Research advances in genotyping of Echinococcus

doi:10.20199/j.issn.1672-2302.2025.05.012

Abstract

Abstract:

Echinococcosis, caused by the larvae of Echinococcus (hydatid cysts) parasitizing in the liver, lung and other tissues and organs of intermediate hosts, is a globally prevalent zoonotic parasitic disease. It not only seriously endangers human health but also exerts a significant impact on the development of animal husbandry. In recent years, research on the genotyping of Echinococcus has advanced with the progress of molecular biology techniques. In this article, we reviewed the genotyping techniques of Echinococcus, major genotyping methods, research progress on the genotyping of two important Echinococcus species and their global epidemic status, with an attempt to offer an insight into the research in future and provide references for better understanding and control of echinococcosis.

Key words: Echinococcus, Genotyping, Echinococcus granulosus, Echinococcus multilocularis

CLC Number:

R383.33

LI Xiaolu, GUO Bangcheng, GAO Jianwei, HAI E, YANG Cong, TIAN Jinhua, BAI Nan, TIAN Yulin. Research advances in genotyping of Echinococcus[J]. Journal of Tropical Diseases and Parasitology, 2025, 23(5): 313-318.

Figures/Tables 1

References 70

[1]	王旭, 王莹, 刘白雪, 等. 棘球绦虫和棘球蚴病的简明认知历史[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(3):372-383. doi: 10.12140/j.issn.1000-7423.2024.03.014
[2]	中华人民共和国中央人民政府. 中共中央、国务院印发“健康中国2030”规划纲要[EB/OL]. (2016-10-25)[2025-04-20]. https://www.gov.cn/zhengce/202203/content_3635233.htm.
[3]	董路, 关少君, 段博芳, 等. 包虫病的流行与诊治研究进展[J]. 草学, 2024(2):70-76.
[4]	Torgerson PR, Devleesschauwer B, Praet N, et al. World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis[J]. PLOS Medicine, 2015, 12(12):e1001920. doi: 10.1371/journal.pmed.1001920 URL
[5]	汪天平, 操治国. 中国棘球蚴病防控进展及其存在的问题[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(3):291-296.
[6]	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[J]. Parasit Vectors, 2022, 15(1):109. doi: 10.1186/s13071-022-05197-8
[7]	蒉嫣, 伍卫平, 韩帅, 等. 2018—2019年全国棘球蚴病监测分析[J]. 中国病原生物学杂志, 2021, 16(9):1025-1029.
[8]	王冰洁, 赵莉, 班万里, 等. 细粒棘球绦虫TaqMan实时荧光定量PCR检测方法的建立及应用[J]. 中国人兽共患病学报, 2021, 37(8):678-682,687. doi: 10.3969/j.issn.1002-2694.2021.00.083
[9]	Eckert J, Thompson RCA, 冯振卿. 细粒棘球绦虫的种内变异及对人体的致病性[J]. 国外医学(寄生虫病分册), 1998, 25(2):64-66.
[10]	李维新, 张国才, 林宇光, 等. 多房棘球绦虫在我国自然动物宿主的发现及其形态学研究[J]. 动物学报, 1985, 31(4):365-371.
[11]	曾诚. 青海省青南高原棘球绦虫新种-石渠棘球绦虫的形态学观察[J]. 现代预防医学, 2013, 40(7):1354-1356.
[12]	焦伟, 柴君杰, 伊斯拉音·乌斯曼, 等. 新疆北部骆驼源细粒棘球绦虫发育和形态特征[J]. 中国寄生虫学与寄生虫病杂志, 1998(3):204-208.
[13]	李滨, 杨莲茹, 常建华, 等. 细粒棘球绦虫虫株鉴定与基因型研究进展[J]. 畜牧与饲料科学, 2013, 34(3):87-89.
[14]	吕凤军, 王冰洁, 丁伟强, 等. 线粒体NADH1基因和微卫星标记在棘球绦虫感染检测中的应用[J]. 草食家畜, 2020(4):43-51.
[15]	马学平, 李丽, 秦迎旭, 等. RAPD技术在宁夏人源细粒棘球蚴基因分型中的应用[J]. 中国病原生物学杂志, 2010, 5(1):37-39.
[16]	Basharat N, Ansari SH, Khan J, et al. Characterization of prevalent Echinococcus granulosus genotypes through modified pcr-rflp technique[J]. J Med Sci, 2021, 29(4):286-290.
[17]	Asheri P, Miahipour A, Zibaei M, et al. Determination of Echinococcus granulosus antigen B polymorphism in human and animal isolates from alborz province by PCR-SSCP[J]. Int J Enteric Pathog, 2021, 9(3):90-93. doi: 10.34172/ijep.2021.18 URL
[18]	魏玉环, 胡媛, 曹建平. 细粒棘球绦虫基因多态性的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2019, 37(4):481-485. doi: 10.12140/j.issn.1000-7423.2019.04.019
[19]	Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing[J]. Mol Biochem Parasitol, 1992, 54(2):165-173. doi: 10.1016/0166-6851(92)90109-W URL
