Opisthorchis viverrini: an underestimated parasite in world health

doi:10.1016/j.pt.2008.08.011

Trends in Parasitology

Volume 24, Issue 11, November 2008, Pages 497-501

https://doi.org/10.1016/j.pt.2008.08.011 Get rights and content

Infection with Opisthorchis viverrini and its associated cholangiocarcinoma (CCA) is an underestimated problem in the Mekong region of Southeast Asia, despite the widespread use of praziquantel and health education measures for parasite control. Although data from Cambodia, Laos and Vietnam are rare, data from Thailand often show wide-ranging variability in epidemiological parameters, including human morbidity and the prevalence and incidence of CCA. The recent discovery of high levels of population genetic variability in O. viverrini in different wetlands in Thailand and Laos, which indicates the presence of sibling species, suggests that we have underestimated the complexity of this epidemiological situation. Future research should determine the relationship between the genetic variability of O. viverrini and patterns of opisthorchiasis-related disease.

Section snippets

Opisthorchis viverrini in Southeast Asia

The World Health Organization (WHO) estimates that approximately five million people with HIV live in the Asia–Pacific Region [1]. This can be compared with a conservative estimate of ten million people infected with the liver fluke Opisthorchis viverrini in Thailand and Laos alone [2]. People infected with Opisthorchis parasites are at risk of developing cholangiocarcinoma (CCA), and those who have advanced CCA will almost certainly die. As with HIV, infection with O. viverrini and the

O. viverrini: an underestimated parasite in world health

O. viverrini is an underestimated parasite in world health [4] because it is mistakenly thought to represent a limited, local problem in Southeast Asia, particularly in Thailand [5]. This is predominantly because of the fact that reasonably accurate spatial and temporal morbidity data and CCA incidence are available from Thailand but not from elsewhere within the Mekong region where O. viverrini occurs 6, 7, 8, 9. Although O. viverrini infection in humans is often asymptomatic, this parasite

Prevalence in humans

The most recent estimate of the number of people infected with O. viverrini in the Mekong region is eight million in Thailand and two million in Laos [2]. This is a substantial underestimate of its prevalence because no data are available for Cambodia or Vietnam, although opisthorchiasis in known to be common in parts of these countries 18, 19. In Thailand, an average of 9.6% of the population is infected [20], with the liver fluke being distributed mainly in the North (19.3% prevalence) and

Incidence of CCA

CCA has caused millions of deaths in southeast Asia [25]. The most important risk factor for CCA is O. viverrini infection, with risk being dependent on intensity [26], previous or current exposure to infection and host genetic polymorphism [27]. A recent study detected residual O. viverrini DNA in both cancerous and non-cancerous tissue in CCA patients in Thailand [28]. By contrast, the risk factors for CCA in areas where liver flukes are not endemic include primary sclerosing cholangitis,

Genetic and molecular characterization of O. viverrini

The study of the molecular genetics of O. viverrini has received considerable impetus from the recent publication that provides the first catalogue of expressed genes (∼14% of the entire transcriptome) for this species [34]. This advance will enhance our ability to conduct comprehensive molecular analyses of the systematics and population genetics of O. viverrini in a similar manner to that proven useful for other parasites, as has been the case for the parasitic protozoan Giardia intestinalis

Current and future threats

The movement of people is a major component of globalization in Asia [40]. O. viverrini is regularly carried to regions outside of its normal distribution by tourists and Thai labourers 2, 41. Because infection is often asymptomatic and of a long duration, infected migrants are likely to remain undiagnosed and shed eggs for long time periods. However, the introduction of O. viverrini to human populations outside of the Mekong region is more likely to come from fish imports. Asia is the world’s

Prevention

The availability of praziquantel provides effective chemotherapy for Opisthorchis parasite infection [46]. There is, however, evidence that repeated infection and treatment could increase the risk of CCA 50, 51. Thus, a more basic approach involving prevention by reducing the consumption of infected fish is likely to have better long-term chances of success. It is difficult to achieve this goal, however, because it involves changing traditional patterns of eating behaviour. A control program

Concluding remarks and future directions

Although our knowledge of the biology of O. viverrini is steadily increasing, fundamental studies on epidemiology and ecology, in addition to genomics and proteomics, are still needed. In addition, investigation of the molecular basis of fluke-induced CCA is likely to be of great importance in the development of biomarkers for the diagnosis of this devastating condition.

