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Similarities and differences among the Opisthorchiidae liver flukes: insights from Opisthorchis felineus

Published online by Cambridge University Press:  16 May 2022

Maria Y. Pakharukova
Affiliation:
Laboratory of Molecular Mechanisms of Pathological Processes, Institute of Cytology and Genetics (ICG), Siberian Branch of Russian Academy of Sciences (SB RAS), 10 Akad. Lavrentieva Ave., Novosibirsk 630090, Russia Department of Natural Sciences, Novosibirsk State University, 2 Pirogova Str., Novosibirsk 630090, Russia
Viatcheslav A. Mordvinov*
Affiliation:
Laboratory of Molecular Mechanisms of Pathological Processes, Institute of Cytology and Genetics (ICG), Siberian Branch of Russian Academy of Sciences (SB RAS), 10 Akad. Lavrentieva Ave., Novosibirsk 630090, Russia
*
Author for correspondence: Viatcheslav A. Mordvinov, E-mail: [email protected]

Abstract

The foodborne liver trematode Opisthorchis felineus (Rivolta, 1884) is a member of the triad of phylogenetically related epidemiologically important Opisthorchiidae trematodes, which also includes O. viverrini (Poirier, 1886) and Clonorchis sinensis (Loos, 1907). Despite similarity in the life cycle, Opisthorchiidae liver flukes also have marked differences. Two species (O. viverrini and C. sinensis) are recognized as Group 1A biological carcinogens, whereas O. felineus belongs to Group 3A. In this review, we focus on these questions: Are there actual differences in carcinogenicity among these 3 liver fluke species? Is there an explanation for these differences? We provide a recent update of our knowledge on the liver fluke O. felineus and highlight its differences from O. viverrini and C. sinensis. In particular, we concentrate on differences in the climate of endemic areas, characteristics of the life cycle, the range of intermediate hosts, genomic and transcriptomic features of the pathogens, and clinical symptoms and morbidity of the infections in humans. The discussion of these questions can stimulate new developments in comparative studies on the pathogenicity of liver flukes and should help to identify species-specific features of opisthorchiasis and clonorchiasis pathogenesis.

Type
Review Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Arunsan, P, Ittiprasert, W, Smout, MJ, Cochran, CJ, Mann, VH, Chaiyadet, S, Karinshak, SE, Sripa, B, Young, ND, Sotillo, J, Loukas, A, Brindley, PJ and Laha, T (2019) Programmed knockout mutation of liver fluke granulin attenuates virulence of infection-induced hepatobiliary morbidity. Elife 8, e41463.CrossRefGoogle ScholarPubMed
Arunsan, P, Chaidee, A, Cochran, CJ, Mann, VH, Tanno, T, Kumkhaek, C, Smout, MJ, Karinshak, SE, Rodpai, R, Sotillo, J, Loukas, A, Laha, T, Brindley, PJ and Ittiprasert, W (2020) Liver fluke granulin promotes extracellular vesicle-mediated crosstalk and cellular microenvironment conducive to cholangiocarcinoma. Neoplasia 22, 203216.CrossRefGoogle ScholarPubMed
Aunpromma, S, Kanjampa, P, Papirom, P, Tangkawattana, S, Tangkawattana, P, Tesana, S, Boonmars, T, Suwannatrai, A, Uopsai, S, Sukon, P and Sripa, B (2016) Prevalence and risk factors for Opisthorchis viverrini infection among cats and dogs in six districts surrounding the Ubolratana Dam, an endemic area for human opisthorchiasis in northeastern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 47, 11531159.Google Scholar
Bansal, PS, Smout, MJ, Wilson, D, Cobos Caceres, C, Dastpeyman, M, Sotillo, J, Seifert, J, Brindley, PJ, Loukas, A and Daly, NL (2017) Development of a potent wound healing agent based on the liver fluke granulin structural fold. Journal of Medicinal Chemistry 60, 42584266.CrossRefGoogle ScholarPubMed
Bateman, A, Cheung, ST and Bennett, HPJ (2018) A brief overview of progranulin in health and disease. Methods in Molecular Biology 1806, 315.CrossRefGoogle ScholarPubMed
Beer, SA (2005) The Biology of Opisthorchiasis Agent. Moscow, Russia: KMK Scientific Press Ltd (in Russian).Google Scholar
Boonmars, T, Wu, Z, Boonjaruspinyo, S, Pinlaor, S, Nagano, I, Takahashi, Y, Kaewsamut, B and Yongvanit, P (2009) Alterations of gene expression of RB pathway in Opisthorchis viverrini infection-induced cholangiocarcinoma. Parasitology Research 105, 12731281.CrossRefGoogle ScholarPubMed
Braga, TT, Agudelo, JS and Camara, NO (2015) Macrophages during the fibrotic process: M2 as friend and foe. Frontiers in Immunology 6, 602.CrossRefGoogle ScholarPubMed
Brazhnikova, NA and Tolkaeva, MV (2002) Cancer of liver, biliary tracts and pancreas at chronic opisthorchiasis. Bulletin of Siberian Medicine 2, 7177 (in Russian).CrossRefGoogle Scholar
Brazhnikova, NA and Tskhai, VF (2004) Clinical Features, Diagnosis and management of the complicated opistorchiasis. Annaly khirurgicheskoy gepatologii (Annals of Surgical Hepatology, Mosk) 9, 9299. (in Russian).Google Scholar
