Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects alone can lead to misidentification at the species level because of morom phological similarity between the eggs of these liver flukes and minute intestinal trematodes of the family h t t heterophyidae.
Trang 1Clonorchis sinensis and Opisthorchis spp in Vietnam: current
status and prospects Pham N Doanha,* and Yukifumi Nawab
*Corresponding author: Tel: +84 91272 3177; E-mail: pndoanh@yahoo.com
Received 8 September 2015; revised 21 November 2015; accepted 25 November 2015 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
mor-phological 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
add-ition, 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
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
and mammals, including humans, are infected by eating fish
only one species, C sinensis, a parasite of mammals, whereas
the genus Opisthorchis includes more than 50 species, of which
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
infec-tion by these liver flukes through the consumpinfec-tion of raw or
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
the record of O felineus in Vietnam was confirmed to be a
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
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
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 fre-quent mis-diagnosis Those minute intestinal flukes often co-infect humans alongside C sinensis or O viverrini, causing further
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Trang 2diagnostic 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
bio-logical data of these liver flukes from neighbouring countries are
also discussed herein
History of the detection of Clonorchis sinensis
and Opisthorchis species
In Vietnam, C sinensis and O felineus were first reported from
O viverrini infection was found among residents in Phu Yen
in humans and animal reservoir hosts have been continuously
reported after the initial report Recently, the O felineus
speci-mens, 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
Vietnam
In addition to C sinensis and O viverrini, three other Opisthorchis
species, O cheelis, O longissimus and one unidentified Opisthorchis
unidentified species was then described as a new species, named
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 morpho-logical appearances and molecular sequence data indicated that
et al are morphologically identical to O parageminus that were
C sinensis and four Opisthorchis species (one mammalian and
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
Japan, clonorchiasis cases have drastically decreased in number since the 1960s and there have been no new case reports since
is still maintained in some areas For example, up to 85% of
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 Le 4 with the author’s permission Note: morphological differences in body size, form and size of testes, and vitelline glands are observed among species.
Trang 3Similarly, prevalence of O viverrini is as high as 70% in some
com-munities in northeast Thailand and 58.5% in an endemic area of
problem in some countries Except for a single report of C sinensis
In Vietnam, clonorchiasis is endemic among human
popula-tions in northern provinces, whereas opisthorchiasis is detected
in central provinces To date, C sinensis infection in humans has
Prevalence varied from 0.2 to 37.5% with the highest levels
(26.0–37.5%) being recorded in Nam Dinh province, followed by
always considered as hotspots of C sinensis infection An
appar-ent anomaly was the report of 76 human clonorchiasis cases in
Thuan Hanh commune, Dak Nong province in central Vietnam
migrated from Nam Dinh and Ninh Binh provinces of northern
Vietnam, and it was concluded that they had acquired the
Opisthorchis viverrini infections have been found amongst
from 0.3 to 36.9%, and Phu Yen province was considered a ‘hot
have never been reported, although O viverrini metacercariae
were found in snakehead fish, Channa striata (Channidae), in An
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
of them are characterized by small size, rough and thick shells
of the family Heterophyidae had been detected in animals in
until the FIBOZOPA project revealed their presence, together with
C sinensis, among inhabitants of Ninh Binh and Nam Dinh provinces,
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
trematodes recovered after deworming were identified as minute
intestinal flukes, Haplorchis pumilio, H taichui, H yokogawai,
Stellantchasmus falcatus and Centrocestus formosanus, whereas
residents living in Nghia Hung district, Nam Dinh province However, 33 patients, who were selected to deworm for identifica-tion of trematodes species, showed extremely high infecidentifica-tion 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
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
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,
commune, Nghia Hung district, Nam Dinh province, the preva-lence of C sinensis infection was 30.2% in 1976, 33% in 1977
fail-ures might be due, in part, to repeated, but unrecognised, infec-tions 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
are considered most important High prevalence of C sinensis infection in cats (70%), dogs (50%) and pigs (27%) were reported
O viverrini in cats were reported in northeastern Thailand
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
prevention programs for clonorchiasis in domestic animals, recent surveys have revealed quite low prevalence of 8.5% in dogs and
Table 1 Distribution and definitive hosts of Clonorchis sinensis and Opisthorchis species in Vietnam
C sinensis 4 , 5 , 24 Dog, cat, human Northern provinces
O viverrini5,11,12,16,17,22,50 Cat, human Central and Southern provinces
O longissimus 4 , 35 , 36 Mallard duck (Anas platyrynchos dom.) Hanoi (North)
O parageminus4,35,36 Mallard duck (Anas platyrynchos dom.), Muscovy duck
(Cairina moschata), chicken (Gallus gallus dom.)
Northern provinces
O cheelis4,35,36 Wild birds (Falco tinnuculus, Circus melanoleucos) Northern provinces
Trang 4not detected in domestic cats, dogs or pigs in Nghe An province,
where infections with several minute intestinal flukes were
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
worms were reported from cats at a slaughterhouse in Da Nang
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
The second intermediate hosts 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
cyprinids) in 46 genera belonging to 11 families were listed as
Mekong sub-region of southeast Asia, O viverrini can infect more than 40 species of cyprinids from 18 genera with extremely
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
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
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
Ninh Binh (only one out of eight sharpbelly fish, Hemiculter
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 cat-fish, Pangasianodon hypophthalmus (family Pangasiidae) in Vinh
reported that the 28S sequence of these samples was consider-ably (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 import-ant 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
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.
Trang 5prevalence 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
snake-head fish, Channa striata, in An Giang province in southern
O viverrini metacercariae recovered from snakehead fish was
uncertain, because it was not possible to infect laboratory animals
O viverrini is restricted to cyprinoids in the endemic areas other
snake-head 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
Although many fish species serve as the second intermediate
hosts, very few species of snails can act as first intermediate
restricted to three Bythinia snail species, Parafossalurus
man-chouricus is an important host for C sinensis in all endemic
coun-tries, although this fluke can infect other snails in China The
prevalence of C sinensis and O viverrini infection in snail hosts is
be over 8% in Bythinia snails in Thailand and that of C sinensis
In Vietnam, few data are available concerning snail hosts In
previous surveys, three snail species, Melanoides tuberculatus,
Parafossarulus manchouricus and Bythinia siamens is, were
identi-fied as the first intermediate hosts for C sinensis in northern
infection rate in snails of 90% is unusually high compared with
any other reports from highly endemic areas of other countries,
Nam Dinh province, C sinensis cercariae were not found in snails
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
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
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
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
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 med-ical 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 identifica-tion of the parasites In early publicaidentifica-tions 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
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 Snail hosts of O viverrini
Russia 54 , 58 Parafossalurus manchouricus
Japan 46 Parafossarulus manchouricus,
Korea 59 Parafossarulus manchouricus
China 42 , 54 Parafossarulus manchouricus,
Alocinma longicornis, Parafossarulus sinensis Semisulcospira cancellata, Bithynia fuchsianus, B robustus, Melanoides tuberculatus, Assiminea lutea
Vietnam Parafossarulus manchouricus, Melanoides tuberculatus, a
Bythinia siamensis, 5 , 13 , 14 , 21 , 62
Melanoides tuberculatus a and Maningila sp a, 18 , 20 , 22
Bithynia siamensis gomiomphalos, Bithynia siamensis siamensis
a Misidentification possibility.
Trang 6attempted to draw realistic pictures of the past and present
scien-tific 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
distribu-tions 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
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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