[20]	Wu YD, Ren ZR, Li L, et al. Whole-genomic comparison reveals complex population dynamics and parasitic adaptation of Echinococcus granulosus sensu stricto[J]. mBio, 2025, 16(5):e03256-24.
[21]	Guo BP, Zhang ZZ, Zheng XT, et al. Prevalence and molecular characterization of Echinococcus granulosus sensu stricto in northern Xinjiang, China[J]. Korean J Parasitol, 2019, 57(2):153-159. doi: 10.3347/kjp.2019.57.2.153 URL
[22]	高明艳, 葛生虎, 文生萍, 等. 青海西宁地区不同宿主棘球蚴和多头蚴感染情况调查[J]. 中国人兽共患病学报, 2023, 39(4):404-408. doi: 10.3969/j.issn.1002-2694.2023.00.021
[23]	毋德芳, 付永, 任宾, 等. 青海人源两型棘球绦虫(棘球蚴)遗传多样性及分化时间研究[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(5):610-615,621. doi: 10.12140/j.issn.1000-7423.2022.05.007
[24]	Avcioglu H, Guven E, Balkaya I, et al. The situation of echinococcosis in stray dogs in Turkey: the first finding of Echinococcus multilocularis and Echinococcus ortleppi[J]. Parasitology, 2021, 148(9):1092-1098. doi: 10.1017/S0031182021000755 URL
[25]	Citterio CV, Obber F, Trevisiol K, et al. Echinococcus multilocularis and other cestodes in red foxes (Vulpes vulpes) of northeast Italy, 2012-2018[J]. Parasite Vector, 2021, 14(1):29. doi: 10.1186/s13071-020-04520-5
[26]	Saarma U, Jõgisalu I, Moks E, et al. A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence[J]. Parasitology, 2009, 136(3):317-328. doi: 10.1017/S0031182008005453 pmid: 19154654
[27]	Laurimäe T, Kinkar L, Moks E, et al. Molecular phylogeny based on six nuclear genes suggests that Echinococcus granulosus sensu lato genotypes G6/G7 and G8/G10 can be regarded as two distinct species[J]. Parasitology, 2018, 145(14):1929-1937. doi: 10.1017/S0031182018000719 pmid: 29781421
[28]	Marinova I, Spiliotis M, Wang JH, et al. Molecular characterization of Echinococcus granulosus isolates from Bulgarian human cystic echinococcosis patients[J]. Parasitol Res, 2017, 116(3):1043-1054. doi: 10.1007/s00436-017-5386-1 pmid: 28110440
[29]	Knapp J, Bart JM, Giraudoux P, et al. Genetic diversity of the cestode Echinococcus multilocularis in red foxes at a continental scale in Europe[J]. PLoS Negl Trop Dis, 2009, 3(6):e452. doi: 10.1371/journal.pntd.0000452 URL
[30]	Bowles J, McManus DP. NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus[J]. Int J Parasitol, 1993, 23(7):969-972. doi: 10.1016/0020-7519(93)90065-7 pmid: 8106191
[31]	Bowles J, Blair D, McManus DP. A molecular phylogeny of the genus Echinococcus[J]. Parasitology, 1995, 110 (Pt 3):317-328. doi: 10.1017/S0031182000080902 URL
[32]	Bowles J, Blair D, McManus DP. Molecular genetic characterization of the cervid strain ('northern form') of Echinococcus granulosus[J]. Parasitology, 1994, 109 (Pt 2):215-221. doi: 10.1017/S0031182000076332 URL
[33]	Scott JC, Stefaniak J, Pawlowski ZS, et al. Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus[J]. Parasitology, 1997, 114 (Pt 1):37-43. doi: 10.1017/S0031182096008062 URL
[34]	Kedra AH, Swiderski Z, Tkach VV, et al. Genetic analysis of Echinococcus granulosus from humans and pigs in Poland, Slovakia and Ukraine. A multicenter study[J]. Acta Parasitol, 1999, 4(44):248-254.
[35]	Lavikainen A, Lehtinen MJ, Meri T, et al. Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus[J]. Parasitology, 2003, 127(Pt 3):207-215. doi: 10.1017/s0031182003003780 pmid: 12964823
[36]	Casulli A, Siles-Lucas M, Tamarozzi F. Echinococcus granulosus sensu lato[J]. Trends Parasitol, 2019, 35(8):663-664. doi: 10.1016/j.pt.2019.05.006 URL
[37]	Kinkar L, Laurimäe T, Sharbatkhori M, et al. New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto[J]. Infect Genet Evol, 2017,52:52-58.
