 75, 536544.CrossRefGoogle ScholarPubMed
Eryildiz, C and Sakru, N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Medical Journal 29(3), 261267.Google ScholarPubMed
Eslami, A, Meshgi, B, Jalousian, F, Rahmani, S and Salari, MA (2016) Genotype and phenotype of Echinococcus granulosus derived from wild sheep (Ovis orientalis) in Iran. The Korean Journal of Parasitology 54(1), 5560.CrossRefGoogle Scholar
Fallahizadeh, S, Arjmand, R, Jelowdarjelowdar, A, Rafiei, A and Kazemi, F (2019) Determination of Echinococcus granulosus genotypes in livestock slaughtered in Shush County, Southwest Iran using PCR-RFLP. Helminthologia 56(3), 196201.CrossRefGoogle ScholarPubMed
Fdaladdin, YAJ, Alsaggaf, AI and Wakid, MH (2013) Comparative epidemiological studies on Echinococcosis of local and imported livestock in Al-Madina Al-Munawwarah in Saudi Arabia. The Egyptian Journal of Hospital Medicine 50(1), 108126.CrossRefGoogle Scholar
Gasser, RB, Zhu, X and McManus, DP (1998) Display of sequence variation in PCR-amplified mitochondrial DNA regions of Echinococcus by single-strand conformation polymorphism. Acta Tropica 71(2), 107115.CrossRefGoogle ScholarPubMed
Gholami, S, Irshadullah, M and Khan, A (2009) Genetic variation of Echinococcus granulosus isolates from Indian buffalo and Iranian sheep, cattle and camel. Journal of Mazandaran University of Medical Sciences 19, 6069.Google Scholar
Gordo, FP and Bandera, CC (1997) Differentiation of Spanish strains of Echinococcus granulosus using larval rostellar hook morphometry. International Journal for Parasitology 27(1), 4149.CrossRefGoogle Scholar
Grosso, G, Gruttadauria, S, Biondi, A, Marventano, S and Mistretta, A (2012) Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World Journal of Gastroenterology 18(13), 14251437.CrossRefGoogle ScholarPubMed
Haag, KL, Araujo, AM, Gottstein, B, Siles-Lucas, M, Thompson, RCA and Zaha, A (1999) Breeding systems in Echinococcus granulosus (Cestoda Taeniidae): selfing or outcrossing? Parasitology 118, 6371.CrossRefGoogle ScholarPubMed
Harandi, MF, Hobbs, RP, Adams, PJ, Mobedi, I, Morgan-Ryan, UM and Thompson, RCA (2002) Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitology 125, 367–73.Google ScholarPubMed
Hayajneh, FMF, Althomali, AMH and Nasr, ATM (2014) Prevalence and characterization of hydatidosis in animals slaughtered at Al Taif abattoir, Kingdom of Saudi Arabia. Open Journal of Animal Sciences 4(1), 3841.CrossRefGoogle Scholar
Hobbs, RP, Lymbery, AJ and Thompson, RCA (1990) Rostellar hook characters of Echinococcus granulosus (Batsch, 1786) from natural and experimental Australian hosts, and its implications for strain recognition. Parasitology 101, 273281.CrossRefGoogle ScholarPubMed
Hussain, A, Maqbool, A, Tanveer, A and Anees, A (2005) Studies on morphology of Echinococcus granulosus from different animal-dog origin. Punjab University Journal of Zoology 20(2), 151157.Google Scholar
Ibrahim, MM (2010) Study of cystic echinococcosis in slaughtered animals in Al Baha region Saudi Arabia: Interaction between some biotic and abiotic factors. Acta Tropica 113, 2633.CrossRefGoogle ScholarPubMed
Irshadullah, M and Nizami, WA (1997) Biochemical characterization of protoscoleces isolated from buffalo hepatic and pulmonary hydatid cyst. Journal of Parasitology and Animal Biolology 6(1), 1324.Google Scholar
Karimi, A and Dianatpour, R (2008) Genotypic and phenotypic characterization of Echinococcus granulosus of Iran. Biotechnology 7, 757762.CrossRefGoogle Scholar
Lodish, H, Berk, A, Zipursky, LS, Matsudaira, P and Baltimore, D (2000) Recombinant DNA and genomics.pp. 1184 in Lodish, H, Berk, A, Zipursky, LS, Matsudaira, P, Baltimore, D and Darnell, J (Eds) Molecular cell biology. 4th edn. New York, W.H. and Freeman Company.Google Scholar
Lubinsky, G (1962) On the environmental plasticity of the number of rostellar hooks in larval Echinococcus multilocularis. Canadian Journal of Zoology 40, 607614.CrossRefGoogle Scholar
Lymbery, AJ and Thompson, RC (1989) Genetic differences between cysts of Echinococcus granulosus from the same host. International Journal of Parasitology 19(8), 961964.CrossRefGoogle ScholarPubMed
Lynch, M (1990) The similarity index and DNA fingerprinting. Molecular Biology and Evolution 7, 478484.Google ScholarPubMed