Bronshtein, AM, Zolotukhin, VA, Gitsu, GA, Sabgaida, TP and Parfenov, SB (1991) The clinico-epidemiological characteristics of opisthorchiasis foci in the Yamalo-Nenets Autonomous Okrug and the treatment results with praziquantel. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 5, 1216 (in Russian).Google Scholar
Brusentsov, II, Katokhin, AV, Brusentsova, IV, Shekhovtsov, SV, Borovikov, SN, Goncharenko, GG, Lider, LA, Romashov, BV, Rusinek, OT, Shibitov, SK, Suleymanov, MM, Yevtushenko, AV and Mordvinov, VA (2013) Low genetic diversity in wide-spread Eurasian liver fluke Opisthorchis felineus suggests special demographic history of this trematode species. PLoS ONE 8, e62453.CrossRefGoogle ScholarPubMed
Cai, XQ, Liu, GH, Song, HQ, Wu, CY, Zou, FC, Yan, HK, Yuan, ZG, Lin, RQ and Zhu, XQ (2012) Sequences and gene organization of the mitochondrial genomes of the liver flukes Opisthorchis viverrini and Clonorchis sinensis (Trematoda). Parasitology Research 110, 235243.CrossRefGoogle ScholarPubMed
Chaiyadet, S, Sotillo, J, Smout, M, Cantacessi, C, Jones, MK, Johnson, MS, Turnbull, L, Whitchurch, CB, Potriquet, J, Laohaviroj, M, Mulvenna, J, Brindley, PJ, Bethony, JM, Laha, T, Sripa, B and Loukas, A (2015) Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype. Journal of Infectious Diseases 212, 16361645.CrossRefGoogle ScholarPubMed
Chalmers, IW and Hoffmann, KF (2012) Platyhelminth venom allergen-like (VAL) proteins: revealing structural diversity, class-specific features and biological associations across the phylum. Parasitology 139, 12311245.CrossRefGoogle ScholarPubMed
Chemich, ND, Ilina, VV, Ilina, NI and Sholohova, SE (2014) The problem of opisthorchiasis in Ukraine and modern approaches to treatment. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 1, 4548 (in Russian).Google Scholar
Chen, Y, Wen, T, Lai, DH, Wen, YZ, Wu, ZD, Yang, TB, Yu, XB, Hide, G and Lun, ZR (2013) Development and evaluation of loop-mediated isothermal amplification (LAMP) for rapid detection of Clonorchis sinensis from its first intermediate hosts, freshwater snails. Parasitology 140, 13771383.CrossRefGoogle ScholarPubMed
Chng, KR, Chan, SH, Ng, AHQ, Li, C, Jusakul, A, Bertrand, D, Wilm, A, Choo, SP, Tan, DMY, Lim, KH, Soetinko, R, Ong, CK, Duda, DG, Dima, S, Popescu, I, Wongkham, C, Feng, Z, Yeoh, KG, Teh, BT, Yongvanit, P, Wongkham, S, Bhudhisawasdi, V, Khuntikeo, N, Tan, P, Pairojkul, C, Ngeow, J and Nagarajan, N (2016) Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma. EBioMedicine 8, 195202.CrossRefGoogle ScholarPubMed
Choi, DW (1984) Clonorchis sinensis: life cycle, intermediate hosts, transmission to man and geographical distribution in Korea. Arzneimittel-Forschung 34, 11451151.Google Scholar
Choi, D, Lim, JH, Lee, KT, Lee, JK, Choi, SH, Heo, JS, Jang, KT, Lee, NY, Kim, S and Hong, ST (2006) Cholangiocarcinoma and Clonorchis sinensis infection: a case–control study in Korea. Journal of Hepatology 44, 10661073.CrossRefGoogle ScholarPubMed
Choi, D, Lim, JH, Lee, KT, Lee, JK, Choi, SH, Heo, JS, Choi, DW, Jang, KT, Lee, NY, Kim, S and Hong, ST (2008) Gallstones and Clonorchis sinensis infection: a hospital-based case-control study in Korea. Journal of Gastroenterology and Hepatology 23, e399e404.CrossRefGoogle ScholarPubMed
Chudthaisong, N, Promthet, S and Bradshaw, P (2015) Risk factors for Opisthorchis viverrini infection in Nong Khai Province, Thailand. Asian Pacific Journal of Cancer Prevention: APJCP 16, 45934596.CrossRefGoogle Scholar
Dangtakot, R, Pinlaor, S, Itthitaetrakool, U, Chaidee, A, Chomvarin, C, Sangka, A, Wilailuckana, C and Pinlaor, P (2017) Coinfection with Helicobacter pylori and Opisthorchis viverrini enhances the severity of hepatobiliary abnormalities in hamsters. Infection and Immunity 85, e00009-17.CrossRefGoogle ScholarPubMed
Dastpeyman, M, Bansal, PS, Wilson, D, Sotillo, J, Brindley, PJ, Loukas, A, Smout, MJ and Daly, NL (2018) Structural variants of a liver fluke derived granulin peptide potently stimulate wound healing. Journal of Medicinal Chemistry 61, 87468753.CrossRefGoogle ScholarPubMed
Doanh, PN and Nawa, Y (2016) Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 1320.CrossRefGoogle ScholarPubMed
Drozdov, VI (1972) The survivability of eggs Opisthorchis felineus (Rivolta, 1884) in different environmental conditions. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 31, 323326 (in Russian).Google Scholar
Eom, KS, Park, HS, Lee, D, Sohn, WM, Yong, TS, Chai, JY, Min, DY, Rim, HJ, Insisiengmay, B and Phommasack, B (2015) Infection status of zoonotic trematode metacercariae in fishes from Vientiane municipality and Champasak Province in Lao PDR. Korean Journal of Parasitology 53, 447453.CrossRefGoogle ScholarPubMed
