The Past and Present Situation of Opisthorchis viverrini Infection in Thailand The Situation of Opisthorchis viverrini Infection in Thailand
Main Article Content
Abstract
Opisthorchis viverrini, a major foodborne trematode, remains a major public health concern in Thailand, particularly in the northern and northeastern provinces. O. viverrini can be transferred to people and reservoir hosts through the consumption of uncooked cyprinid fish with metacercariae. Chronic infection with O. viverrini can lead to a severe condition known as cholangiocarcinoma (CCA). According to the Nationwide Hospital Admission Database, Thailand has experienced the highest incidence of CCA globally in recent years. Particularly, between 2009 and 2013, there was an incidence rate of 14.6 cases per 100,000 individuals within the population and a corresponding mortality rate (MR) of 14%. In addition, high incidence rates of CCA were reported in Khon Kaen Province from 1989 to 2018, with a rate of 36.1 per 100,000 person-years in men and 14.4 per 100,000 person-years in women. Despite the reduction in the overall prevalence of O. viverrini at the national level, several studies have indicated that the infection remains highly prevalent in some communities in the northeastern and northern regions. Some communities have demonstrated a prevalence of O. viverrini exceeding 20%, and rates reaching as high as 45.7%. Therefore, in populations with a high prevalence, programs to control this parasite should be implemented, including monitoring eating habits. This review article provides a comprehensive overview of the current distribution of O. viverrini in Thailand, outlining its pathophysiology, background, and preventive and control strategies. In addition, this review suggests that individuals in high-risk communities should act to eradicate liver fluke, as this is crucial for the overall health of the community.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Kaewpitoon N, Kaewpitoon SJ, Pengsaa P, Sripa B. Opisthorchis viverrini: the carcinogenic human liver fluke. World J Gastroenterol 2008;14(5):666-74.
Sithithaworn P, Andrews RH, Nguyen VD, Wongsaroj T, Sinuon M, Odermatt P, et al. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol Int 2012;61(1):10-6.
Sripa B, Suwannatrai AT, Sayasone S, Do DT, Khieu V, Yang Y. Current status of human liver fluke infections in the Greater Mekong Subregion. Acta Trop 2021;224:106133.
Fedorova OS, Fedotova MM, Zvonareva OI, Mazeina SV, Kovshirina YV, Sokolova TS, et al. Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Negl Trop Dis 2020;14(6):e0008421.
Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, et al. Liver fluke induces cholangiocarcinoma. PLoS Med 2007;4(7):e201.
Sripa B, Pairojkul C. Cholangiocarcinoma: lessons from Thailand. Curr Opin Gastroenterol 2008;24(3):349-56.
Sripa B, Bethony JM, Sithithaworn P, Kaewkes S, Mairiang E, Loukas A, et al. Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop 2011;120 Suppl 1:S158-68.
Harrington D, Lamberton PHL, McGregor A. Human liver flukes. Lancet Gastroenterol Hepatol 2017;2(9):680-9.
Zhao TT, Feng YJ, Doanh PN, Sayasone S, Khieu V, Nithikathkul C, et al. Model-based spatial-temporal mapping of opisthorchiasis in endemic countries of Southeast Asia. Elife 2021;10:e59755.
Aung WPP, Htoon TT, Tin HH, Thinn KK, Sanpool O, Jongthawin J, et al. First report and molecular identification of Opisthorchis viverrini infection in human communities from Lower Myanmar. PLoS One 2017;12(5):e0177130.
Sadun EH. Studies on Opisthorchis viverrini in Thailand. Am J Hyg 1955;62(2):81-115.
Upatham ES, Brockelman WY, Viyanant V, Lee P, Kaengraeng R, Prayoonwiwat B. Incidence of endemic Opisthorchis viverrini infection in a village in northeast Thailand. Am J Trop Med Hyg 1985;34(5):903-6.
Jongsuksuntigul P , Imsomboon T . Opisthorchiasis control in Thailand. Acta Trop 2003;88(3):229-32.
Wongsaroj T, Nithikathkul C, Rojkitikul W, Nakai W, Royal L, Rammasut P. National survey of helminthiasis in Thailand. Asian Biomed 2014;8:779-83.
