[en] Foodborne zoonotic trematode (FZT) infections are common neglected tropical diseases in Southeast Asia. Their complicated life cycles involve freshwater snails as intermediate hosts. A cross-sectional study was conducted in Yen Bai and Thanh Hoa provinces in North and Central Vietnam, to investigate the diversity of cercariae of potential FZT and to construct the phylogenetic relationship of trematode cercariae based on the Internal Transcribed Spacer 2 (ITS2) region. Among 17 snail species collected from various habitats, 13 were infected by 10 cercarial groups among which parapleurolophocercous, pleurolophocercous, and echinostome cercariae were of zoonotic importance. The monophyletic tree separated cercarial sequences into different groups following the description of the cercariae families in which Haplorchidae, Opisthorchiidae, Echinochasmidae, and Echinostomatidae are important families of FZT. The overall prevalence was different among snail species and habitats and showed a seasonal trend. Parapleurolophocercous and echinostome cercariae emerged as the most common cercariae in snails in Yen Bai, while monostome, echinostome, and megalura cercariae were most common in Thanh Hoa. Using a molecular approach, we identified Parafossarulus striatulus as the first intermediate snail host of Clonorchis sinensis in Thac Ba Lake. Melanoides tuberculata and Bithynia fuchsiana were we identified preferred intermediate snail hosts of a diverse range of trematode species including intestinal flukes (i.e., Haplorchis pumilio and Echinochasmus japonicus) in Yen Bai and Thanh Hoa, respectively.
Precision for document type :
Analysis of case law/Statutory reports
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Nguyen Thi Xuan Phuong ✱; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) ; Institute of Ecology and Biological Resources > Department of Nematology
Bui, Dung Thi ✱; Institute of Ecology and Biological Resources, Hanoi, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Ha Noi, Vietnam. dung_parasitologist@yahoo.com ; Graduate University of Science and Technology, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Cau Giay, Ha Noi, Vietnam. dung_parasitologist@yahoo.com
Lempereur, Laetitia ✱; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
✱ These authors have contributed equally to this work.
Language :
English
Title :
Insights on foodborne zoonotic trematodes in freshwater snails in North and Central Vietnam
Alternative titles :
[en] Insights on foodborne zoonotic trematodes in freshwater snails in North and Central Vietnam
Original title :
[en] Insights on foodborne zoonotic trematodes in freshwater snails in North and Central Vietnam
Publication date :
March 2021
Journal title :
Parasitology Research
ISSN :
0932-0113
eISSN :
1432-1955
Publisher :
Springer Science and Business Media Deutschland GmbH, Germany
Special issue title :
Insights on foodborne zoonotic trematodes in freshwater snails in North and Central Vietnam
ARES CCD - Académie de Recherche et d'Enseignement Supérieur. Coopération au Développement Nafosted - National Foundation for Science and Technology Development
Funding number :
106.05-2017.26
Funding text :
The study was mainly supported by the international project “Foodborne Zoonotic Trematode infections and integrated control in Vietnam” (FOODTINC) and the Académie de recherche et d’enseignement supérieur (ARES-CCD), Belgium, and partly by the national project for molecular work under grant number 106.05-2017.26 funded by the Vietnam National Foundation for Science and Technology Development (NAFOSTED).