Ershov, NI, Mordvinov, VA, Prokhortchouk, EB, Pakharukova, MY, Gunbin, KV, Ustyantsev, K, Genaev, MA, Blinov, AG, Mazur, A, Boulygina, E, Tsygankova, S, Khrameeva, E, Chekanov, N, Fan, G, Xiao, A, Zhang, H, Xu, X, Yang, H, Solovyev, V, Lee, SM, Liu, X, Afonnikov, DA and Skryabin, KG (2019) New insights from Opisthorchis felineus genome: update on genomics of the epidemiologically important liver flukes. BMC Genomics 20, 399.CrossRefGoogle ScholarPubMed
Fedorov, KP (1979) The Ecology of Liver Flukes in Novosibirsk Oblast, Ecology and Morphology of Helminths in Western Siberia (in Russian). Novosibirsk, Russia: Nauka (in Russian).Google Scholar
Fedorov, KP, Babueva, RV and Karpenko, SV (1989) The role of the owsianka Leucaspius delineatus in maintaining opisthorchiasis foci in Novosibirsk Province. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 6, 6467 (in Russian).Google Scholar
Fedorova, OS, Kovshirina, YV, Kovshirina, AE, Fedotova, MM, Deev, IA, Petrovsky, FI, Filimonov, AV, Dmitrieva, AI, Kudyakov, LA, Saltykova, IV, Mikhalev, EV, Odermatt, P and Ogorodova, LM (2016) Analysis of the incidence of Opisthorchis felineus invasion and malignant neoplasms of the hepatobiliary system in the Russian Federation. Bulletin of Siberian Medicine 15, 147158 (in Russian).CrossRefGoogle Scholar
Fedorova, OS, Fedotova, MM, Zvonareva, OI, Mazeina, SV, Kovshirina, YV, Sokolova, TS, Golovach, EA, Kovshirina, AE, Konovalova, UV, Kolomeets, IL, Gutor, SS, Petrov, VA, Hattendorf, J, Ogorodova, LM and Odermatt, P (2020) Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Neglected Tropical Diseases 14, e0008421.CrossRefGoogle ScholarPubMed
Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO) (2014) ‘Top Ten’ List of Food-Borne Parasites Released (Internet). Geneva, Switzerland: World Health Organization. Available at http://www.fao.org/news/story/en/item/237323/icode/ (Accessed 24 December 2021).Google Scholar
Gibbs, GM, Roelants, K and O'Bryan, MK (2008) The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins—roles in reproduction, cancer, and immune defense. Endocrine Reviews 29, 865897.CrossRefGoogle ScholarPubMed
Gosudarstvennyj Doklad (The State Report). On the state sanitary and epidemiological welfare of the population in the Russian Federation in 2013. 2014. 1191. Moscow: Federal Service for Supervision of Consumer Rights Protection and Human Welfare; Rospotrebnadzor. Editor: Popova A.Y. Available at http://www.rospotrebnadzor.ru/upload/iblock/3b8/gd_2013_dlya-sayta.pdf.Google Scholar
Gouveia, MJ, Pakharukova, MY, Laha, T, Sripa, B, Maksimova, GA, Rinaldi, G, Brindley, PJ, Mordvinov, VA, Amaro, T, Santos, LL, Correia da Costa, JM and Vale, N (2017) Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model. Carcinogenesis 38, 929937.CrossRefGoogle Scholar
Gouveia, MJ, Pakharukova, MY, Rinaldi, G, Mordvinov, VA, Brindley, PJ, Gärtner, F and Vale, N (2020) Helminth infection-induced carcinogenesis: spectrometric insights from the liver flukes, Opisthorchis and Fasciola. Experimental Results 1, E40.CrossRefGoogle Scholar
Harinasuta, C and Harinasuta, T (1984) Opisthorchis viverrini: life cycle, intermediate hosts, transmission to man and geographical distribution in Thailand. Arzneimittel-Forschung 34, 11641167.Google Scholar
Harinasuta, T, Riganti, M and Bunnag, D (1984) Opisthorchis viverrini infection: pathogenesis and clinical features. Arzneimittel-Forschung 34, 11671169.Google ScholarPubMed
Haugen, B, Karinshak, SE, Mann, VH, Popratiloff, A, Loukas, A, Brindley, PJ and Smout, MJ (2018) Granulin secreted by the food-borne liver fluke Opisthorchis viverrini promotes angiogenesis in human endothelial cells. Frontiers in Medicine 5, 30.CrossRefGoogle ScholarPubMed
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. A review of human carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 100, 1441.Google Scholar
Ip, M, Leung, N and Cheng, AF (1995) Acute clonorchiasis. Scandinavian Journal of Infectious Diseases 27, 645646.CrossRefGoogle ScholarPubMed
Ju, JW, Joo, HN, Lee, MR, Cho, SH, Cheun, HI, Kim, JY, Lee, YH, Lee, KJ, Sohn, WM, Kim, DM, Kim, IC, Park, BC and Kim, TS (2009) Identification of a serodiagnostic antigen, legumain, by immunoproteomic analysis of excretory-secretory products of Clonorchis sinensis adult worms. Proteomics 9, 30663078.CrossRefGoogle ScholarPubMed
Jung, KW, Won, YJ, Kong, HJ and Lee, ES (2019) Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2016. Cancer Research and Treatment 51, 417430.CrossRefGoogle ScholarPubMed
Kanunnikova, EA and Solovyh, GM (2007) Typification of foci of opisthorchiasis in the Orenburg region. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 3, 1114 (in Russian).Google Scholar