The scientific challenge of providing a comprehensive epidemiological understanding of the O. viverrini species complex

Acknowledgements

This research was supported by a Wellcome Trust Collaborative Research Initiative Grant, the Thailand Research Fund through the Royal Golden Jubilee PhD. Program, the European Commission through a TREMKIT project, the Faculty of Medicine, Khon Kaen University, Overseas Visiting Professor Program and the Deutsche Forschungsgemeinschaft (PE1611/1–1).

References (53)

P. Sithithaworn et al.
Epidemiology of Opisthorchis viverrini
Acta Trop.
(2003)
T.N. Petney
Environmental, cultural and social changes and their influence on parasite infections
Int. J. Parasitol.
(2001)
P. Sithithaworn
Parasite-associated morbidity: liver fluke infection and bile duct cancer in northeast Thailand
Int. J. Parasitol.
(1994)
V. Vatanasapt
Northeast Thailand: a region with high incidence of cholangiocarcinoma
Lancet
(1990)
B. Sripa
Pathobiology of opisthorchiasis: an update
Acta Trop.
(2003)
D.A. Mayer et al.
The role of helminth infections in carcinogenesis
Adv. Parasitol.
(2007)
S. Kaewkes
Taxonomy and biology of liver flukes
Acta Trop.
(2003)
W.Y. Brockelman
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)
S. Sayasone
Epidemiology of Opisthorchis viverrini in a rural district of southern Lao PDR
Trans. R. Soc. Trop. Med. Hyg.
(2007)
P. Jongsuksuntigul et al.
Opisthorchiasis control in Thailand
Acta Trop.
(2003)

E.S. Upatham

Rate of re-infection by Opisthorchis viverrini in an endemic northeast Thai community after chemotherapy

Int. J. Parasitol.

(1988)

N. Suksumek

TaqMan real-time PCR assay for specific detection of Opisthorchis viverrini DNA in Thai patients with hepatocellular carcinoma and cholangiocarcinoma

Exp. Parasitol.

(2008)

S.A. Khan

Cholangiocarcinoma

Lancet

(2005)

W. Saijuntha

Genetic markers for the identification and characterization of Opisthorchis viverrini, a medically important food borne trematode in southeast Asia

Acta Trop.

(2006)

W. Saijuntha

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)

S. Pinlaor

Hepatobiliary changes, antibody response, and alteration of liver enzymes in hamsters re-infected with Opisthorchis viverrini

Exp. Parasitol.

(2004)

WHO (2007) AIDS epidemic update. World Health Organisation–United Nations Program on...

P.J. Hotez

Control of neglected tropical diseases

N. Engl. J. Med.

(2007)

B. Sripa

Liver fluke induces cholangiocarcinoma

PLoS Med.

(2007)

D.M. Parkin

Cholangiocarcinoma: epidemiology, mechanisms of carcinogenesis and prevention

Cancer Epidemiol. Biomarkers Prev.

(1993)

B. Sripa et al.

Cholangiocarcinoma: lessons from Thailand

Curr. Opin. Gastroenterol.

(2008)

IARC

Infection with liver flukes (Opisthorchis viverrini, Opisthorchis felineus and Clonorchis sinensis)

IARC Monogr. Eval. Carcinog. Risks Hum.

(1994)

T. Patel et al.

Cholangiocarcinoma: emerging approaches to a challenging cancer

Curr. Opin. Gastroenterol.

