Mekong River Commission

Liver and intestinal flukes: an underrated health risk in the Mekong Basin

By Kent G. Hortle*

Humans and other mammals can become infected by eating uncooked freshwater fish and other aquatic animals, including insect larvae

In the Mekong Basin, fish and other aquatic animals such as frogs, molluscs and crustaceans are important components of the traditional diet. Despite a generally high average intake of aquatic animals [1], individual consumption varies widely across the Lower Mekong Basin. Inadequate intake of high-protein foods is associated with malnutrition, which is still common, particularly in remote and rural areas or where people have limited access to fish and other aquatic animals— such as Luang Prabang in northern Laos. Although governments and aid agencies have emphasised the need to increase rice production to ensure people receive sufficient energy each day, there is increasing awareness of the importance of maintaining a nutrientdense diet. Fish or other aquatic animals can provide much of our essential daily requirements of protein, minerals and vitamins. But improving the intake of high-nutrient foods alone will not necessarily translate to improved public health. Inadequate health care and hygiene can lead to infection by common water and soil-borne parasites, which may impair absorption or metabolism, leading to malnutrition despite apparently adequate dietary intake [2, 3]. Efforts to improve nutrition must therefore be complemented by health education and the provision of basic services for water and sewage management, vital elements in rural development.

Southeast Asian liver fluke
In the Mekong Basin, as in Asia generally, another health risk comes from consuming raw or fermented fish and other aquatic animals that may contain the cysts of parasites, including liver and intestinal flukes. Particularly implicated in parasite transmission are common dishes such as koi pla (fish, salt, chilli, lemon and other ingredients) or partly fermented fish such as and pla ra [4]. Fermentation for several months or high concentrations of salt and spices may kill parasites, but cooking is the only way to ensure that fish is safe to eat [5].

Three-stage life cycle of liver fl ukes

 

Flukes are from a class of flatworm known as trematodes. Among fish-borne zoonotic trematodes (those that can be transmitted to humans), the most well-documented in the Mekong Basin is the Southeast Asian liver fluke Opisthorchis viverrini, a small fluke about 6-10 mm in length. Like many flukes, O. viverrini requires three hosts to complete its life cycle. Adult flukes typically live in the bile ducts of mammals, including dogs, cats, rats, pigs and humans, but they may also be found in the gall bladder and pancreatic ducts. Adults reproduce sexually, passing eggs with the bile into the host's small intestine, from where they eventually enter the environment in faeces. If the eggs reach a water body, they may be ingested by an aquatic snail. In the Mekong Basin, only snails in the genus Bithynia are suitable first intermediate hosts. They typically inhabit shallow, clear weedy waters such as rice paddies, and it appears that irrigation favours these snails by providing a suitable habitat year round. After passing through several stages within the snail, many cercariae - the free-swimming stage of the fluke - emerge from each snail and search for a fish, into which they burrow and encyst as metacercariae, which are usually found in the muscle and skin.

Southeast Asian liver fluke
(Opisthorchis viverrini)

The Southeast Asian liver fluke infects at least 93 species of fish in the Mekong Basin, and cyprinids seem to be particularly susceptible [6]. If a person eats infected parts of a fish raw, the fluke cysts rupture in the duodenum, releasing larvae that swim up the bile ducts, where they develop into adults. People who are infected typically have less than 50 flukes, but some individuals may harbour up to 3,000 [7, 8]. The flukes can live inside humans for up to ten years, so consumers of raw fish tend to accumulate a parasite burden as they get older. The adult flukes feed by sucking on the walls of the bile duct, ingesting blood, other fluids and fragments of tissue. Although some people appear not to be greatly affected, the parasites can cause a range of gastrointestinal symptoms, liver enlargement, and various other ill-effects, the most serious being cholangiocarcinoma, a cancer of the bile ducts that is usually fatal. The parasite has been dubbed 'the carcinogenic liver fluke' and liver cancer rates are high throughout northeast Thailand [4], with Khon Kaen province having the highest incidence of cholangiocarcinoma in the world [9].