[38]	Laurimäe T, Kinkar L, Andresiuk V, et al. Genetic diversity and phylogeography of highly zoonotic Echinococcus granulosus genotype G1 in the Americas (Argentina, Brazil, Chile and Mexico) based on 8279bp of mtDNA[J]. Infect Genet Evol, 2016,45:290-296.
[39]	Alvarez Rojas CA, Romig T, Lightowlers MW. Echinococcus granulosus sensu lato genotypes infecting humans-review of current knowledge[J]. Int J Parasitol, 2014, 44(1):9-18. doi: 10.1016/j.ijpara.2013.08.008 URL
[40]	Rausch RL. A consideration of infraspecific categories in the genus Echinococcus Rudolphi, 1801 (Cestoda: Taeniidae)[J]. J Parasitol, 1967, 53(3):484-491. pmid: 6026838
[41]	Nakao M, Xiao N, Okamoto M, et al. Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis[J]. Parasitol Int, 2009, 58(4):384-389. doi: 10.1016/j.parint.2009.07.010 URL
[42]	Robbins WT, Galeuzzi O, Graham K, et al. Echinococcus multilocularis infection in a red fox (Vulpes vulpes) on Prince Edward Island, Canada[J]. Can Vet J, 2022, 63(9):962-966.
[43]	Deplazes P, Rinaldi L, Alvarez Rojas CA, et al. Global distribution of alveolar and cystic echinococcosis[J]. Adv Parasitol, 2017,95:315-493.
[44]	Dakkak A. Echinococcosis/hydatidosis: a severe threat in Mediterranean countries[J]. Vet Parasitol, 2010, 174(1/2):2-11. doi: 10.1016/j.vetpar.2010.08.009 URL
[45]	Hua RQ, Du XD, He X, et al. Genetic diversity of Echinococcus granulosus sensu lato in China: Epidemiological studies and systematic review[J]. Transbound Emerg Dis, 2022, 69(5):e1382-e1392.
[46]	Wang X, Xiao ZJ, Xue CZ, et al. Clinical confirmation of an infection with Echinococcus multilocularis (Mongolian genotype): first case report of human alveolar echinococcosis in Inner Mongolia,China[J]. Infect Dis Poverty, 2025, 14(1):74. doi: 10.1186/s40249-025-01342-4
[47]	Konyaev SV, Yanagida T, Nakao M, et al. Genetic diversity of Echinococcus spp. in Russia[J]. Parasitology, 2013, 140(13):1637-1647. doi: 10.1017/S0031182013001340 pmid: 23985385
[48]	Alvarez Rojas CA, Kronenberg PA, Aitbaev S, et al. Genetic diversity of Echinococcus multilocularis and Echinococcus granulosus sensu lato in Kyrgyzstan: The A2 haplotype of E.multilocularis is the predominant variant infecting humans[J]. PLoS Negl Trop Dis, 2020, 14(5):e0008242. doi: 10.1371/journal.pntd.0008242 URL
[49]	Ito A, Budke CM. The present situation of echinococcoses in Mongolia[J]. J Helminthol, 2015, 89(6):680-688. doi: 10.1017/S0022149X15000620 pmid: 26234999
[50]	Beigh A, Darzi M, Bashir S, et al. Epidemiological and molecular characterization of Echinococcus granulosus isolated from small ruminants in Kashmir valley, India[J]. Iran J Parasitol, 2021, 16(3):357-365.
[51]	Umhang G, Richomme C, Bastid V, et al. National survey and molecular diagnosis of Echinococcus granulosus sensu lato in livestock in France, 2012[J]. Parasitology, 2020, 147(6):667-672. doi: 10.1017/S0031182020000190 URL
[52]	Bohard L, Lallemand S, Borne R, et al. Complete mitochondrial exploration of Echinococcus multilocularis from French alveolar echinococcosis patients[J]. Int J Parasitol, 2023, 53(10):555-564. doi: 10.1016/j.ijpara.2023.03.006 pmid: 37148987
[53]	Bonelli P, Serra E, Dei Giudici S, et al. Molecular phylogenetic analysis of Echinococcus granulosus sensu lato infecting sheep in Italy[J]. Acta Trop, 2024,252:107151.
[54]	Cafiero S A, Rossi C, Cenni L, et al. The Echinococcus multilocularis cycle: first detection of intermediate host in a highly endemic region of Northeastern Italy[J]. Ann Parasitol, 2024,70:105-106.
