Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects

Trans R Soc Trop Med Hyg 2016; 110: 13–20
doi:10.1093/trstmh/trv103

REVIEW

Clonorchis sinensis and Opisthorchis spp. in Vietnam: current
status and prospects
Pham N. Doanha,* and Yukifumi Nawab
a

Institute of Ecology and Biological Resources, Viet Nam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay,
Hanoi, Viet Nam; bResearch Affairs Office, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
*Corresponding author: Tel: +84 91272 3177; E-mail:

Received 8 September 2015; revised 21 November 2015; accepted 25 November 2015

Keywords: Clonorchis sinensis, Intermediate hosts, Opisthorchis spp., Small liver flukes, Vietnam

Introduction
Small liver flukes of the genera Clonorchis, Loos, 1907, and
Opisthorchis Blanchard, 1895, in the family Opisthorchiidae,
exploit freshwater snails and fish as the first and second intermediate hosts, respectively.1 The final hosts, fish-eating birds
and mammals, including humans, are infected by eating fish harbouring infective metacercariae.1 The genus Clonorchis contains
only one species, C. sinensis, a parasite of mammals, whereas
the genus Opisthorchis includes more than 50 species, of which
about 30 are parasites of birds.2 The most important members
of these genera for human health are C. sinensis, Opisthorchis
viverrini and O. felineus, each of which annually infect thousands
of people, mainly in Asian countries. There is a close association
between infection with these flukes and incidence of cholangiocarcinoma.1 Approximately 700 million people are at risk of infection by these liver flukes through the consumption of raw or
partially cooked freshwater fish (mainly cyprinid fish).3

In Vietnam, all three medically important small liver flukes
have been recorded in dogs, cats and humans, and three other
Opisthorchis species, O. chelis, O. longsissimus and O. parageminus, have been found in wild and domestic birds.4–6 However,

the record of O. felineus in Vietnam was confirmed to be a misidentification of O. viverrini.5 For a long time, much attention has
focused on the two medically important species, C. sinensis and
O. viverrini, which were assumed to cause a serious public health
problem in some endemic areas in northern (for C. sinensis) and
central (for O. viverrini) Vietnam. In fact, numerous reports
about the high prevalence of these flukes in humans/mammals,
fish and also snail hosts were previously published in domestic
journals.5–24 From 2004 to 2012, the Fish-borne Zoonotic
Parasites (FIBOZOPA) project was conducted as collaboration
between the Danish International Development Agency
(DANIDA) and the Vietnam government. Extensive surveys during
this project revealed that the prevalence of C. sinensis and
O. viverrini in humans, as well as in intermediate hosts, were far
lower than that reported in the earlier surveys.25–34 Discrepancies
between the earlier reports and the recent results of FIBOZOPA
are largely due to mis identification of small fluke eggs in faecal
samples in the earlier studies. Opisthorchiidae eggs, including
those of C. sinensis and O. viverrini, are highly similar to those of
minute intestinal flukes of the family Heterophyidae, leading to frequent mis-diagnosis. Those minute intestinal flukes often co-infect
humans alongside C. sinensis or O. viverrini, causing further

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Clonorchis sinensis and Opisthorchis viverrini are clinically important small liver flukes because of their known
association with development of cholangiocarcinoma. In Vietnam, high prevalence of C. sinensis infection in
humans was previously reported in northern provinces, and O. viverrini infection has been detected in several
central provinces. However, diagnosis of C. sinensis and O. viverrini infections in the past was merely based on
faecal egg examination. This method alone can lead to misidentification at the species level because of morphological similarity between the eggs of these liver flukes and minute intestinal trematodes of the family
Heterophyidae. In fact, recent surveys in Vietnam revealed that infection with several minute intestinal flukes,
such as Haplorchis pumilio and H. taichui, are much more common than infection with C. sinensis or O. viverrini,
and they often co-infect humans. Thus, previously reported prevalence of small liver fluke infection in Vietnam
was likely over-estimated due to mis identification of parasites in copro-parasitological examinations. In addition, there is some confusion about identification of cercariae, metacercariae and also adults of C. sinensis
and O. viverrini in intermediate and definitive hosts. The aim of this review is, therefore, to draw realistic pictures
of the past and present scientific reports on the epidemiology and biology of C. sinensis and Opisthorchis spp.
infection in Vietnam.