Anucherngchai S, Tejangkura T, Chontananarth T (2016) Epidemiological situation and molecular identification of cercarial stage in freshwater snails in Chao-Phraya Basin. Central Thailand Asian Pac J Trop Biomed 6:539–545. 10.1016/j.apjtb.2016.01.015 DOI: 10.1016/j.apjtb.2016.01.015
Anucherngchai S, Tejangkura T, Chontananarth T (2017) Molecular confirmation of trematodes in the snail intermediate hosts from Ratchaburi Province, Thailand. Asian Pac. J. Trop. Dis 7:286–292. 10.12980/apjtd.7.2017D6-399 DOI: 10.12980/apjtd.7.2017D6-399
Barber KE, Mkoji GM, Loker ES (2000) PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. Am J Trop Med Hyg 62:434–440 DOI: 10.4269/ajtmh.2000.62.434
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) GenBank. Nucleic Acids Res 45:D37–D42. 10.1093/nar/gkw1070 DOI: 10.1093/nar/gkw1070
Bouchet P (2005) Classification and nomenclator of gastropod families. ConchBooks
Bui TD, Madsen H, Dang TT (2010) Distribution of freshwater snails in family-based VAC ponds and associated waterbodies with special reference to intermediate hosts of fish-borne zoonotic trematodes in Nam Dinh Province. Vietnam Acta Trop 116:15–23. 10.1016/j.actatropica.2010.04.016 DOI: 10.1016/j.actatropica.2010.04.016
Bui NT, Pham TT, Nguyen NT, Nguyen VH, Murrell D, Phan TV (2016) The importance of wild fish in the epidemiology of Clonorchis sinensis in Vietnam. Parasitol Res 115:3401–3408. 10.1007/s00436-016-5100-8 DOI: 10.1007/s00436-016-5100-8
Bui TD, Pham ND, Saegerman C, Losson B (2016) Current status of fasciolosis in Vietnam: an update and perspectives. J Helminthol 90:511–522. 10.1017/S0022149X15000929 DOI: 10.1017/S0022149X15000929
Chai J-Y, Park J-H, Han E-T, Guk S-M, Shin E-H, Lin A, Kim J-L, Sohn W-M, Yong T-S, Eom KS, Min D-Y, Hwang E-H, Phommmasack B, Insisiengmay B, Rim H-J (2005) Mixed infections with Opisthorchis viverrini and intestinal flukes in residents of Vientiane Municipality and Saravane Province in Laos. J Helminthol 79:283–289. 10.1079/JOH2005302 DOI: 10.1079/JOH2005302
Chai J-Y, Shin E-H, Lee S-H, Rim H-J (2009) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:S69–S102. 10.3347/kjp.2009.47.S.S69 DOI: 10.3347/kjp.2009.47.S.S69
Choi DW (1984) Clonorchis sinensis: life cycle, intermediate hosts, transmission to man and geographical distribution in Korea. Arzneimittelforschung. 34:1145–1151
Choi DW, Chung BJ (1975) Clonorchis sinensis in Kyungpook Province, Korea: 1. Distribution and demonstration of the cercaria of Clonorchis sinensis from snail, Parafossarulus manchouricus Bourgigant. Kisaengchunghak Chapchi 13:133–138. 10.3347/kjp.1975.13.2.133 DOI: 10.3347/kjp.1975.13.2.133
Chontananarth T, Tejangkura T, Wetchasart N, Chimburut C (2017) Morphological characteristics and phylogenetic trends of trematode cercariae in freshwater snails from Nakhon Nayok Province, Thailand. Korean J Parasitol 55:47–54. 10.3347/kjp.2017.55.1.47 DOI: 10.3347/kjp.2017.55.1.47
Christensen NO, Frandsen F (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop 41(2):181–202
Chung BJ, Joo CY, Choi DW (1980) Seasonal variation of snail population of Parafossarulus manchouricus and larval trematode infection in river Kumho, Kyungpook province, Korea. Kisaengchunghak Chapchi 18:54–64
Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial, Plymouth routine in multivariate ecological. Research, Plymouth
Clausen JH, Madsen H, Murrell KD, Phan TV, Nguyen TTH, Do TD, Nguyen TLA, Nguyen MH, Dalsgaard A (2012) Prevention and control of fish-borne zoonotic trematodes in fish nurseries, Vietnam. Emerg. Infect. Dis. 18:1438–1445. 10.3201/eid1809.111076 DOI: 10.3201/eid1809.111076
Dang NT, Ho TH (2017) Fauna of Viet Nam (Mollusca, Gastropoda, Bivalvia). Science and Technology Publishhing House 29:59–182