[55]	Sałamatin R, Kowal J, Nosal P, et al. Cystic echinococcosis in Poland: genetic variability and the first record of Echinococcus granulosus sensu stricto (G1 genotype) in the country[J]. Parasitol Res, 2017, 116(11):3077-3085. doi: 10.1007/s00436-017-5618-4 pmid: 28975403
[56]	Karamon J, Samorek-Pieróg M, Sroka J, et al. The first record of Echinococcus ortleppi (G5) tapeworms in grey wolf (Canis lupus)[J]. Pathogens, 2021, 10(7):853. doi: 10.3390/pathogens10070853 URL
[57]	Karamon J, Stojecki K, Samorek-Pieróg M, et al. Genetic diversity of Echinococcus multilocularis in red foxes in Poland: the first report of a haplotype of probable Asian origin[J]. Folia Parasitol, 2017,64:2017.007.
[58]	Halapy J, Šnábel V, Antolová D, et al. Echinococcus granulosus sensu lato in grey wolves (Canis lupus) population in Slovakia-epidemiology and genetic analysis[J]. Sci Rep, 2025,15:22590.
[59]	Laurimaa L, Süld K, Moks E, et al. First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia,and comparisons with other countries in Europe[J]. Vet Parasitol, 2015, 212(3/4):200-205. doi: 10.1016/j.vetpar.2015.06.004 URL
[60]	Antolová D, Šnábel V, Jarošová J, et al. Human alveolar echinococcosis in Slovakia: Epidemiology and genetic diversity of Echinococcus multilocularis,2000-2023[J]. PLoS Negl Trop Dis, 2024, 18(1):e0011876. doi: 10.1371/journal.pntd.0011876 URL
[61]	Šnábel V, Kuzmina TA, Antipov AA, et al. Molecular study of Echinococcus granulosus cestodes in Ukraine and the first genetic identification of Echinococcus granulosus sensu stricto (G1 genotype)in the country[J]. Acta Parasitol, 2022, 67(1):244-254. doi: 10.1007/s11686-021-00450-z
[62]	Tahiri S, Naoui H, Iken M, et al. Genotyping of human Echinococcus granulosus cyst in Morocco[J]. J Parasit Dis, 2019, 43(4):560-565. doi: 10.1007/s12639-019-01127-1
[63]	Boufana B, Lahmar S, Rebaï W, et al. Genetic variability and haplotypes of Echinococcus isolates from Tunisia[J]. Trans R Soc Trop Med Hyg, 2014, 108(11):706-714. doi: 10.1093/trstmh/tru138 URL
[64]	Aregawi WG, Levecke B, Ashenafi H, et al. Epidemiology of Echinococcus granulosus sensu lato in the Greater Horn of Africa: a systematic review[J]. PLoS Negl Trop Dis, 2024, 18(1):e0011894. doi: 10.1371/journal.pntd.0011894 URL
[65]	Schurer JM, Bouchard E, Bryant A, et al. Echinococcus in wild canids in québec (Canada) and Maine (USA)[J]. PLoS Negl Trop Dis, 2018, 12(8):e0006712. doi: 10.1371/journal.pntd.0006712 URL
[66]	Jenkins EJ, Peregrine AS, Hill JE, et al. Detection of European strain of Echinococcus multilocularis in North America[J]. Emerg Infect Dis, 2012, 18(6):1010-1012. doi: 10.3201/eid1806.111420 pmid: 22608114
[67]	Jesudoss Chelladurai JRJ, Quintana TA, Johnson WL, et al. Cystic echinococcosis in cattle and sheep caused by Echinococcus granulosus sensu stricto genotypes G1 and G3 in the USA[J]. Parasit Vectors, 2024, 17(1):128. doi: 10.1186/s13071-024-06192-x pmid: 38486339
[68]	Rodriguez-Prado U, Jimenez-Gonzalez DE, Avila G, et al. Short report: Genetic variation of Echinococcus canadensis (G7) in Mexico[J]. Am J Trop Med Hyg, 2014, 91(6):1149-1153. doi: 10.4269/ajtmh.14-0317 URL
[69]	Debiaggi MF, Soriano SV, Pierangeli NB, et al. Genetic characterization of human hydatid cysts shows coinfection by Echinococcus canadensis G7 and Echinococcus granulosus sensu stricto G1 in Argentina[J]. Parasitol Res, 2017, 116(9):2599-2604. doi: 10.1007/s00436-017-5555-2 URL
[70]	Das Neves LB, Dias-Correia TP, Bittencourt-Oliveira F, et al. Human cystic echinococcosis: first molecular identification of Echinococcus canadensis G7 in Brazil[J]. Parasitol Res, 2024, 123(6):239. doi: 10.1007/s00436-024-08262-6