Mariaux, J (1996) Cestode systematics: any progress? International Journal for Parasitology 26(3), 231243.CrossRefGoogle ScholarPubMed
McManus, DP (2002) The molecular epidemiology of Echinococcus granulosus and cystic hydatid disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 96(1), S151S157.CrossRefGoogle ScholarPubMed
Menekşe, G, Özsoy, KM, Dağlioğlu, E, Güzel, E, Güzel, A and Belen, D (2012) Pediatric giant-sized intracerebral hydatid cyst: reports of two cases. Journal of Neurological Sciences 29(4), 841846.Google Scholar
Metwally, DM, Qassim, LE, Al-Turaiki, IM, Almeer, RS and El-Khadragy, MF (2018) Gene-based molecular analysis of Cox1 in Echinococcus granulosus cysts isolated from naturally infected livestock in Riyadh, Saudi Arabia. PLoS ONE 13(4), e0195016.CrossRefGoogle ScholarPubMed
Mostafa, OMS, Taha, HA and Ramadan, G (2003) Diagnosis of Fasciola gigantica in snail using the polymerase chain reaction (PCR) assay. Journal of the Egyptian Society of Parasitology 33(3), 733742.Google ScholarPubMed
Nakao, M, McManus, D, Schantz, P, Craig, P and Ito, AA (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713722.CrossRefGoogle ScholarPubMed
Nakao, M, Lavikainen, A, Yanagida, T and Ito, A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). International Journal for Parasitology 43, 10171029.CrossRefGoogle Scholar
Nei, M and Li, WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceeding of the National Academy of Science of the United States of America 76, 52695273.CrossRefGoogle ScholarPubMed
Nejad, MR, Taghipour, N, Nochi, Z, Mojarad, EN, Mohebbi, SR, Harandi, MF, et al. (2012) Molecular identification of animal isolates of Echinococcus granulosus from Iran using four mitochondrial genes. Journal of Helminthology 86(4), 485492.CrossRefGoogle Scholar
Nikmanesh, B, Mirhendi, H, Ghalavand, Z, Alebouyeh, M, Sharbatkhori, M, et al. (2014) Genotyping of Echinococcus granulosus isolates from human clinical samples based on sequencing of mitochondrial genes in Iran, Tehran. Iranian Journal of Parasitology 9(1), 20.Google ScholarPubMed
Nungari, L, Mbae, C, Gikunju, J, et al. (2019) Prevalence and genotyping of Echinococcus species from livestock in Kajiado County, Kenya. BioMed Research International 2019, 17.CrossRefGoogle ScholarPubMed
Oudni-M'rad, M, Cabaret, J, M'rad, S, et al. (2006) Genetic differences between Tunisian camel and sheep strains of the cestode Echinococcus granulosus revealed by SSCP. Parasite 13(2), 131136.CrossRefGoogle ScholarPubMed
Pezeshki, A, Akhlaghi, L, Sharbatkhori, M, Razmjou, E, Oormazdi, H, Mohebali, M, et al. (2013) Genotyping of Echinococcus granulosus from domestic animals and humans from Ardabil Province, northwest Iran. Journal of Helminthology 87(4), 387391.CrossRefGoogle ScholarPubMed
Rahimi, HR, Kia, EB, Mirhendi, SH, Talebi, A, Fasihi-Harandi, M, Jalali-zand, N and Rokni, MB (2007) A New primer pair in ITS1 region for molecular studies on Echinococcus granulosus. Iranian Journal of Public Health 36, 4549.Google Scholar
Ramos-Sarmiento, D and Chiluisa-Utreras, V (2020) First molecular identification of hydatid tapeworm Echinococcus granulosus sensu lato G6/G7 in Ecuador. Journal of Helminthology 94, e100.CrossRefGoogle Scholar
Rashed, AA, Omer, HM, Fouad, MA and Al-Shareef, AM (2004) The effect of severe cystic hydatidosis on the liver of a Najdi sheep with special reference to the cyst histology and histochemistry. Journal of the Egyptian Society of Parasitology 34(1), 297304.Google Scholar
Rojas, CAA, Ebi, D, Paredes, R, et al. (2017) High intraspecific variability of Echinococcus granulosus sensu stricto in Chile. Parasitology International 66(2), 112115.CrossRefGoogle Scholar
Romig, T, Deplazes, P, Jenkins, D, Giraudoux, P, Massolo, A, Craig, PS, Wassermann, M, Takahashi, K and de la Rue, M (2017) Ecology and life cycle patterns of Echinococcus species. Advances of Parasitology 95, 213314.CrossRefGoogle ScholarPubMed
Simsek, S, Balkaya, I, Ciftci, AT and Utuk, AE (2011) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Veterinary of Parasitology 178, 367369.CrossRefGoogle ScholarPubMed
Stefanić, S, Shaikenov, BS, Deplazes, P, Dinkel, A, Torgerson, PRA and Mathis, A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitology Research 92(4), 347351.CrossRefGoogle Scholar
