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

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.

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: pndoanh@yahoo.com Received 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 # The Author 2015 Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene All rights reserved For permissions, please e-mail: journals.permissions@oup.com 13 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 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 Opisthorchis spp found in Vietnam (A) Opisthorchis longsissimus; (B) Opisthorchis chelis; (C) Opisthorchis parageminus, and (D) Opisthorchis viverrini Scale bar: 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 14 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 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 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 15 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 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 16 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 Figure 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 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 17 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 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 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 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 References King S, Scholz T Trematodes of the family Opisthorchiidae: a minireview Korean J Parasitol 2001;39:209–21 Biology Catalog Index of the Described Animalia of the World; 2007 http://bug.tamu.edu/research/collection/hallan/test/Platyhelminthes/ Family/Opisthorchiidae.txt [accessed 18 June 2007] Keiser J, Utzinger J Food-borne trematodiases Clin Microbiol Rev 2009;22:466–83 Le NT Fauna of Vietnam Vol Trematodes of Humans and Animals [in Vietnamese] Hanoi: Science and Techniques Publishing House; 2000 De NV, Murrell KD, Cong LD et al The food-borne trematode zoonoses of Vietnam Southeast Asian J Trop Med Public Health 2003;34: 12–34 De NV The fishborne trematodes in Vietnam Southeast Asian J Trop Med Public Health 2004;35:299–301 Chau LV, Chuyen TV The result of investigation for clonrochiasis by epidemiological approach Scientific report of research on medicine [in 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from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 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 Transactions of the Royal Society of Tropical Medicine and Hygiene 15 Khue PV, Thuy NH Study on clonorchiasis and the transmission route from animals to humans [in Vietnamese] J Pract Health 1996;3:27 35 Le NT Trematodes of birds and mammals in Northern Vietnam [in Russian] [thesis] Moscova: USSR Academy of 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88:177–86 Downloaded from http://trstmh.oxfordjournals.org/ by guest on January 6, 2016 20 ... 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. .. Tropical Medicine and Hygiene Table 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... 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,