(2007)

R. Muller

Worms and Human Disease

(2002)

S. Vichasri

Opisthorchis viverrini: intensity and rates of infection in cyprinoid fish from an endemic focus in northeast Thailand

Southeast Asian J. Trop. Med. Public Health

(1982)

P. Sithithaworn

Epidemiology of food-borne trematodes and other parasite infections in a fishing community on the Nam Ngum reservoir, Lao PDR

Southeast Asian J. Trop. Med. Public Health

(2006)

Cited by (180)

Roaming behavior of the owned domestic cats (Felis catus) with possible roles in the transmission of Opisthorchis viverrini in the endemic area in Khon Kaen, Thailand
2023, Acta Tropica
In the endemic area of the liver fluke (Opisthorchis viverrini) infection, effective control of opisthorchiasis using One Health approaches requires transmission interruption in all hosts in the parasite life cycle. Owned domestic cats (Felis catus) are considered an important species among mammalian reservoirs. Similar to humans, household cats become infected by eating raw, contaminated fish and spread the O. viverrini eggs to the environment by defecation. In rural areas, cat owners usually feed their cats with human food or food waste, especially fish dishes. There is a high risk for cats to become infected and deposit eggs in the peri-household environment. The lack of research on domestic cats led us to study their roaming behavior, roaming range, habitat preference and risk of disease transmission. GPS loggers were harnessed to 28 domestic cats in 7 villages around Lawa Lake, the endemic area of human opisthorchiasis. All cats were examined for the O. viverrini infection status using modified formalin-ether concentration technique (MFECT) before application of the GPS device used to observe and record their roaming distance and range area. Then, composition analysis for habitat selection was performed using the location data. Additionally, cat owners were interviewed using participatory epidemiologic methods for their perceptions and knowledge about the reservoir hosts of this trematode. Our study suggested that the prevalence of O. viverrini in cats in this area has not declined appreciably in comparison with our previous study four years ago, although the treatment and control has been applied intensively in humans. The longest distance that individual cats roamed ranged from 51 to 363 meters (mean±SD = 154.48±90.71). The cats traveled tracks around their home. There was no significant difference in the average distance that cats ranged between O. viverrini infected group (154.13±72.80 meters) and the non-infected group (154.67±101.39 meters) was found. Compositional analysis suggested that the domestic cats preferred urban habitats where food and safety were probably more available. It appears that the main transmission route for infection of cats was contaminated fish fed to cats or fish that remained in their houses. Therefore, owners should refrain from feeding their cats potentially contaminated foods, food scraps and raw fish remains and prevent their cats from accessing them. Moreover, the participatory epidemiology results suggest that awareness of villagers is not enough for the effective and sustainable control of the disease.
The burden of opisthorchiasis and leptospirosis in Thailand: A nationwide syndemic analysis
2022, Acta Tropica
Citation Excerpt :
Trematode infection Opisthorchis viverrini is widely spread in Southeast Asia, including regions of the Democratic People's Republic of Lao, Vietnam, Thailand, and Cambodia, with more than 10 million people infected. ( Andrews et al., 2008; Sithithaworn et al., 2012; Sripa et al., 2007). Opisthorchiasis is linked with hepatobiliary morbidity, including chronic cholangitis, periductal fibrosis, cholelithiasis, bile duct cancer, or cholangiocarcinoma (CCA) (Bouvard et al., 2009; Sripa et al., 2012; Sripa et al., 2007).
Opisthorchiasis, caused by the foodborne trematode parasite Opisthorchis viverrini, is co-endemic with leptospirosis in the Greater Mekong Subregion. Socio-economic determinants, occupational risk factors, and reservoir hosts interact with the diseases in the threat to human health, but the situation has not been explored. We, therefore, studied the interaction between the diseases and their associated risks using a syndemic approach with nationwide data for Thailand. Methods included Bayesian mapping, principal component analysis (PCA), and nested correlation analysis to analyze the data for 2009 and 2014. Bayesian mapping demonstrates that opisthorchiasis acts in a synergistic manner to massively alter the risk of leptospirosis at the provincial level, particularly in areas of opisthorchiasis endemicity in Northeast Thailand. Socio-economic and occupational factors significantly influence the disease syndemic with moderate effect sizes of -0.4 and 0.5, respectively (P<0.001). These effects are most remarkable in the northeastern region, which has not only the highest poverty level but also the highest proportion of occupational risk (P<0.001). Cats and dogs play crucial roles in maintaining the syndemic (r-value 7 and 6 with P<0.001). The study shows that opisthorchiasis and leptospirosis become syndemic, especially in North-East, Thailand. Socio-economic and occupational variables are positively syndemic as they are representative of neglected tropical diseases. The role of reservoir hosts underlines the value of an interdisciplinary approach, such as One Health for Sustainability Disease Control.