Sweatman, GK and Williams, JF (1963) Comparative studies on the biology and morphology of Echinococcus granulosus from domestic livestock, moose and reindeer. Parasitology 53, 493514.CrossRefGoogle ScholarPubMed
Taha, HA (2012) Genetic variations among Echinococcus granulosus isolates in Egypt using RAPD-PCR. Parasitology Research 111(5), 19932000.CrossRefGoogle ScholarPubMed
Tang, CT, Quian, YC, Kang, YM, Cui, GW, Lu, HC, Shu, LM, Wang, YH and Tang, L (2004) Study on the ecological distribution of alveolar Echinococcus in Hulunbeier pasture of Inner Mongolia, China. Parasitology 128, 187194.CrossRefGoogle Scholar
Tashani, OA, Zhang, LH, Boufana, B, Jegi, A and McManus, DP (2002) Epidemiology and strain characteristics of Echinococcus granulosus in the Benghazi area of eastern Libya. Annals of Tropical Medicine and Parasitology 96(4), 369381.CrossRefGoogle ScholarPubMed
Thompson, RCA (1995) Biology and systematics of Echinococcus. pp. 150in Thompson, RCA and Lymbery, AJ (Eds) Echinococcus and hydatid disease. Wallingford: CAB.Google Scholar
Thompson, RCA and McManus, DP (2001) Aetiology: parasites and life-cycles. pp. 119in Eckert, J, Gemmell, MA, Meslin, FX and Pawlowski, ZS (Eds) Manual on echinococcosis in humans and animals: a public health problem of global concern. WHO/OIE, Paris, France.Google Scholar
Thompson, RCA, Boxell, AC, Ralston, BJ, Constantine, CC, Hobbs, RP, Shury, T and Olson, ME (2006) Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439447.CrossRefGoogle ScholarPubMed
Toulah, FH and Albalawi, IM (2019a) Prevalence and histopathological studies on cystic echinococcosis among slaughtered sheep in Makkah, Kingdom of Saudi Arabia. Jacobs Journal of Veterinary Science and Research 6(1), 041.Google Scholar
Toulah, FH and Albalawi, IM (2019b) Prevalence of hydatidosis among slaughtered sheep in Makkah, Kingdom of Saudi Arabia. Journal of Bacteriology and Parasitology 10, 358.CrossRefGoogle Scholar
Toulah, FH, El Shafi, AA, Alsolami, MN and Wakid, MH (2017) Hydatidosis among imported animals in Jeddah, Saudi Arabia. Journal of Liver and Clinical Research 4(1), 1031.Google Scholar
Turcekova, L, Snabel, V, D'Amelio, S, Busi, M and Dubinsky, P (2003) Morphological and genetic characterization of Echinococcus granulosus in the Slovak Republic. Acta Tropica 85, 223229.CrossRefGoogle ScholarPubMed
Wassermann, M, Woldeyes, D, Gerbi, BM, et al. (2016) A novel zoonotic genotype related to Echinococcus granulosus sensu stricto from southern Ethiopia. International Journal of Parasitology 46, 663668.CrossRefGoogle ScholarPubMed
Williams, JGK, Kubelik, AR, Livak, KJ, Rafalski, JA and Tingey, SV (1990) DNA polymorphism amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 18, 65316535.CrossRefGoogle ScholarPubMed
Yan, B, Liu, X, Wu, J, Zhao, S, Yuan, W, Wang, B and Wang, Y (2018) Genetic diversity of Echinococcus granulosus genotype G1 in Xinjiang, northwest of China. The Korean Journal of Parasitology 56(4), 391396.CrossRefGoogle ScholarPubMed
Yap, KW and Thompson, RC (1987) CTAB precipitation of cestode DNA. Parasitology Today 3(7), 220222.CrossRefGoogle ScholarPubMed
Yildiz, K and Gurcan, IS (2009) The detection of Echinococcus granulosus strains using larval rostellar hook morphometry. Turkiye Parazitolojii Dergisi 33(2), 199202.Google ScholarPubMed
Zhang, LH, Gasser, RB, Zhu, X and McManus, DP (1990) Screening for different genotypes of Echinococcus granulosus within China and Argentina by single-strand conformation polymorphism (SSCP) analysis. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 329334.CrossRefGoogle Scholar
Zhang, L, Eslami, A, Hosseini, SH and McManus, DP (1998) 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 59, 171174.CrossRefGoogle ScholarPubMed
Zhu, XQ and Gasser, RB (1998) Single-strand conformation polymorphism (SSCP)-based mutation scanning approaches to fingerprint sequence variation in ribosomal DNA of ascaridoid nematodes. Electrophoresis 19, 13661373.CrossRefGoogle ScholarPubMed
Zhu, XQ, Jacobs, DE, Chilton, NB, Sani, RA, Cheng, NABY and Gasser, RB (1998) Molecular characterization of a Toxocara variant from cats in Kuala Lumpur, Malaysia. Parasitology 117, 155164.CrossRefGoogle ScholarPubMed