Kaprin, AD, Starinskiy, VV and Petrova, GV (2013) Zlokachestvennye novoobrazovaniya v Rossii v 2013 godu (Malignancies in Russia in 2012). In P. Herzen Moscow Oncology Research Institute. Editor: Starinskiy VV. Moscow, Russia: Healthcare Ministry Publications, pp. 1232.Google Scholar
Kim, EM, Bae, YM, Choi, MH and Hong, ST (2012) Cyst formation, increased anti-inflammatory cytokines and expression of chemokines support for Clonorchis sinensis infection in FVB mice. Parasitology International 61, 124129.CrossRefGoogle ScholarPubMed
Kovner, AV, Pakharukova, MY, Maksimova, GA and Mordvinov, VA (2019) Characteristics of liver fibrosis associated with chronic Opisthorchis felineus infection in Syrian hamsters and humans. Experimental and Molecular Pathology 110, 104274.CrossRefGoogle ScholarPubMed
Kovshirina, YV, Fedorova, OS, Vtorushin, SV, Kovshirina, AE, Ivanov, SD, Chizhikov, AV, Onishchenko, SV, Ogorodova, LM and Odermatt, P (2019) Case report: two cases of cholangiocarcinoma in patients with Opisthorchis felineus infection in Western Siberia, Russian Federation. American Journal of Tropical Medicine and Hygiene 100, 599603.CrossRefGoogle ScholarPubMed
Kurathong, S, Lerdverasirikul, P, Wongpaitoon, V, Pramoolsinsap, C, Kanjanapitak, A, Varavithya, W, Phuapradit, P, Bunyaratvej, S, Upatham, ES and Brockelman, WY (1985) Opisthorchis viverrini infection and cholangiocarcinoma. A prospective, case-controlled study. Gastroenterology 89, 151156.CrossRefGoogle ScholarPubMed
Laoprom, N, Sithithaworn, P, Ando, K, Sithithaworn, J, Wongkham, S, Laha, T, Klinbunga, S, Webster, JP and Andrews, RH (2010) Microsatellite loci in the carcinogenic liver fluke, Opisthorchis viverrini and their application as population genetic markers. Infection Genetics and Evolution 10, 146153.CrossRefGoogle ScholarPubMed
Laoprom, N, Sithithaworn, P, Andrews, RH, Ando, K, Laha, T, Klinbunga, S, Webster, JP and Petney, TN (2012) Population genetic structuring in Opisthorchis viverrini over various spatial scales in Thailand and Lao PDR. PLoS Neglected Tropical Diseases 6, e1906.CrossRefGoogle ScholarPubMed
Lee, MR, Yoo, WG, Kim, YJ, Chung, EJ, Cho, SH and Ju, JW (2018) Venom allergen-like protein 28 in Clonorchis sinensis: four epitopes on its surface and the potential role of Cys124 for its conformational stability. Parasitology Research 117, 25212530.CrossRefGoogle ScholarPubMed
Liang, C, Hu, XC, Lv, ZY, Wu, ZD, Yu, XB, Xu, J and Zheng, HQ (2009) (Experimental establishment of life cycle of Clonorchis sinensis). Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27, 148150 (in Chinese).Google ScholarPubMed
Lun, ZR, Gasser, RB, Lai, DH, Li, AX, Zhu, XQ, Yu, XB and Fang, YY (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infectious Diseases 5, 3141.CrossRefGoogle ScholarPubMed
L'vova, MN, Duzhak, TG, Tsentalovich, I, Katokhin, AV and Mordvinov, VA (2014) (Secretome of the adult liver fluke Opisthorchis felineus). Parazitologiia 48, 169184 (in Russian).Google ScholarPubMed
Lvova, MN, Tangkawattana, S, Balthaisong, S, Katokhin, AV, Mordvinov, VA and Sripa, B (2012) Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitology International 61, 167172.CrossRefGoogle Scholar
Lvova, M, Zhukova, M, Kiseleva, E, Mayboroda, O, Hensbergen, P, Kizilova, E, Ogienko, A, Besprozvannykh, V, Sripa, B, Katokhin, A and Mordvinov, V (2016) Hemozoin is a product of heme detoxification in the gut of the most medically important species of the family Opisthorchiidae. International Journal for Parasitology 46, 147156.CrossRefGoogle ScholarPubMed
Maeng, S, Lee, HW, Bashir, Q, Kim, TI, Hong, SJ, Lee, TJ, Sohn, WM, Na, BK, Kim, TS and Pak, JH (2016) Oxidative stress-mediated mouse liver lesions caused by Clonorchis sinensis infection. International Journal for Parasitology 46, 195204.CrossRefGoogle ScholarPubMed
Mairiang, E, Chaiyakum, J, Chamadol, N, Laopaiboon, V, Srinakarin, J, Kunpitaya, J, Sriamporn, S, Suwanrungruang, K and Vatanasapt, V (2006) Ultrasound screening for Opisthorchis viverrini-associated cholangiocarcinomas: experience in an endemic area. Asian Pacific Journal of Cancer Prevention 7, 431433.Google Scholar
Maksimova, GA, Pakharukova, MY, Kashina, EV, Zhukova, NA, Kovner, AV, Lvova, MN, Katokhin, AV, Tolstikova, TG, Sripa, B and Mordvinov, VA (2017) Effect of Opisthorchis felineus infection and dimethylnitrosamine administration on the induction of cholangiocarcinoma in Syrian hamsters. Parasitology International 66, 458463.CrossRefGoogle ScholarPubMed
Mordvinov, VA and Furman, DP (2010) The Digenea parasite Opisthorchis felineus: a target for the discovery and development of novel drugs. Infectious Disorders – Drug Targets 10, 385401.CrossRefGoogle ScholarPubMed
Mordvinov, VA, Ershov, NI, Pirozhkova, DS, Pakharukov, YV and Pakharukova, MY (2017 a) ABC transporters in the liver fluke Opisthorchis felineus. Molecular and Biochemical Parasitology 216, 6068.CrossRefGoogle ScholarPubMed