P. N. Doanh and Y. Nawa

diagnostic confusion. The purpose of this review is, therefore, to
update information about C. sinensis and Opisthorchis spp. to
work the real epidemiological situation and prospects of these
liver flukes in Vietnam. In addition, the epidemiological and biological data of these liver flukes from neighbouring countries are
also discussed herein.

History of the detection of Clonorchis sinensis
and Opisthorchis species

Epidemiology and prevalence of Clonorchis
sinensis and Opisthorchis viverrini infection
in humans

Clonorchis sinensis infection has been reported from many parts
of east Asia (Russia, Japan, Korea and China), whereas O. viverrini
infection has been reported from Thailand, Laos and Cambodia
with prevalence reaching 100% in some endemic areas.39–45 In
Japan, clonorchiasis cases have drastically decreased in number
since the 1960s and there have been no new case reports since
1991.46 Elsewhere, high prevalence of small liver fluke infection
is still maintained in some areas. For example, up to 85% of villagers in some parts of China are infected with C. sinensis.42

Figure 1. Opisthorchis spp. found in Vietnam. (A) Opisthorchis longsissimus; (B) Opisthorchis chelis; (C) Opisthorchis parageminus, and (D) Opisthorchis
viverrini. Scale bar: 2 mm. Reproduced from Le4 with the author’s permission. Note: morphological differences in body size, form and size of testes, and
vitelline glands are observed among species.

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In Vietnam, C. sinensis and O. felineus were first reported from
humans in 1887 and 1907, respectively.5 Much later (in 1994),
O. viverrini infection was found among residents in Phu Yen province, central Vietnam.11 While C. sinensis and O. viverrini infection
in humans and animal reservoir hosts have been continuously
reported in the endemic areas,4–34 O. felineus has never been
reported after the initial report. Recently, the O. felineus specimens, which were collected in Vietnam and deposited in the US
National Parasite Collection in the Agricultural Research Services,
US Department of Agriculture (ARS/USDA), were re-identified as
O. viverrini.5 Thus, the existence of O. felineus is rather unlikely in
Vietnam.
In addition to C. sinensis and O. viverrini, three other Opisthorchis
species, O. cheelis, O. longissimus and one unidentified Opisthorchis
sp., were collected from wild and domestic birds in 1968.35 The

unidentified species was then described as a new species, named
O. parageminus, in 1970.36 Although details of these avian

Opisthorchis species (Figure 1) are given in the textbook Fauna of
Vietnam published in 2000 in Vietnamese language,4 they were
not recognised even by Vietnamese parasitologists. Recently Dao
et al. collected liver flukes from domestic ducks and mistakenly
claimed the first finding of Opisthorchis in birds in Vietnam. They
identified these specimens as O. viverrini although their morphological appearances and molecular sequence data indicated that
they were not O. viverrini.37 From the description and the drawing,
Nawa et al.38 pointed out that the specimens collected by Dao
et al. are morphologically identical to O. parageminus that were
previously recovered from ducks in northern Vietnam.4,36 Thus,
C. sinensis and four Opisthorchis species (one mammalian and
three avian species) are present in Vietnam (Table 1).


Transactions of the Royal Society of Tropical Medicine and Hygiene

Table 1. Distribution and definitive hosts of Clonorchis sinensis and Opisthorchis species in Vietnam
Species

Definitive hosts

Distribution

C. sinensis 4,5,24
O. viverrini 5,11,12,16,17,22,50
O. longissimus 4,35,36
O. parageminus 4,35,36

Dog, cat, human
Cat, human
Mallard duck (Anas platyrynchos dom.)
Mallard duck (Anas platyrynchos dom.), Muscovy duck
(Cairina moschata), chicken (Gallus gallus dom.)
Wild birds (Falco tinnuculus, Circus melanoleucos)

Northern provinces
Central and Southern provinces
Hanoi (North)
Northern provinces