Liver Fluke Infection Throughout Human Evolution
2022, Gastro Hep Advances
The species of liver fluke that infect humans are zoonotic parasites that we share with other animals. The complex way in which humans have interacted with their environment, and the animals that live alongside them, has affected our ancestors’ risk of infection by these helminths for millions of years. Here, we describe the range of flukes that can survive in the human liver and the health consequences that result from infection. Our focus is on Clonorchis sinensis (Chinese liver fluke), Fasciola hepatica (sheep liver fluke), F. gigantica (giant liver fluke), Opisthorchis viverrini (Southeast Asian liver fluke), O. felineus (cat liver fluke), and Dicrocoelium dendriticum (lancet liver fluke). We use our knowledge of where different kinds of liver flukes are endemic to estimate when and where human ancestors would have been exposed to infection over deep time. DNA evidence is used to investigate the evolutionary origins of the major species of liver flukes. The archaeological evidence for different species of fluke helps to show in which periods of human history they were most common. These flukes spread to humans from wild animals in early prehistory because of our ancestor’s hunter-gatherer lifestyle and later from farm animals after the development of agriculture. We explore when and how some species have been able to spread across the world, whereas others are limited to particular geographic regions because of the endemic distribution of snail and vertebrate intermediate hosts. It is clear that human activity and migrations have played a key role in the expanding geographical range where we find liver flukes endemic today.
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
2022, Infection, Genetics and Evolution
The group 1 carcinogen, the liver fluke Opisthorchis viverrini is the causative agent of opisthorchiasis and subsequent bile duct cancer (cholangiocarcinoma; CCA), which is an important public health problem in Southeast Asia. Bithynia snails are known to be the sole intermediate host of O. viverrini, and distributed throughout endemic areas of opisthorchiasis. Since 2001, the genetic variation investigation of O. viverrini has progressively been investigated. Comprehensive genetic variation studies of O. viverrini and Bithynia snails were undertaken and consecutively published in 2007 by Saijuntha and colleagues. These studies provided genetic evidence that O. viverrini and Bithynia snails are both species complex with evidence of co-evolution. Later, several studies have provided data in support of this finding, and have continuously to date reinforced that both O. viverrini and Bithynia are species complexes. Moreover, studies have shown that genetic variation of O. viverrini is related to geographical, temporal, fish host species including geographical genetic variation of its snail host, Bithynia siamensis sensu lato. This is significant and important in our understanding of the evolution and phylogenetic relationships between species within the O. viverrini and Bithynia species complexes. A comprehensive knowledge of the systematics and population genetics of O. viverrini and Bithynia snails provides a sound basis to instigate and develop effective prevention and control programs targeting opisthorchiasis and CCA in the endemic areas of Southeast Asia. Thus, this review examines the historical series of investigations of the systematics and population genetics of O. viverrini including Bithynia spp. in Southeast Asia since molecular genetic investigations commenced some 20 years ago.
A fluorescence AuNPs-LISA: A new approach for Opisthorchis viverrini (Ov) antigen detection with a simple fluorescent enhancement strategy by surfactant micelle in urine samples
2021, Spectrochimica Acta - Part A: Molecular and Biomolecular Spectroscopy
The colorimetric AuNPs-LISA is a new, powerful technique for the detection of Opisthorchis viverrini antigen (OvAg) in urine samples. However, the diagnostic sensitivity of the colorimetric AuNPs-LISA is powerless to screen ultralow concentrations of OvAg in urine samples in cases of early stage liver fluke infection. This work, we aimed to improve the diagnostic sensitivity of the colorimetric AuNPs-LISA by developing a new fluorescence AuNPs-LISA. O-phenylenediamine (OPD) was used as the chromogenic substrate instead of the tetramethylbenzidine (TMB) of the colorimetric AuNPs-LISA. Interestingly, the fluorescence of the OPD oxidation product by the peroxidase-like activity of labelled AuNPs can be extremely enhanced by a non-ionic surfactant, especially the Triton X-100. The proposed assay exhibited a dynamic linear detection of OvAg concentration in the range of 34.18 ng mL⁻¹ to 273.44 ng mL⁻¹ with the limit of detection at 36.97 ng mL⁻¹ which the detection sensitivity enhancement around 1200-fold when comparing with the colorimetric AuNPs-LISA. This model exhibits high diagnosis sensitivity, specificity and accuracy, 91.28%, 91.75%, and 91.59%, respectively, compared to the traditional ELISA. The fluorescence AuNPs-LISA showed excellent potential for the diagnosis of OvAg in urine samples from endemic areas. This will provide an effective tool for the detection, control and elimination of human opisthorchiasis.
Natural variables separate the endemic areas of Clonorchis sinensis and Opisthorchis viverrini along a continuous, straight zone in Southeast Asia
2024, Infectious Diseases of Poverty