Mordvinov, VA, Shilov, AG and Pakharukova, MY (2017 b) Anthelmintic activity of cytochrome P450 inhibitors miconazole and clotrimazole: in-vitro effect on the liver fluke Opisthorchis felineus. International Journal of Antimicrobial Agents 50, 97100.CrossRefGoogle ScholarPubMed
Mordvinov, VA, Minkova, GA, Kovner, AV, Ponomarev, DV, Lvova, MN, Zaparina, O, Romanenko, SA, Shilov, AG and Pakharukova, MY (2021) A tumorigenic cell line derived from a hamster cholangiocarcinoma associated with Opisthorchis felineus liver fluke infection. Life Sciences 20, 119494.CrossRefGoogle Scholar
Mulvenna, J, Sripa, B, Brindley, PJ, Gorman, J, Jones, MK, Colgrave, ML, Jones, A, Nawaratna, S, Laha, T, Suttiprapa, S, Smout, MJ and Loukas, A (2010) The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics 10, 10631078.CrossRefGoogle ScholarPubMed
Na, BK, Pak, JH and Hong, SJ (2020) Clonorchis sinensis and clonorchiasis. Acta Tropica 203, 105309.CrossRefGoogle ScholarPubMed
Nishiura, H, Tsunoda, T and Akao, N (2003) (A case of severe eosinophilia in the acute phase of Opisthorchis viverrini infection). Kansenshogaku Zasshi 77, 677681 (in Japanese).CrossRefGoogle ScholarPubMed
Nugaraitė, D, Mažeika, V and Paulauskas, A (2019) Helminths of mustelids with overlapping ecological niches: Eurasian otter Lutra lutra (Linnaeus, 1758), American mink Neovison vison Schreber, 1777, and European polecat Mustela putorius Linnaeus, 1758. Helminthologia 56, 6674.CrossRefGoogle ScholarPubMed
Ovchinnikov, VY, Afonnikov, DA, Vasiliev, GV, Kashina, EV, Sripa, B, Mordvinov, VA and Katokhin, AV (2015) Identification of microRNA genes in three opisthorchiids. PLoS Neglected Tropical Diseases 9, e0003680.CrossRefGoogle ScholarPubMed
Pak, JH, Son, WC, Seo, SB, Hong, SJ, Sohn, WM, Na, BK and Kim, TS (2016) Peroxiredoxin 6 expression is inversely correlated with nuclear factor-κB activation during Clonorchis sinensis infestation. Free Radical Biology and Medicine 99, 273285.CrossRefGoogle ScholarPubMed
Pakharukova, MY and Mordvinov, VA (2016) The liver fluke Opisthorchis felineus: biology, epidemiology, and carcinogenic potential. Transactions of the Royal Society of Tropical Medicine and Hygiene 110, 2836.CrossRefGoogle ScholarPubMed
Pakharukova, MY, Vavilin, VA, Sripa, B, Laha, T, Brindley, PJ and Mordvinov, VA (2015) Functional analysis of the unique cytochrome P450 of the liver fluke Opisthorchis felineus. PLoS Neglected Tropical Diseases 9, e0004258.CrossRefGoogle ScholarPubMed
Pakharukova, MY, Pakharukov, YV and Mordvinov, VA (2018) Effects of miconazole/clotrimazole and praziquantel combinations against the liver fluke Opisthorchis felineus in vivo and in vitro. Parasitology Research 117, 23272331.CrossRefGoogle ScholarPubMed
Pakharukova, MY, Samsonov, VA, Serbina, EA and Mordvinov, VA (2019 a) A study of tribendimidine effects in vitro and in vivo on the liver fluke Opisthorchis felineus. Parasites & Vectors 12, 23.CrossRefGoogle ScholarPubMed
Pakharukova, MY, Zaparina, OG, Kapushchak, YK, Baginskaya, NV and Mordvinov, VA (2019 b) Opisthorchis felineus infection provokes time-dependent accumulation of oxidative hepatobiliary lesions in the injured hamster liver. PLoS ONE 14, e0216757.CrossRefGoogle ScholarPubMed
Pakharukova, MY, Zaparina, OG, Kovner, AV and Mordvinov, VA (2019 c) Inhibition of Opisthorchis felineus glutathione-dependent prostaglandin synthase by resveratrol correlates with attenuation of cholangiocyte neoplasia in a hamster model of opisthorchiasis. International Journal for Parasitology 49, 963973.CrossRefGoogle Scholar
Pakharukova, MY, Zaparina, O, Hong, SJ, Sripa, B and Mordvinov, VA (2021) A comparative study of Helicobacter pylori infection in hamsters experimentally infected with liver flukes Opisthorchis felineus, Opisthorchis viverrini, or Clonorchis sinensis. Scientific Reports 11, 7789.CrossRefGoogle ScholarPubMed
Park, GM, Im, K, Huh, S and Yong, TS (2000) Chromosomes of the liver fluke, Clonorchis sinensis. Korean Journal of Parasitology 38, 201206.CrossRefGoogle ScholarPubMed
Park, DS, Na, SJ, Cho, SH, June, KJ, Cho, YC and Lee, YH (2014) Prevalence and risk factors of clonorchiasis among residents of riverside areas in Muju-gun, Jeollabuk-do, Korea. Korean Journal of Parasitology 52, 391397.CrossRefGoogle ScholarPubMed
Pelgunov, AN, Kazakov, BE, Fedorov, KP, Bocharova, TM and Sous, SM (2006) Parasitic fauna in the fish of the Ob River basin. In Pavlov, DS and Mochek, AD (eds), Fish Ecology in the Ob–Irtysh River Basin. Moscow, Russia: KMK, pp. 410476 (in Russian).Google Scholar
Petney, TN, Andrews, RH, Saijuntha, W, Wenz-Mücke, A and Sithithaworn, P (2013) The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini. International Journal for Parasitology 43, 10311046.CrossRefGoogle ScholarPubMed