Distribution in the Lower Mekong Basin
Northeast Thailand was considered the epicentre for Opisthorchis viverrini infection, which led to a major campaign from 1984-1994 to treat infected people, discourage people from eating raw fish, and reduce environmental contamination by faeces. Although the campaign had some success, infection rates remain high in rural areas where people eat raw or partly fermented fish, and where defecating outdoors is still commonplace. In Thailand, rates are highest in the north (19.3% of the population) and the northeast (15.7%), reflecting consumption of raw or fermented fish products. Rates are lower in central Thailand (3.8%) and are zero in the south [4].

In the Lao PDR the southeast Asian liver fluke is possibly more prevalent than in Thailand. Nationwide, the infection rate among primary school children is about 11% [10], and in rural areas average infection rates vary between about 44% and 95% [11]. In Cambodia, infection rates with intestinal parasites are high in rural areas, but infection with Opisthorchis is relatively rare, presumably because few people eat uncooked fish. In Kampong Cham, one study found only 4% of children had liver flukes [12] and in a study in Battambang, no children were infected with liver flukes [13].

Although present in southern Viet Nam, the Southeast Asian liver fluke seems uncommon, although there has been no comprehensive study in the Mekong Delta. But the similar Chinese liver fluke, Clonorchis sinensis, is common in parts of northern Viet Nam where fish is eaten raw. In one study, the infection rate was about 52% and all respondents were infected by at least one species of fish-borne fluke [14].

Other flukes transmitted by aquatic animals
It is only recently that the occurrence and prevalence of other fish-borne zoonotic trematodes has begun to be documented in the Mekong Basin, and there is even less information on the trematodes that are transmitted via other aquatic animals (see table below).

In the family Heterophyidae, at least seven species of intestinal flukes are now known to occur in the Lower Mekong Basin, and several of these are common.

These flukes are smaller (<1-2 mm) than Opisthorchis species and adults live in the intestine, where they may cause various ill effects, which usually increase in severity as the parasite load increases. Significant pathology in the heart, brain, and spinal cord of humans may also occur, thought to be caused by the atypical movement of fluke eggs through the circulatory system [15]. Heterophyid flukes live as adults in mammals and birds, and they infect snails and fish as intermediate hosts. In some parts of the basin, the rate of infection with intestinal flukes such as Haplorchis taichui is much higher than that of O. viverrini, which probably reflects the distribution of the intermediate snail hosts [7, 16].

Echinostomatids are also commonly found in humans in the Mekong Basin, and are probably most-often contracted by eating raw fish. But undercooked or raw molluscs, tadpoles or frogs may also be a significant route for infection.

Lethicodendriids and plagiorchids appear to be relatively rare in humans, as they are only contracted by people who eat raw or undercooked aquatic insects such as dragonfly or damselfly nymphs or naiads. However, in northeast Thailand, a study published in 1973 estimated an infection rate of 10-40% as a result of widespread consumption of raw dragonfly naiads (the aquatic nymphal stage) caught in flooded rice fields [17]. A possible infection route that has not been studied is the incidental ingestion of cysts in aquatic insects in the stomachs of fish that are eaten whole and uncooked.