地区	国家	细粒棘球绦虫基因型	多房棘球绦虫基因型	地区	国家	细粒棘球绦虫基因型	多房棘球绦虫基因型
亚洲	中国	G1、G3、G5、G6、G7、G8、G10^[45]	亚洲型、蒙古型^[46]		波兰	G1、G5、G7^[55-56]	亚洲型、欧洲型^[57]
亚洲	中国	G1、G3、G5、G6、G7、G8、G10^[45]	亚洲型、蒙古型^[46]		爱沙尼亚	G1、G8、G10^[58]	欧洲型^[59]
	俄罗斯	G1、G3、G6、G8、G10^[47]	亚洲型、蒙古型、欧洲型、北美洲型^[47]		斯洛伐克	G1、G3、G7、G8^[58]	欧洲型^[60]
	俄罗斯	G1、G3、G6、G8、G10^[47]	亚洲型、蒙古型、欧洲型、北美洲型^[47]		乌克兰	G1、G7^[61]
	吉尔吉斯斯坦	G1、G3、G4、G6、G7^[48]	亚洲型^[48]	非洲	摩洛哥	G1、G3^[62]
	吉尔吉斯斯坦	G1、G3、G4、G6、G7^[48]	亚洲型^[48]		突尼斯	G1、G3、G4、G6^[63]
	蒙古	G1、G6、G7、G10^[49]	蒙古型^[41]		苏丹	G1、G5、G6^[64]
	印度	G1、G2、G3、G5、G6^[50]	亚洲型^[41]		肯尼亚	G1、G3、G4、G5、G6、G7^[64]
	日本	G1^[18]	亚洲型^[41]	北美洲	加拿大	G6、G8、G10^[65]	北美洲型、欧洲型^[66]
欧洲	法国	G1、G3、G5、G6、G7^[51]	欧洲型^[52]		美国	G1、G3、G8、G10^[67]	亚洲型、北美洲型^[41]
					墨西哥	G1、G5、G7、G8^[68]
				南美洲	阿根廷	G1、G3、G5、G6、G7^[69]
	意大利	G1、G3、G4、G5、G6、G7^[53]	欧洲型^[54]
					巴西	G1、G3、G5、G7^[70]