Petney, TN, Andrews, RH, Saijuntha, W, Tesana, S, Prasopdee, S, Kiatsopit, N and Sithithaworn, P (2018) Taxonomy, ecology and population genetics of Opisthorchis viverrini and its intermediate hosts. Advances in Parasitology 101, 139.CrossRefGoogle ScholarPubMed
Petrenko, VA, Pakharukova, MY, Kovner, AV, Lvova, MN, Lyakhovich, VV and Mordvinov, VA (2017) Secretion of thioredoxin peroxidase protein of cat liver fluke Opisthorchis felineus during modeling of experimental opisthorchiasis. Bulletin of Experimental Biology and Medicine 162, 773776.CrossRefGoogle ScholarPubMed
Petrova, GV, Starinskiy, VV, Gretsova, OP, Shahzadova, AO and Samsonov, YV (2019) Cancer care to the population of Russia in 2017 according to the data of federal statistical observation. Oncology. Journal Them. P.A. Hercena 1, 3240. https://doi.org/10.17116/onkolog2019801132.Google Scholar
Pitaksakulrat, O, Webster, BL, Webster, JP, Laha, T, Saijuntha, W, Lamberton, PHL, Kiatsopit, N, Andrews, RH, Petney, TN and Sithithaworn, P (2018) Phylogenetic relationships within the Opisthorchis viverrini species complex with specific analysis of O. viverrini sensu lato from Sakon Nakhon, Thailand by mitochondrial and nuclear DNA sequencing. Infection Genetics and Evolution 62, 8694.CrossRefGoogle Scholar
Pomaznoy, MY, Logacheva, MD, Young, ND, Penin, AA, Ershov, NI, Katokhin, AV and Mordvinov, VA (2016) Whole transcriptome profiling of adult and infective stages of the trematode Opisthorchis felineus. Parasitology International 65, 1219.CrossRefGoogle ScholarPubMed
Pozio, E, Armignacco, O, Ferri, F and Gomez Morales, MA (2013) Opisthorchis felineus, an emerging infection in Italy and its implication for the European Union. Acta Tropica 126, 5462.CrossRefGoogle ScholarPubMed
Prakobwong, S, Pinlaor, S, Yongvanit, P, Sithithaworn, P, Pairojkul, C and Hiraku, Y (2009) Time profiles of the expression of metalloproteinases, tissue inhibitors of metalloproteases, cytokines and collagens in hamsters infected with Opisthorchis viverrini with special reference to peribiliary fibrosis and liver injury. International Journal for Parasitology 39, 825835.CrossRefGoogle ScholarPubMed
Prasopdee, S, Kulsantiwong, J, Piratae, S, Khampoosa, P, Thammasiri, C, Suwannatrai, A, Laha, T, Grams, R, Loukas, A and Tesana, S (2015) Temperature dependence of Opisthorchis viverrini infection in first intermediate host snail, Bithynia siamensis goniomphalos. Acta Tropica 141, 112117.CrossRefGoogle ScholarPubMed
Rim, HJ (2005) Clonorchiasis: an update. Journal of Helminthology 79, 269281.CrossRefGoogle ScholarPubMed
Safiullin, RT and Shibitov, SK (2012) Opisthorchiasis of carnivores. Veterinary Medicine 12, 3033 (in Russian).Google Scholar
Saijuntha, W, Andrews, RH, Sithithaworn, P and Petney, TN (2022) Current assessment of the systematics and population genetics of Opisthorchis viverrini sensu lato (Trematoda: Opisthorchiidae) and its first intermediate host Bithynia siamensis sensu lato (Gastropoda: Bithyniidae) in Thailand and Southeast Asia. Infection Genetics and Evolution 97, 105182.CrossRefGoogle ScholarPubMed
Scaramozzino, P, Condoleo, R, Martini, E, Bossu, T, Aquilani, S, Spallucci, V, Aquilini, E and Marozzi, S (2018) Behaviour and eating habits as determinants for human opisthorchiasis in the Bolsena Lake area, Italy. Folia Parasitologica 65, 2018.013.CrossRefGoogle ScholarPubMed
Schuster, RK (2010) Opisthorchiidosis – a review. Infectious Disorders – Drug Targets 10, 402415.CrossRefGoogle ScholarPubMed
Schuster, RK, Specht, P and Rieger, S (2021) On the helminth fauna of the muskrat (Ondatra zibethicus (Linnaeus, 1766)) in the Barnim District of Brandenburg State/Germany. Animals 11, 2444.CrossRefGoogle ScholarPubMed
Serbina, EA (2012) Biological significance of the seasonal pattern in emission of Opisthorchidae and Echinochasmidae trematode cercariae in the southern ecosystems of Western Siberia. Russian Journal of Parasitology 2, 2834 (in Russian).Google Scholar
Shekhovtsov, SV, Katokhin, AV, Romanov, KV, Besprozvannykh, VV, Fedorov, KP, Yurlova, NI, Serbina, EA, Sithithaworn, P, Kolchanov, NA and Mordvinov, VA (2009) A novel nuclear marker, pm-int9, for phylogenetic studies of Opisthorchis felineus, Opisthorchis viverrini, and Clonorchis sinensis (Opisthorchiidae, Trematoda). Parasitology Research 106, 293–237.CrossRefGoogle ScholarPubMed
Shi, Y, Yu, K, Liang, A, Huang, Y, Ou, F, Wei, H, Wan, X, Yang, Y, Zhang, W and Jiang, Z (2020) Identification and analysis of the tegument protein and excretory-secretory products of the carcinogenic liver fluke Clonorchis sinensis. Frontiers in Microbiology 11, 555730.CrossRefGoogle ScholarPubMed