Family           Species	Known definitive hosts	1st intermediate snail host	2nd intermediate host
Opisthorchiidae
Opisthorchis viverrini	Mammals, including dogs, cats, rats, pigs and man	Bithyniidae. 3 species of Bithynia in the Mekong Basin	Freshwater fish
Heterophyidae
Haplorchis taichui	Piscivorous birds and mammals, including cats, dogs, foxes and man	Thiaridae. Includes Melania spp. and Tarebia granifera in the Mekong Basin	Fish, freshwater and brackish species
Haplorchis yokogawai
Centrocestus formosanus
Centrocestus caninus
Stellantchasmus falcatus
Procerovum calderoni
Echinostomatidae
Echinochasmus japonicus	Birds and mammals, including cats dogs, pigs, rats and man	Lymnaeidae and Planorbidae	Snails, mussels, tadpoles, frogs, fish
Echinostoma malayanum
Echinostoma ilocanum
Echinostoma revolutum
Lecithodendriidae
Prosthodendrium molenkampi	Birds and mammals, including bats, primates - macaques, slow loris and man	Bithyniidae, Bithynia spp., Melania?	Dragonflies and damselflies
Phaneropsolus bonnei
Phaneropsolus spinicirrus
Plagiorchiidae
Plagiorchis harinasutai	Bats, some other mammals, birds, reptiles	Viviparidae Lymnaeidae	Aquatic insect larvae and nymphs, snails

Fish-borne flukes and aquaculture
The role of wild fish in transmitting some species of flukes is well-documented, but there is less information on fish grown in aquaculture systems. Some authors speculate that an increasing rate of human infection with the Chinese liver fluke in China and several other countries is a consequence of aquaculture development [18]. But studies in Viet Nam show that fluke infections in farmed fish vary greatly, depending upon such factors as proximity of fish to aquatic snails, the use of pelleted feed, the species cultured, and the presence of reservoir hosts. In the Mekong Delta, one study found that zoonotic trematode infection rates were low in aquaculture fish - 2.6% in catfish and zero in snakeheads, compared with an average infection rate of 10.3% for wild fish [19]. Another study [20] examined four kinds of aquaculture systems in the Mekong Delta and also found generally low rates of zoonotic fluke infection, with only heterophyid flukes detected. In intensive rearing systems, where fish were largely isolated from snails, few fish were infected. In farms raising walking catfish (Clarias), no fish were infected and in giant gourami farms only 1.7% of fish were infected. In the other two systems, human and animal waste was used and fish may have been near infected snails. In garden-pond-pigsty systems, known as VAC in Vietnamese, 3% of fish were infected and in carp polyculture systems, the infection rate was 6.6%. Infection rates increased in the flood season, consistent with greater proximity of fish to snails. Some fish species in aquaculture systems had higher infection rates than others, probably because they fed in shallow water where snails were present.

In a fish-farming area in northern Viet Nam, infection rates in farmed fish were much higher than those reported from the Mekong delta. About 45% of fish were infected with zoonotic trematodes, despite a very low infection rate of 0.6% in the fish farmers themselves [21]. The high incidence of cysts in fish may be a result of the presence of dogs, cats and pigs as reservoir hosts of adult flukes, as well as poor preparation of ponds, from which snails and other fish should be removed before restocking.

The occurrence of cysts in fishery products calls for continuing vigilance at fish processing factories, given the importance of aquaculture for exports in the region and the need to certify food safety.

Eliminating and avoiding fluke infections
Cooking all freshwater fish and other aquatic animals prevents any infection by zoonotic trematodes. Hence there is no need to be concerned about the safety of eating fishery products, providing they are cooked. People who have become infected as a result of eating raw or undercooked aquatic animals are treated with antibiotics, usually praziquantel, which is typically 100% effective for eliminating the parasites. It should also be noted that the problem of zoonotic parasite transmission is not confined to fish and other aquatic animals; all kinds of meat (including beef, lamb and pork) may transmit parasites, but it is the lack of cooking (or undercooking) that is the main health issue.The prevalence of zoonotic flukes can be reduced by improving human hygiene, but there is no practical means to completely eradicate these parasites in the environment. To do so, we would need to prevent dogs, cats, foxes, fish-eating birds and other primary hosts from eating raw fish, and we would also need to eradicate the snails that are intermediate hosts, which would be very difficult and ecologically undesirable [22].

*Kent Hortle was a technical advisor to the MRC Fisheries Programme from 2001 to 2005. He currently works as a Consultant on Fisheries and Environment and as an Honorary Research Associate at the Water Studies Centre of Monash University, Melbourne..

References

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