O. cheelis 4,35,36

Stellantchasmus falcatus and Centrocestus formosanus, whereas
C. sinensis was rarely found in the same samples.25,32 For example,
Dung et al.25 found small trematode eggs in 64.9% of stools from
residents living in Nghia Hung district, Nam Dinh province.
However, 33 patients, who were selected to deworm for identification of trematodes species, showed extremely high infection rates of
small intestinal trematodes, H. pumilio (100% and 416.2 flukes/
patient) and H. taichui (69.7% and 40.1 flukes/patient), but only a
half of them (51.5%) were infected with C. sinensis at low intensity
of 4.2 flukes/patient.25 These results strongly suggest that estimated
prevalence of clonorchiasis and opisthorchiasis in the past in
Vietnam were greatly inflated due to misidentification.
Misdiagnosis of opisthorchiasis due to misidentification of
parasite species had also happened in Nan province in northern
Thailand, where H. taichui was highly endemic but O. viverrini
was rarely detected.53 Also, misidentification of eggs could help

explain the apparent limited reduction of C. sinensis infection
after mass screening and treatment associated with prevention
campaigns during 1980–2000. For example, the prevalence in
Dong Huong commune, Kim Son district, Ninh Binh province,
was 18.5% in 1994 and 22.5% in 1995.14 Similarly, in Nghia Phu
commune, Nghia Hung district, Nam Dinh province, the prevalence of C. sinensis infection was 30.2% in 1976, 33% in 1977
and 35% in 1996–1998.14, 20,23,24 These apparent treatment failures might be due, in part, to repeated, but unrecognised, infections with minute intestinal flukes.

Infection rates in animal reservoir hosts
The reservoir hosts of C. sinensis and O. viverrini are a wide range of
wild and domestic fish-eating mammals, e.g., foxes, domestic
dogs, cats, pigs and rodents.41,42 Of these, cats, dogs and pigs
are considered most important. High prevalence of C. sinensis
infection in cats (70%), dogs (50%) and pigs (27%) were reported
in southern China.42,54 Similarly, relatively high infection rates of
O. viverrini in cats were reported in northeastern Thailand
(36.4%) and in Lao PDR (20–36%).54
In Vietnam, domestic cats and dogs were found to be the main
reservoir hosts. Similar to the situation in humans, high infection
rates of C. sinensis in cats (68.1–92.0%) and dogs (40.1–67.0%)
were reported in Ninh Binh and Nam Dinh provinces in earlier
times, 1980–1996.8,10,15 However, despite a lack of treatment/
prevention programs for clonorchiasis in domestic animals, recent
surveys have revealed quite low prevalence of 8.5% in dogs and
16.6% in cats in northern provinces.55 Clonorchis sinensis was

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Similarly, prevalence of O. viverrini is as high as 70% in some communities in northeast Thailand and 58.5% in an endemic area of
Laos.43–45 Thus, C. sinensis and O. viverrini infections are still a
problem in some countries. Except for a single report of C. sinensis
infection in central east Thailand,47 no geographical overlap has
been seen in the distributions of these liver flukes.48
In Vietnam, clonorchiasis is endemic among human populations in northern provinces, whereas opisthorchiasis is detected
in central provinces. To date, C. sinensis infection in humans has
been reported in almost all northern provinces (Figure 2).5–24
Prevalence varied from 0.2 to 37.5% with the highest levels
(26.0–37.5%) being recorded in Nam Dinh province, followed by
Ninh Binh province (23.5–31.0%).5–24 These two provinces were
always considered as hotspots of C. sinensis infection. An apparent anomaly was the report of 76 human clonorchiasis cases in
Thuan Hanh commune, Dak Nong province in central Vietnam
near Cambodia.49 However, all those infected people had
migrated from Nam Dinh and Ninh Binh provinces of northern
Vietnam, and it was concluded that they had acquired the infection in their home town.49
Opisthorchis viverrini infections have been found amongst people living in 10 central provinces (Figure 2) with prevalence ranging
from 0.3 to 36.9%, and Phu Yen province was considered a ‘hot
spot’.11,12,16–18,22 In the south of the country, human cases
have never been reported, although O. viverrini metacercariae
were found in snakehead fish, Channa striata (Channidae), in An
Giang province26 and adult worms were found from cats in Tay
Ninh province.50
It should be noted that in the past, diagnosis of C. sinensis and
O. viverrini infections in Vietnam was made merely based on the
detection of small fluke eggs in stool samples. It is difficult,
or practically impossible, to distinguish the eggs of the family
Opisthorchiidae, including C. sinensis and Opisthorchis species, from
those of minute intestinal flukes of the family Heterophyidae.1 All
of them are characterized by small size, rough and thick shells