Shimalov, VV (2001) Lichinki gel'mintov ryb reki Bug, opasnye dlia cheloveka (Fish helminthic larvae from bug river dangerous to humans). Meditsinskaya Parazitologiya i Parazitarnye Bolezni 2, 2831 (in Russian).Google Scholar
Shin, HR, Oh, JK, Lim, MK, Shin, A, Kong, HJ, Jung, KW, Won, YJ, Park, S, Park, SJ and Hong, ST (2010) Descriptive epidemiology of cholangiocarcinoma and clonorchiasis in Korea. Journal of Korean Medical Science 25, 10111016.CrossRefGoogle ScholarPubMed
Shuteev, MM (1977) Parasite fauna of the muskrat from the upper Ob pine forest. Parazitologiya 11, 538540 (in Russian).Google ScholarPubMed
Siben, AN, Domatsky, VN, Fedorova, OA and Klyatsky, AV (2019) Reindeer parasites of the Khanty-Mansi Autonomous Region-Yugra (Russia): feces study. Advances in Animal and Veterinary Sciences 7, 4549.Google Scholar
Sidorov, EG (1983) Natural Foci of Opisthorchosis. Alma-Ata, USSR: Nauka (in Russian).Google Scholar
Skripova, LV (2013) (Contamination of water objects with helminth eggs and protozoan cysts in the Minsk Region). Meditsinskaya Parazitologiya i Parazitarnye Bolezni 1, 3637 (in Russian).Google Scholar
Smout, MJ, Laha, T, Mulvenna, J, Sripa, B, Suttiprapa, S, Jones, A, Brindley, PJ and Loukas, A (2009) A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathogens 5, e1000611.CrossRefGoogle ScholarPubMed
Smout, MJ, Sotillo, J, Laha, T, Papatpremsiri, A, Rinaldi, G, Pimenta, RN, Chan, LY, Johnson, MS, Turnbull, L, Whitchurch, CB, Giacomin, PR, Moran, CS, Golledge, J, Daly, N, Sripa, B, Mulvenna, JP, Brindley, PJ and Loukas, A (2015) Carcinogenic parasite secretes growth factor that accelerates wound healing and potentially promotes neoplasia. PLoS Pathogens 11, e1005209.CrossRefGoogle ScholarPubMed
Sripa, B, Brindley, PJ, Mulvenna, J, Laha, T, Smout, MJ, Mairiang, E, Bethony, JM and Loukas, A (2012 a) The tumorigenic liver fluke Opisthorchis viverrini–multiple pathways to cancer. Trends in Parasitology 28, 395407.CrossRefGoogle ScholarPubMed
Sripa, B, Thinkhamrop, B, Mairiang, E, Laha, T, Kaewkes, S, Sithithaworn, P, Periago, MV, Bhudhisawasdi, V, Yonglitthipagon, P, Mulvenna, J, Brindley, PJ, Loukas, A and Bethony, JM (2012 b) Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by Opisthorchis viverrini. PLoS Neglected Tropical Diseases 6, e1654.CrossRefGoogle ScholarPubMed
Sripa, B, Tesana, S, Yurlova, N and Nawa, Y (2017) A historical review of small liver fluke infections in humans. Parasitology International 66, 337340.CrossRefGoogle ScholarPubMed
Steele, JA, Richter, CH, Echaubard, P, Saenna, P, Stout, V, Sithithaworn, P and Wilcox, BA (2018) Thinking beyond Opisthorchis viverrini for risk of cholangiocarcinoma in the lower Mekong region: a systematic review and meta-analysis. Infectious Diseases of Poverty 7, 44.CrossRefGoogle ScholarPubMed
Sun, J, Huang, Y, Huang, H, Liang, P, Wang, X, Mao, Q, Men, J, Chen, W, Deng, C, Zhou, C, Lv, X, Zhou, J, Zhang, F, Li, R, Tian, Y, Lei, H, Liang, C, Hu, X, Xu, J, Li, X and Yu X, (2013) Low divergence of Clonorchis sinensis in China based on multilocus analysis. PLoS ONE 8, e67006.CrossRefGoogle ScholarPubMed
Suttiprapa, S, Loukas, A, Laha, T, Wongkham, S, Kaewkes, S, Gaze, S, Brindley, PJ and Sripa, B (2008) Characterization of the antioxidant enzyme, thioredoxin peroxidase, from the carcinogenic human liver fluke, Opisthorchis viverrini. Molecular and Biochemical Parasitology 160, 116122.CrossRefGoogle ScholarPubMed
Tangkawattana, S and Tangkawattana, P (2018) Reservoir animals and their roles in transmission of Opisthorchis viverrini. Advances in Parasitology 101, 6995.CrossRefGoogle ScholarPubMed
Tangkawattana, S, Sereerak, P, Upontain, S, Tangkawattana, P and Sripa, B (2021) Investigation of possible alternate animal reservoir hosts of Opisthorchis viverrini. Acta Tropica 217, 105850.CrossRefGoogle ScholarPubMed
Techasen, A, Namwat, N, Loilome, W, Bungkanjana, P, Khuntikeo, N, Puapairoj, A, Jearanaikoon, P, Saya, H and Yongvanit, P (2012) Tumor necrosis factor-α (TNF-α) stimulates the epithelial-mesenchymal transition regulator Snail in cholangiocarcinoma. Medical Oncology 29, 30833091.CrossRefGoogle ScholarPubMed
Thanee, M, Loilome, W, Techasen, A, Namwat, N, Boonmars, T, Pairojkul, C and Yongvanit, P (2015) Quantitative changes in tumor-associated M2 macrophages characterize cholangiocarcinoma and their association with metastasis. Asian Pacific Journal of Cancer Prevention 16, 30433050.CrossRefGoogle ScholarPubMed
Thu, ND, Dalsgaard, A, Loan, LT and Murrell, KD (2007) Survey for zoonotic liver and intestinal trematode metacercariae in cultured and wild fish in An Giang Province, Vietnam. Korean Journal of Parasitology 45, 4554.CrossRefGoogle Scholar
Tselepatiotis, E, Mantadakis, E, Papoulis, S, Vassalou, E, Kotsakis, P and Samonis, G (2003) A case of Opisthorchis felineus infestation in a pilot from Greece. Infection 31, 430432.CrossRefGoogle Scholar
