Elsevier

Acta Tropica

Volume 225, January 2022, 106216
Acta Tropica

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

https://doi.org/10.1016/j.actatropica.2021.106216Get rights and content

Abstract

The prevalence of Opisthorchis viverrini, a fish-borne zoonotic trematode that can provoke cholangiocarcinoma, is high in the Northeast Thailand. The aim of this study was to determine the prevalence of O. viverrini metacercariae in the cyprinid fish and determine its association of O. viverrini infection among the consumers who regularly buy fish in the markets. A cross-sectional study was conducted in nine provinces covering 20 districts of Thailand, and we examined 778 cyprinoid fish specimens belonging to five species purchased from local markets. Pepsin-HCl digestion method was used to recover O. viverrini metacercariae from fish. In all districts surveyed, O. viverrini metacercariae-positive fish were found with the infection rates ranging from 3.9 to 21.1%. All five fish species studied were positive for O. viverrini metacercariae: Henicorhynchus siamensis (13.7%), Cyclocheilichtys spp. (12.7%), Hampala spp. (8.1%), Systomus spp. (6.9%) and Barbonymus goniatus (5.0%). An average prevalence of O. viverrini infection was 7.1% in the fish consumers surveyed in the markets. The source of fish was determined and our results showed that parasitized fish are sold in markets up to 100 km away from the point of capture, which contributes to the dispersion and maintenance of this helminthiasis. Our results point to the transmission of liver flukes via markets, in spite of many active programs of health education, elimination, prevention and control aimed to reduce O. viverrini infection and subsequent cholangiocarcinoma in the endemic areas of Thailand.

Introduction

Opisthorchis viverrini infection is a representative fish-borne zoonotic trematode (FZT) and is a public health problem in the endemic area of the Greater Mekong Subregion (Eom et al., 2015), especially in the Northeast Thailand (Prakobwong et al., 2017b; Sithithaworn et al., 2012). The first intermediate host of O. viverrini in Thailand is freshwater snails of the genus Bithynia spp., the second intermediate hosts are various cyprinid fish, and then humans as the main definitive host (Conlan et al., 2011). Humans in endemic areas are infected by ingesting raw or undercooked cyprinoid fish containing the infective O. viverrini metacercariae (Pinlaor et al., 2013) in dishes such as chopped raw fish salad (Rangsin et al., 2009). After consuming raw cyprinoid fish containing O. viverrini metacercariae, excystation occurs in the duodenum and the excysted juvenile worms travel into the host's biliary ducts causing injury and inflammation-mediated oxidative/nitrative DNA damage (Pinlaor et al., 2008). Chronic infection results in periductal fibrosis (Prakobwong et al., 2009; Sripa et al., 2009), with a risk of cholangiocarcinoma development (Sripa et al., 2012; Sripa and Pairojkul, 2008).

Most of the epidemiological studies on the second intermediate hosts (cyprinoid fish) to date have been designed to determine the prevalences and intensities of O. viverrini in cyprinoid fish in the areas near the rivers in the Greater Mekong Subregion (Eom et al., 2015; Namsanor et al., 2020). In the Northeast Thailand, surveys of O. viverrini metacercariae in cyprinoid fish caught in rivers, reservoirs and ponds/lakes revealed six species of host fish: Cyclocheilichthys armatus, Hampala dispar, Henicorhynchus siamensis, Osteochilus hasselti, Puntioplites proctozysron and Puntius orphoides. Studies in 20 provinces in the Northeast Thailand showed that O. viverrini metacercariae infection rate in cyprinoid fish was 24.3% (Pinlaor et al., 2013). O. viverrini metacercariae were mainly found in the muscle tissues (the edible part) of fish, followed by the fins, head and visceral organs (Manivong et al., 2009); the intensity of O. viverrini metacercariae per fish was 4–6 cysts/fish (Namsanor et al., 2020). Epidemiological survey for O. viverrini metacercariae in cyprinid fish have been reported repeatedly from various places of the Greater Mekong Subregion (Prakobwong et al., 2017a, 2017b; Touch et al., 2009). Also, previous studies of epidemiological survey for human opisthorchiasis in the Northeast Thailand showed the prevalence of over 10% (Prakobwong et al., 2017a, 2017b; Prakobwong and Suwannatrai, 2020). In spite of these epidemiological studies, geographical distribution of infected fish by commercial activities and its correlation with the prevalence of O. viverrini infection in humans has never been fully examined.

The prevalence of O. viverrini infection in humans in the Northeast Thailand has gradually decreased from 34.6% to 10–15%, depending on the community surveyed (Jongsuksuntigul and Imsomboon, 2003). Nevertheless, infection in humans in the high endemicity areas continues with the registered values of 10% or over (Kaewpitoon et al., 2012). A recent study as a part of a three-years management program in the endemic areas demonstrated the high re-infection rates of O. viverrini-infection in humans (Prakobwong and Suwannatrai, 2020). Although infection with O. viverrini in humans has often been associated with settlement near river basins (Prakobwong et al., 2017a), at least 5–10% of infected people are living far away from waterbodies where this infection was supposed to be originated. In this study, we investigated the infection status of O. viverrini metacercariae in cyprinoid fish sold in markets in the endemic area in upper Northeast Thailand. Then, we investigate the prevalence of O. viverrini infection among the consumers who buy fish in the markets. The results of this epidemiological study is discussed in view of the risk factors associated with O. viverrini infection.

Section snippets

Study area and the collection of cyprinoid fish

A total of 778 cyprinid fish were collected and examined for O. viverrini infection in 2019–2021. They were obtained at least three occasions (1 kg per seller per occasion) in the wet and dry seasons from each main market in 20 districts in nine provinces in the upper part of the Northeast Thailand (details in Fig. 1 and Table 1). The stalls selected have been established in the market for at least three years. The river basin of the origin of the fish was recorded based on the information

Prevalence and intensity of metacercariae in cyprinoid fish sold in the markets

Of the 778 cyprinoid fish collected from nine provinces in Northeast Thailand, 93 were infected with O. viverrini metacercariae. All the fish species studied were parasitized; the average prevalence in markets was 11.9% (95% CI, 9.7-14.4x0025 x0025) (details in Fig. 1). The average intensity of metacercariae in fish in markets was 6.7 metacercariae/infected fish (range: 1–45), with the highest intensity being 12.5 metacercariae/infected fish. Statistically higher prevalence were observed in

Discussion

Opisthorchiasis-associated CCA is responsible for more than 20,000 deaths every year in Thailand and constitutes a serious public health concern that has a great socioeconomic impact on poor families and communities (Jongsuksuntigul and Imsomboon, 2003; Saijuntha et al., 2019). The Greater Mekong Subregion, especially the Northeast Thailand, is known as the highly endemic area of O. viverrini infection (Pinlaor et al., 2013). In rural areas, 60–90% of people are estimated to consume raw

Conclusion

The high prevalence of O. viverrni metacercariae in cyprinoid fish was detected in markets (11.9%, range 3.9–21.9%). Our study showed that local markets play an important role in both the maintenance of the high prevalence of opisthorchiasis and its spread into other areas in the Northeast Thailand. The active programs of health education, elimination, prevention and control in endemic areas to reduce O. viverrini infection would be a concern.

Declaration of Competing Interest

The authors declare no conflicts of interest.

Acknowledgments

This study was supported by the Faculty of Science, Udonthani Rajabhat University. We also thank Professor Dr. Yukifumi Nawa from the Faculty of the Medicine, Khon Kaen University, for English editing of the manuscript.

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