with an operculum at one end.51,52 Although small intestinal flukes
of the family Heterophyidae had been detected in animals in
Vietnam,4 they had never been thought of as human pathogens
until the FIBOZOPA project revealed their presence, together with
C. sinensis, among inhabitants of Ninh Binh and Nam Dinh provinces,
which were considered as hyperendemic for clonorchiasis.25–34 In
recent surveys, small fluke eggs were detected in 22.7–64.9% and
9.4–30.9% of stool samples from residents in Nam Dinh and
Ninh Binh province, respectively.25,32,34 Surprisingly, most of the
trematodes recovered after deworming were identified as minute
intestinal flukes, Haplorchis pumilio, H. taichui, H. yokogawai,

Northern provinces


P. N. Doanh and Y. Nawa

commonly found.28 Very recently, Hung et al. detected small
trematode eggs in 32.7% of dog faecal samples, 49.0% of cats
and 13.0% of pigs in Gia Vien district, Ninh Binh province, without
identification to the species level.34 Although C. sinensis adult
worms were reported from cats at a slaughterhouse in Da Nang
province, central Vietnam,56 their geographical origin is unknown.
Whether C. sinensis is endemic in Da Nang province remains to be
determined.
As to the animal reservoir hosts for O. viverrini, the infection rates
varied from 30 to 60% in cats in Phu Yen province, central
Vietnam,14,17 and was 17.8% in cats in Tay Ninh province, southern
Vietnam where human opisthorchiasis has not been reported.50

The second intermediate hosts

not detected in domestic cats, dogs or pigs in Nghe An province,
where infections with several minute intestinal flukes were

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Figure 2. A map showing the distribution of Clonorchis sinensis and
Opisthorchis viverrini in Vietnam. Clonorchiasis and opisthorchiasis
endemic provinces are indicated by black color and grids, respectively.
Nam Dinh and Ninh Binh provinces in the north are known as hotspots
of clonorchiasis, whereas Phu Yen province in the central Vietnam is a
hotspot of opisthorchiasis. Clonorchiasis patients in Dak Nong province
were the immigrants from Nam Dinh and Ninh Binh provinces. In Da
Nang province, C. sinensis was found in cats at the slaughterhouse, but
no human cases in this province. In the south, O. viverrini adult worms
were found in cats in Tay Ninh province and metacercariae in fish in An
Giang province, but O. viverrini infection in humans has never been
reported. In Vinh Long province, C. sinensis metacercariae was reported
to be found in catfish, but its identification is doubtful.

Various fish species can serve as the second intermediate hosts of
liver flukes. While O. viverrini preferentially infect cyprinids,
C. sinensis can infect not only cyprinids but also an array of
other fish families.48,54 In China, 132 fish species (including 71
cyprinids) in 46 genera belonging to 11 families were listed as
second hosts, with prevalence up to 95%.42 In the greater
Mekong sub-region of southeast Asia, O. viverrini can infect

more than 40 species of cyprinids from 18 genera with extremely
variable prevalence ranging from 2.1 to 100%.44,54
Early studies in northern Vietnam reported metacercariae
of C. sinensis in seven fish species (Tilapia mossambica,
Hypothalmichthys molitrix, Anabas testudineus, Cyprinus carpio,
Carassius carassius, Mylopharyngedon piceus and Cirrhina molitrorella) with extremely high prevalence of infection (13–100%).5,6 In
these previous reports, no strict morphological discrimination was
made between metacercariae of C. sinensis and those of minute
intestinal flukes. The FIBOZOPA project (2004–2012) reported for
the first time that metacercariae of the latter group were much
more common than those of C. sinensis.25–34 In contrast to the
earlier reports, the surveys conducted by FIBOZOPA project found
metacercariae of various minute intestinal trematodes (Haplorchis
pumilio, H. taichui, H. yokogawai, Centrocestus formosanus,
Stellantchasmus falcatus, Procerovum varium and Echinochasmus
japonicus), whereas C. sinensis metacercariae were not found in
Nghe An province,27 or were rarely found in Nam Dinh (only one
out of 1185 silver carp Hypophthalmichthys molitrix),29–31 and in
Ninh Binh (only one out of eight sharpbelly fish, Hemiculter leucisculus),34 as well as very low infection rates in other northern provinces
(from 0.1 to 0.4% of 1500 fish of five species).33 Taking all these
recent reports together, the prevalence of C. sinensis metacercariae
in fish in northern Vietnam is far lower than reported previously.
Surprisingly, C. sinensis metacercariae were reported from catfish, Pangasianodon hypophthalmus (family Pangasiidae) in Vinh
Long province in southern Vietnam.57 However, the authors
reported that the 28S sequence of these samples was considerably (8.3%) different from that of C. sinensis in the DNA database
in Genbank, suggesting that the metacercariae they found are not
C. sinensis. Unfortunately, the sequence data of these samples
have not been deposited in Genbank, so we are unable to check
the sequence similarities of these samples with other trematodes.
Because the catfish (Pangasianodon hypophthalmus) is an important product for export, re-analysis of the molecular data is