Wattanawong O, Iamsirithaworn S, Kophachon T, Nak-Ai W, Wisetmora A, Wongsaroj T, et al. Current status of helminthiases in Thailand: a cross-sectional, nationwide survey, 2019. Acta Trop 2021;223:106082.
Sriamporn S, Pisani P, Pipitgool V, Suwanrungruang K , Kamsa - ard S , Parkin DM. Prevalence of Opisthorchis viverrini infection and incidence of cholangiocarcinoma in Khon Kaen, Northeast Thailand. Trop Med Int Health 2004;9(5):588-94.
Kaewpitoon SJ, Kaewpitoon N, Rujirakul R, Ueng-Arporn N, Matrakool L, Tongtawee T. The carcinogenic liver fluke Opisthorchis viverrini among rural community people in northeast Thailand: a cross- sectional descriptive study using multistage sampling technique. Asian Pac J Cancer Prev 2015;16(17):7803-7.
Martviset P, Phadungsil W, Na-Bangchang K, Sungkhabut W, Panupornpong T, Prathaphan P, et al. Current prevalence and geographic distribution of helminth infections in the parasitic endemic areas of rural northeastern Thailand. BMC Public Health 2023;23(1):448.
Thinkhamrop K, Khuntikeo N, Laohasiriwong W, Chupanit P, Kelly M, Suwannatrai AT. Association of comorbidity between Opisthorchis viverrini infection and diabetes mellitus in the development of cholangiocarcinoma among a high-risk population, northeastern Thailand. PLoS Negl Trop Dis 2021;15(9):e0009741.
Wijit A, Morakote N, Klinchid J. High prevalence of haplorchiasis in Nan and Lampang Provinces, Thailand, proven by adult worm recovery from suspected opisthorchiasis cases. Korean J Parasitol 2013;51(6):767-9.
Buathong S, Phaiphilai K, Ruang-Areerate T, Sitthichot N, Thita T, Mungthin M, et al. Genetic differentiation of Opisthorchis-like eggs in northern Thailand using stool specimens under national strategic plan to control liver fluke infection and cholangiocarcinoma. Am J Trop Med Hyg 2020;103(3):1118-24.
Suwannahitatorn P, Klomjit S, Naaglor T, Taamasri P, Rangsin R, Leelayoova S, et al. A follow-up study of Opisthorchis viverrini infection after the implementation of control program in a rural community, central Thailand. Parasit Vectors 2013;6:188.
Buathong S, Leelayoova S, Mungthin M, Ruang-Areerate T, Naaglor T, Suwannahitatorn P, et al. Molecular discrimination of Opisthorchis-like eggs from residents in a rural community of central Thailand. PLoS Negl Trop Dis 2017;11(11):e0006030.
Boondit J, Suwannahitatorn P, Siripattanapipong S, Leelayoova S, Mungthin M, Tan-Ariya P, et al. An epidemiological survey of Opisthorchis viverrini infection in a lightly infected community, eastern Thailand. Am J Trop Med Hyg 2020;102(4):838-43.
Kaewpitoon N, Kaewpitoon SJ, Ueng-arporn N, Rujirakul R, Churproong S, Matrakool L, et al. Carcinogenic human liver fluke: current status of Opisthorchis viverrini metacercariae in Nakhon Ratchasima,Thailand. Asian Pac J Cancer Prev 2012;13(4):1235-40.
Pinlaor S, Onsurathum S, Boonmars T, Pinlaor P, Hongsrichan N, Chaidee A, et al. Distribution and abundance of Opisthorchis viverrini metacercariae in cyprinid fish in northeastern Thailand. Korean J Parasitol 2013;51(6):703-10.
Charoensuk L, Ribas A, Chedtabud K, Prakobwong S. Infection rate of Opisthorchis viverrini metacercariae in cyprinoid fish from the markets and its association to human opisthorchiasis in the local community in the Northeast Thailand. Acta Trop 2022;225:106216.