View all citing articles on Scopus

View full text

Trends in Parasitology

OpinionOpisthorchis viverrini: an underestimated parasite in world health

Section snippets

Opisthorchis viverrini in Southeast Asia

O. viverrini: an underestimated parasite in world health

Prevalence in humans

Incidence of CCA

Genetic and molecular characterization of O. viverrini

Current and future threats

Prevention

Concluding remarks and future directions

Acknowledgements

Acta Trop.

Int. J. Parasitol.

Int. J. Parasitol.

Lancet

Acta Trop.

Adv. Parasitol.

Acta Trop.

Int. J. Parasitol.

Trans. R. Soc. Trop. Med. Hyg.

Acta Trop.

Int. J. Parasitol.

Exp. Parasitol.

Lancet

Acta Trop.

Int. J. Parasitol.

Exp. Parasitol.

Control of neglected tropical diseases

N. Engl. J. Med.

Liver fluke induces cholangiocarcinoma

PLoS Med.

Cholangiocarcinoma: epidemiology, mechanisms of carcinogenesis and prevention

Cancer Epidemiol. Biomarkers Prev.

Cholangiocarcinoma: lessons from Thailand

Curr. Opin. Gastroenterol.

Infection with liver flukes (Opisthorchis viverrini, Opisthorchis felineus and Clonorchis sinensis)

IARC Monogr. Eval. Carcinog. Risks Hum.

Cholangiocarcinoma: emerging approaches to a challenging cancer

Curr. Opin. Gastroenterol.

Worms and Human Disease

Opisthorchis viverrini: intensity and rates of infection in cyprinoid fish from an endemic focus in northeast Thailand

Southeast Asian J. Trop. Med. Public Health

Epidemiology of food-borne trematodes and other parasite infections in a fishing community on the Nam Ngum reservoir, Lao PDR

Southeast Asian J. Trop. Med. Public Health

Opinion
Opisthorchis viverrini: an underestimated parasite in world health