required to validate this report.
While extensive surveys have been done on C. sinensis infection
in fish intermediate hosts, not much work has been done on the


Transactions of the Royal Society of Tropical Medicine and Hygiene

prevalence of O. viverrini metacercariae in Vietnam. To date, only
two fish species have been identified as second intermediate
hosts for O. viverrini. The prevalence in crucian carp, Carassius
carassius, in Phu Yen province was 10–29%,17 and those of snakehead fish, Channa striata, in An Giang province in southern
Vietnam was as low as 1.9%.26 In fact, the identification of
O. viverrini metacercariae recovered from snakehead fish was
uncertain, because it was not possible to infect laboratory animals
for adult worm recovery.26 Since fish intermediate hosts for
O. viverrini is restricted to cyprinoids in the endemic areas other
than Vietnam,54 detection of O. viverrini metacercariae in snakehead fish of the family Pangasiidae is quite unusual. Further
confirmation is necessary to include or exclude snakehead fish
as the second intermediate host for O. viverrini.

The first intermediate hosts

Conclusions and prospects
Clonorchis sinensis and four Opisthorchis species from mammals
and birds are present in Vietnam. Among these, C. sinensis and
O. viverrini have been paid much attention because of their medical importance. They have been reported from intermediate and
definitive hosts, including humans, with high prevalence in some
areas. However, there was some confusion about the identification of the parasites. In early publications in Vietnam, not much
attention was paid to differentiate C. sinensis and O. viverrini
from closely related minute intestinal flukes of the family

Heterophyidae, resulting in inaccurate information (summarized
in Table 3) concerning epidemiology as well as the identification
of the first and second intermediate hosts. In this review, we

Table 2. The first intermediate hosts of Clonorchis sinensis and Opisthorchis viverrini in different countries
Country

Snail hosts of C. sinensis

Russia54,58
Japan46
Korea59
China42,54

Parafossalurus manchouricus
Parafossarulus manchouricus,
Parafossarulus manchouricus
Parafossarulus manchouricus,
Alocinma longicornis,
Parafossarulus sinensis
Semisulcospira cancellata,
Bithynia fuchsianus, B. robustus, Melanoides tuberculatus,
Assiminea lutea
Parafossarulus manchouricus, Melanoides tuberculatus,a
Bythinia siamensis, 5,13,14,21,62

Vietnam
Lao60
Thailand54,60
Cambodia61

a

Snail hosts of O. viverrini

Melanoides tuberculatus a and Maningila sp.a,18,20,22
Bithynia siamensis goniomphalos
Bithynia funiculata,
Bithynia siamensis gomiomphalos, Bithynia siamensis siamensis
Bithynia siamensis siamensis

Misidentification possibility.