Laoprom N, Prathummang S, Chuangchaiya S, Navanesan S, Munajat MB, Suwannatrai AT, et al. Opisthorchis viverrini metacercarial infection in cyprinid fish in Nakhon Phanom Province, northeastern Thailand. Trop Biomed 2021;38(2):25-30.
Harinasuta C, Harinasuta T. Opisthorchis viverrini: life cycle, intermediate hosts, transmission to man and geographical distribution in Thailand. Arzneimittelforschung 1984;34(9B):1164-7.
Sri-Aroon P, Butraporn P, Limsomboon J, Kerdpuech Y, Kaewpoolsri M, Kiatsiri S. Freshwater mollusks of medical importance in Kalasin Province, northeast Thailand. Southeast Asian J Trop Med Public Health 2005;36(3):653-7.
Brockelman WY, Upatham ES, Viyanant V, Ardsungnoen S, Chantanawat R. Field studies on the transmission of the human liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. Int J Parasitol 1986;16(5):545-52.
Kiatsopit N, Sithithaworn P, Saijuntha W, Boonmars T, Tesana S, Sithithaworn J, et al. Exceptionally high prevalence of infection of Bithynia siamensis goniomphalos with Opisthorchis viverrini cercariae in different wetlands in Thailand and Lao PDR. Am J Trop Med Hyg 2012;86(3):464-9.
Namsanor J, Sithithaworn P, Kopolrat K, Kiatsopit N, Pitaksakulrat O, Tesana S, et al. Seasonal transmission of Opisthorchis viverrini sensu lato and a lecithodendriid trematode species in Bithynia siamensis goniomphalos snails in northeast Thailand. Am J Trop Med Hyg 2015;93(1):87-93.
Rachprakhon P, Purivirojkul W. Very low prevalence of Opisthorchis viverrini s.l. cercariae in Bithynia siamensis siamensis snails from the canal network system in the Bangkok Metropolitan Region, Thailand. Parasite 2021;28:2.
Aunpromma S, Tangkawattana P, Papirom P, Kanjampa P, Tesana S, Sripa B, et al. High prevalence of Opisthorchis viverrini infection in reservoir hosts in four districts of Khon Kaen Province, an opisthorchiasis endemic area of Thailand. Parasitol Int 2012;61(1):60-4.
Aunpromma S, Kanjampa P, Papirom P, Tangkawattana S, Tangkawattana P, Tesana S, et al. Prevlence 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 J Trop Med Public Health 2016;47(6):1153-9.
Tangkawattana S, Sereerak P, Upontain S, Tangkawattana P, Sripa B. Investigation of possible alternate animal reservoir hosts of Opisthorchis viverrini. Acta Trop 2021;217:105850.
Suttiprapa S, Sotillo J, Smout M, Suyapoh W, Chaiyadet S, Tripathi T, et al. Opisthorchis viverrini proteome and host-parasite interactions. Adv Parasitol 2018;102:45-72.
Bhamarapravati N, Thammavit W, Vajrasthira S. Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. Am J Trop Med Hyg 1978;27(4):787-94.
Sripa B, Jumnainsong A, Tangkawattana S, Haswell MR. Immune response to Opisthorchis viverrini infection and its role in pathology. Adv Parasitol 2018;102:73-95.
Prakobwong S, Pinlaor S, Yongvanit P, Sithithaworn P, Pairojkul C, Hiraku Y. 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. Int J Parasitol 2009;39(7):825-35.
Mairiang E,Laha T,Bethony JM,Thinkhamrop B, Kaewkes S, Sithithaworn P, et al. Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitol Int 2012;61(1):208-11.
Ninlawan K, O’Hara SP, Splinter PL, Yongvanit P, Kaewkes S, Surapaitoon A, et al. Opisthorchis viverrini excretory/secretory products induce toll-like receptor 4 upregulation and production of interleukin 6 and 8 in cholangiocyte. Parasitol Int 2010;59(4):616-21.
Smout MJ, Laha T, Mulvenna J, Sripa B, Suttiprapa S, Jones A, et al. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog 2009;5(10):e1000611.
Thamavit W, Bhamarapravati N, Sahaphong S, Vajrasthira S, Angsubhakorn S. Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Res 1978;38(12):4634-9.
Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. A review of human carcinogens--part B: biological agents. Lancet Oncol 2009;10(4):321-2.
Fedorova OS, Kovshirina YV, Kovshirina AE, Fedotova MM, Deev IA, Petrovskiy FI, et al. Opisthorchis felineus infection and cholangiocarcinoma in the Russian Federation: a review of medical statistics. Parasitol Int 2017;66(4):365-71.
Maksimova GA, Pakharukova MY, Kashina EV, Zhukova NA, Kovner AV, Lvova MN, et al. Effect of Opisthorchis felineus infection and dimethylnitrosamine administration on the induction of cholangiocarcinoma in Syrian hamsters. Parasitol Int 2017;66(4):458-63.
Green A, Uttaravichien T, Bhudhisawasdi V, Chartbanchachai W, Elkins DB, Marieng EO, et al. Cholangiocarcinoma in north east Thailand. A hospital-based study. Trop Geogr Med 1991;43(1-2):193-8.
Banales JM, Cardinale V, Carpino G, Marzioni M, Andersen JB, Invernizzi P, et al. Expert consensus document: cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European Network for the Study of Cholangiocarcinoma (ENS-CCA). Nat Rev Gastroenterol Hepatol 2016;13(5):261-80.
Kamsa-ard S, Kamsa-ard S, Luvira V, Suwanrungruang K, Vatanasapt P, Wiangnon S. Risk factors for cholangiocarcinoma in Thailand: a systematic review and metaanalysis. Asian Pac J Cancer Prev 2018;19(3):605-14.
Charoensuk L, Subrungruang I, Mungthin M, Pinlaor S, Suwannahitatorn P. Comparison of stool examination techniques to detect Opisthorchis viverrini in low intensity infection. Acta Trop 2019;191:13-6.
Kopolrat KY, Singthong S, Khuntikeo N, Loilome W, Worasith C, Homwong C, et al. Performance of Mini Parasep® SF stool concentrator kit, Kato-Katz, and formalin-ethyl acetate concentration methods for diagnosis of opisthorchiasis in northeast Thailand. Parasit Vectors 2022;15(1):234.
Sakolvaree Y, Ybanez L, Chaicumpa W. Parasites elicited cross-reacting antibodies to Opisthorchis viverrini. Asian Pac J Allergy Immunol 1997;15(2):115-22.
Wongsaroj T, Sakolvaree Y, Chaicumpa W, Maleewong W, Kitikoon V, Tapchaisri P, et al. Affinity purified oval antigen for diagnosis of Opisthorchis viverrini. Asian Pac J Allergy Immunol 2001;19(4):245-58.
Tesana S, Srisawangwong T, Sithithaworn P, Itoh M, Phumchaiyothin R. The ELISA-based detection of anti-Opisthorchis viverrini IgG and IgG4 in samples of human urine and serum from an endemic area of north-eastern Thailand. Ann Trop Med Parasitol 2007;101(7):585-91.
Sadaow L, Rodpai R, Janwan P, Boonroumkaew P, Sanpool O, Thanchomnang T, et al. An innovative test for the rapid detection of specific IgG antibodies in human whole-blood for the diagnosis of Opisthorchis viverrini infection. Trop Med Infect Dis 2022;7(10):308.
Rodpai R , Luvira V , Sadaow L , Sukeepaisarnjaroen W, Kitkhuandee A, Paonariang K, et al. Rapid assessment of Opisthorchis viverrini IgG antibody in serum: a potential diagnostic biomarker to predict risk of cholangiocarcinoma in regions endemic for opisthorchiasis. Int J Infect Dis 2022;116:80-4.
Worasith C, Sithithaworn J, Wongphutorn P, Homwong C, Khongsukwiwat K, Techasen A, et al. Accuracy of a new rapid diagnostic test for urinary antigen detection and assessment of drug treatment in opisthorchiasis. Infect Dis Poverty 2023;12(1):102.
Wongratanacheewin S, Pumidonming W, Sermswan RW, Pipitgool V, Maleewong W. Detection of Opisthorchis viverrini in human stool specimens by PCR. J Clin Microbiol 2002;40(10):3879-80.