Uddin, MH, Jang, JJ and Hong, ST (2016) C3H/He mice as an incompatible cholangiocarcinoma model by Clonorchis sinensis, dicyclanil and N-nitrosodimethylamine. Korean Journal of Parasitology 54, 281289.CrossRefGoogle ScholarPubMed
Vale, N, Gouveia, MJ, Botelho, M, Sripa, B, Suttiprapa, S, Rinaldi, G, Gomes, P, Brindley, PJ and Correia da Costa, JM (2013) Carcinogenic liver fluke Opisthorchis viverrini oxysterols detected by LC-MS/MS survey of soluble fraction parasite extract. Parasitology International 62, 535542.CrossRefGoogle ScholarPubMed
Vinogradov, KN (1892) About new species (Distomum sibiricum) of human liver fluke. Trudy Tomskogo Obshchestva Estestvoispytatelei 3, 116130 (in Russian).Google Scholar
Wang, C, Lei, H, Tian, Y, Shang, M, Wu, Y, Li, Y, Zhao, L, Shi, M, Tang, X, Chen, T, Lv, Z, Huang, Y, Tang, X, Yu, X and Li, X (2017) Clonorchis sinensis granulin: identification, immunolocalization, and function in promoting the metastasis of cholangiocarcinoma and hepatocellular carcinoma. Parasites & Vectors 10, 262.CrossRefGoogle ScholarPubMed
Wang, C, He, Q, Yin, Y, Wu, Y and Li, X (2021) Clonorchis sinensis granulin promotes malignant transformation of hepatocyte through EGFR-mediated RAS/MAPK/ERK and PI3K/Akt signaling pathways. Frontiers in Cellular and Infection Microbiology 11, 734750.CrossRefGoogle ScholarPubMed
Wilbers, RHP, Schneiter, R, Holterman, MHM, Drurey, C, Smant, G, Asojo, OA, Maizels, RM and Lozano-Torres, JL (2018) Secreted venom allergen-like proteins of helminths: conserved modulators of host responses in animals and plants. PLoS Pathogens 14, e1007300.CrossRefGoogle ScholarPubMed
Woo, HS, Kim, TY, Sohn, WM and Yong, TS (2015) A tegument-specific venom allergen-like protein of Clonorchis sinensis. Parasitology Research 114, 329333.CrossRefGoogle ScholarPubMed
Yablokov, DD (1984) Opisthorchiasis in Man. Tomsk, Russia: Tomsk University Press (in Russian).Google Scholar
Yoshino, TP, Brown, M, Wu, XJ, Jackson, CJ, Ocadiz-Ruiz, R, Chalmers, IW, Kolb, M, Hokke, CH and Hoffmann, KF (2014) Excreted/secreted Schistosoma mansoni venom allergen-like 9 (SmVAL9) modulates host extracellular matrix remodelling gene expression. International Journal for Parasitology 44, 551563.CrossRefGoogle ScholarPubMed
Yothaisong, S, Thanee, M, Namwat, N, Yongvanit, P, Boonmars, T, Puapairoj, A and Loilome, W (2014) Opisthorchis viverrini infection activates the PI3K/AKT/PTEN and Wnt/beta-catenin signaling pathways in a Cholangiocarcinogenesis model. Asian Pacific Journal of Cancer Prevention 15, 1046310468.CrossRefGoogle Scholar
Young, ND, Nagarajan, N, Lin, SJ, Korhonen, PK, Jex, AR, Hall, RS, Safavi-Hemami, H, Kaewkong, W, Bertrand, D, Gao, S, Seet, Q, Wongkham, S, Teh, BT, Wongkham, C, Intapan, PM, Maleewong, W, Yang, X, Hu, M, Wang, Z, Hofmann, A, Sternberg, PW, Tan, P, Wang, J and Gasser, RB (2014) The Opisthorchis viverrini genome provides insights into life in the bile duct. Nature Communications 5, 4378.CrossRefGoogle ScholarPubMed
Young, ND, Stroehlein, AJ, Kinkar, L, Wang, T, Sohn, WM, Chang, BCH, Kaur, P, Weisz, D, Dudchenko, O, Aiden, EL, Korhonen, PK and Gasser, RB (2021) High-quality reference genome for Clonorchis sinensis. Genomics 113, 16051615.CrossRefGoogle ScholarPubMed
Zadesenets, KS, Katokhin, AV, Mordvinov, VA and Rubtsov, NB (2012) Comparative cytogenetics of opisthorchid species (Trematoda, Opisthorchiidae). Parasitology International 61, 8789.CrossRefGoogle ScholarPubMed
Zaparina, O, Rakhmetova, AS, Kolosova, NG, Cheng, G, Mordvinov, VA and Pakharukova, MY (2021) Antioxidants resveratrol and SkQ1 attenuate praziquantel adverse effects on the liver in Opisthorchis felineus infected hamsters. Acta Tropica 220, 105954.CrossRefGoogle ScholarPubMed
Zavoikin, VD, Beer, SA, Pliushcheva, GL, Sholokhova, SE and Nikiforova, TF (1989) Opistorkhoz na levykh pritokakh Dnepra (Opisthorchiasis at left Dnieper watersheds). Meditsinskaya Parazitologiya i Parazitarnye Bolezni 2, 914 (in Russian).Google Scholar
Zen, Y, Adsay, NV, Bardadin, K, Colombari, R, Ferrell, L, Haga, H, Hong, SM, Hytiroglou, P, Klöppel, G, Lauwers, GY, van Leeuwen, DJ, Notohara, K, Oshima, K, Quaglia, A, Sasaki, M, Sessa, F, Suriawinata, A, Tsui, W, Atomi, Y and Nakanuma, Y (2007) Biliary intraepithelial neoplasia: an international interobserver agreement study and proposal for diagnostic criteria. Modern Pathology 20, 701719.CrossRefGoogle ScholarPubMed
Zubov, NA, Belikov, ES, Zaĭtseva, LN, Kotrikov, VV and Mezentsev, VI (1989) Opistorkhoz v Tobol'ske po dannym autopsiĭ za 1950-1987 gg [Opisthorchiasis in Tobolsk based on 1950-1987 autopsy data]. Meditsinskaya Parazitologiya i Parazitarnye Bolezni (5), 1013.Google Scholar
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