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Although many fish species serve as the second intermediate
hosts, very few species of snails can act as first intermediate
hosts.42,54,58–62 Reported snail hosts of C. sinensis and O. viverrini
from different countries are listed in Table 2. While O. viverrini is
restricted to three Bythinia snail species, Parafossalurus manchouricus is an important host for C. sinensis in all endemic countries, although this fluke can infect other snails in China. The
prevalence of C. sinensis and O. viverrini infection in snail hosts is
usually lower than 2%.44 However, prevalence of O. viverrini can
be over 8% in Bythinia snails in Thailand and that of C. sinensis
reached 27% in Parafossalurus species in China.41,42,54
In Vietnam, few data are available concerning snail hosts. In
previous surveys, three snail species, Melanoides tuberculatus,
Parafossarulus manchouricus and Bythinia siamens is, were identified as the first intermediate hosts for C. sinensis in northern provinces with prevalence ranging from 4.9 to 90%.13,14,21,62 An
infection rate in snails of 90% is unusually high compared with
any other reports from highly endemic areas of other countries,

even in highly endemic areas of China.42,54 In recent surveys in
Nam Dinh province, C. sinensis cercariae were not found in snails
examined.34
As the first intermediate hosts for O. viverrini, two snail species,
Melanoides tuberculatus and Maningila sp., were reported with
infection rates of 2.6–8.0% in Phu Yen province and 0.2% in Dak
Lak province.18,20,22 As can be seen in Table 2, except for
Vietnam, O. viverrini and C. sinensis exploit entirely different snail
species. Only in Vietnam, both O. viverrini and C. sinensis were
reported from M. tuberculatus. In addition, as mentioned above
that O. viverrini are restricted to Bithynia snails,54 the role of
M. tuberculatus and also Maningila sp. as the first intermediate
hosts of O. viverrini in Vietnam is questionable. Since all members
of the families Opisthorchiidae and Heterophyidae have similar
pleurolophocercous cercariae,63 morphological identification of
cercariae to species is extremely difficult. The identification of
the first intermediate snail hosts of C. sinensis and O. viverrini in
Vietnam require further extensive surveys using molecular tools
and experimental infections.


P. N. Doanh and Y. Nawa

Table 3. Uncertain reports on the location and hosts of Clonorchis sinensis and Opisthorchis viverini in Vietnam
Fluke
species

Human case

C. sinensis

In Dak Nong province Cats at slaughter house in Da Melanoides tuberculatus, Parafossarulus
Catfish in Vinh Long
in the central49
Nang province in central56
manchouricus, Bythinia siamensis 5,13,14,21,62
province in the south57
18,20,22
Ducks in Phu Yen province,
Melanoides tuberculatus and Maningila sp.
Snakehead fish in An
central37
Giang province26

O. viverrini

Reservoir host

1st intermediate host

2nd intermediate host

Note: Probable overestimation of the prevalence in human, animals, fish and snail hosts were not included in this table.

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Acknowledgements: The authors are most grateful to Dr. David Blair,
James Cook University, for his careful proof reading of this manuscript.
Authors’ contributions: PND wrote the first draft of the manuscript; YN
reviewed and edited it. Subsequent revisions were made in collaboration
of both authors. Both authors read and approved the final version of the
paper. PND and YN are the guarantors of the paper.

Funding: None.
Competing interests: None declared.
Ethical approval: Not required.

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attempted to draw realistic pictures of the past and present scientific understanding of the epidemiology of C. sinensis and
Opisthorchis species in Vietnam. Based on this, future studies
may be planned to obtain more accurate information on the
life-cycle, epidemiology and transmission dynamics of these
medically important liver flukes.
Clonorchis sinensis is known to be widely distributed in northern
provinces, whereas O. viverrini is present in central and southern

provinces of Vietnam. This segregation is consistent with the
broader natural distribution of the two species. While C. sinensis
is endemic in the far east of Russia and East Asia from Korea
through much of China, including regions close to northern
Vietnam, O. viverrini is found in the Lower Mekong, from the
north and northeast of Thailand, Lao PDR and Cambodia close
to central and southern Vietnam. Two uncertain reports of
C. sinensis in cats in a central province and its metacercariae in
catfish in a southern province, together with mis identification
of O. viverrini from ducks, may incorrectly reflect the distributions
of these flukes. It is important to know whether these distributions have a clear-cut border or not, and to know which factors
decide this segregation. Since Vietnam is the only country in
which both species occur, it provides us with a good opportunity
to address the above questions. The clarification of the life cycles
of C. sinensis and O. viverrini in every endemic area in Vietnam will
provide the best answers, and are necessary to elucidate the
biology and ecology as well as for the control of these zoonotic
parasites.


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