Kaewkong W, Intapan PM, Sanpool O, Janwan P, Thanchomnang T, Laummaunwai P, et al. Molecular differentiation of Opisthorchis viverrini and Clonorchis sinensis eggs by multiplex real-time PCR with high resolution melting analysis. Korean J Parasitol 2013;51(6):689-94.
Sato M, Pongvongsa T, Sanguankiat S, Yoonuan T, Dekumyoy P, Kalambaheti T, et al. Copro-DNA diagnosis of Opisthorchis viverrini and Haplorchis taichui infection in an endemic area of Lao PDR. Southeast Asian J Trop Med Public Health 2010;41(1):28-35.
Lamaningao P, Kanda S, Laimanivong S, Shimono T, Darcy AW, Phyaluanglath A, et al. Development of a PCR assay for diagnosing trematode (Opisthorchis and Haplorchis) infections in human stools. Am J Trop Med Hyg 2017;96(1):221-8.
Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Chilton NB, Petney TN, et al. Mitochondrial DNA sequence variation among geographical isolates of Opisthorchis viverrini in Thailand and Lao PDR, and phylogenetic relationships with other trematodes. Parasitology 2008;135(12):1479-86.
Thaenkham U, Nuamtanong S, Sa-nguankiat S, Yoonuan T, Touch S, Manivong K, et al. Monophyly of Opisthorchis viverrini populations in the lower Mekong basin, using mitochondrial DNA nad1 gene as the marker. Parasitol Int 2010;59(2):242-7.
Sithithaworn P , Nuchjungreed C , Srisawangwong T, Ando K, Petney TN, Chilton NB, et al. Genetic variation in Opisthorchis viverrini ( Trematoda : Opisthorchiidae) from northeast Thailand and Laos PDR based on random amplified polymorphic DNA analyses. Parasitol Res 2007;100(3):613-7.
Laoprom N, Sithithaworn P, Andrews RH, Ando K, Laha T, Klinbunga S, et al. Population genetic structuring in Opisthorchis viverrini over various spatial scales in Thailand and Lao PDR. PLoS Negl Trop Dis 2012;6(11):e1906.
Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Pipitgool V, Tesana S, et al. Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. Int J Parasitol 2007;37(6):695-703.
Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Satrawaha R, Chilton NB, et al. Genetic variation at three enzyme loci within a Thailand population of Opisthorchis viverrini. Parasitol Res 2008;103(6):1283-7.
Pitaksakulrat O, Webster BL, Webster JP, Laha T, Saijuntha W, Lamberton PHL, et al. 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. Infect Genet Evol 2018;62:86-94.
Namsanor J, Pitaksakulrat O, Kopolrat K, Kiatsopit N, Webster BL, Gower CM, et al. Impact of geography and time on genetic clusters of Opisthorchis viverrini identified by microsatellite and mitochondrial DNA analysis. Int J Parasitol 2020;50(14):1133-44.
Kiatsopit N, Sithithaworn P, Saijuntha W, Petney TN, Andrews RH. Opisthorchis viverrini: implications of the systematics of first intermediate hosts, Bithynia snail species in Thailand and Lao PDR. Infect Genet Evol 2013;14:313-9.
Saijuntha W, Andrews RH, Sithithaworn P, Petney TN. 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. Infect Genet Evol 2022;97:105182.
Kamsa-Ard S, Santong C, Kamsa-Ard S, Luvira V, Luvira V, Suwanrungruang K, et al. Decreasing trends in cholangiocarcinoma incidence and relative survival in Khon Kaen, Thailand: an updated, inclusive, population-based cancer registry analysis for 1989-2018. PLoS One 2021;16(2):e0246490.
Thinkhamrop K, Khuntikeo N, Sithithaworn P, Thinkhamrop W, Wangdi K, Kelly MJ, et al. Correction to: repeated praziquantel treatment and Opisthorchis viverrini infection: a population-based cross-sectional study in northeast Thailand. Infect Dis Poverty 2019;8(1):33.
Saengsawang P, Promthet S, Bradshaw P. Reinfection by Opisthorchis viverrini after treatment with Praziquantel. Asian Pac J Cancer Prev 2016;17(2):857-62.