Derycke S, Sheibani Tezerji R, Rigaux A, Moens T (2012) Investigating the ecology and evolution of cryptic marine nematode species through quantitative real-time PCR of the ribosomal ITS region. Mol Ecol Resour 12:607–619. 10.1111/j.1755-0998.2012.03128.x DOI: 10.1111/j.1755-0998.2012.03128.x
Do TD, Nguyen VD, Waikagul J, Dalsgaard A, Chai J-Y, Sohn W-M, Murrell KD (2007) Fishborne zoonotic intestinal trematodes, Vietnam. Emerg Infect Dis 13:1828–1833. 10.3201/eid1312.070554 DOI: 10.3201/eid1312.070554
Dodangeh S, Daryani A, Sharif M, Gholami S, Kialashaki E, Moosazadeh M, Sarvi S (2019) Freshwater snails as the intermediate host of trematodes in Iran: a systematic review. Epidemiol Health 41. 10.4178/epih.e2019001
Edan M (2006) Review of free-range duck farming systems in northern Vietnam and assessment of their implication in the spreading of the highly pathogenic (H5N1) strain of avian influenza (HPAI). Food and Agriculture Organization
Engels D, Savioli L (2006) Reconsidering the underestimated burden caused by neglected tropical diseases. Trends Parasitol 22:363–366. 10.1016/j.pt.2006.06.004 DOI: 10.1016/j.pt.2006.06.004
Esch GW, Curtis LA, Barger MA (2001) A perspective on the ecology of trematode communities in snails. Parasitology 123(Suppl):S57–S75 DOI: 10.1017/S0031182001007697
Georgieva S, Selbach C, Faltýnková A, Soldánová M, Sures B, Skírnisson K, Kostadinova A (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors 6:64. 10.1186/1756-3305-6-64 DOI: 10.1186/1756-3305-6-64
Graczyk T (1991) Variability of metacercariae of Diplostomum spathaceum (Rudolphi, 1819) (Trematoda, Diplostomidae). Acta Parasitol Pol 36
Imani-Baran A, Yakhchali M, Malekzadeh-Viayeh R, Farahnak A (2013) Seasonal and geographic distribution of cercarial infection in Lymnaea gedrosiana (Pulmunata: Lymnaeidae) in North West Iran. Iran J Parasitol 8:423–429
Islam Z, Zahangir Alam M, Akter S, Chandra Roy B, Mondal MH (2012) Distribution patterns of vector snails and trematode cercaria in their vectors in some selected areas of Mymensingh. J Environ Sci Nat Resour 5:37–46
Joo CY (1980) Epidemiological studies of Clonorchis sinensis in vicinity of river Taewha, Kyungnam province, Korea. Kisaengchunghak Chapchi 18:199–214. 10.3347/kjp.1980.18.2.199 DOI: 10.3347/kjp.1980.18.2.199
Kim VV, Dalsgaard A, Blair D, Le TH (2009) Haplorchis pumilio and H. taichui in Vietnam discriminated using ITS-2 DNA sequence data from adults and larvae. Exp Parasitol 123:146–151. 10.1016/j.exppara.2009.06.011 DOI: 10.1016/j.exppara.2009.06.011
Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176 DOI: 10.1023/A:1022681123340
Lai D-H, Hong X-K, Su B-X, Liang C, Hide G, Zhang X, Yu X, Lun Z-R (2016) Current status of Clonorchis sinensis and clonorchiasis in China. Trans R Soc Trop Med Hyg 110:21–27. 10.1093/trstmh/trv100 DOI: 10.1093/trstmh/trv100
Le VC, Nguyen VD, Kieu TL (1996) Determination of animal reservoirs and intermediate hosts of liver flukes, Summary Record of Scientific Research Works 1991–1996. National Institute of Malariology, Parasitology and Entomology 1996, Hanoi
Le TH, Nguyen VD, Agatsuma T, Blair D, Vercruysse J, Dorny P, Nguyen TGT, McManus DP (2007) Molecular confirmation that Fasciola gigantica can undertake aberrant migrations in human hosts. J Clin Microbiol 45:648–650. 10.1128/JCM.01151-06 DOI: 10.1128/JCM.01151-06
Le TH, De NV, Agatsuma T, Thi Nguyen TG, Nguyen QD, McManus DP, Blair D (2008) Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. Int J Parasitol 38:725–730. 10.1016/j.ijpara.2007.10.003 DOI: 10.1016/j.ijpara.2007.10.003
Littlewood DTJ, Bray RA (2000) Interrelationships of the Platyhelminthes. CRC Press, London
Lun Z-R, Gasser RB, Lai D-H, Li A-X, Zhu X-Q, Yu X-B, Fang Y-Y (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5:31–41 DOI: 10.1016/S1473-3099(04)01252-6
Madsen H, Coulibaly G, Furu P (1987) Distribution of freshwater snails in the river Niger basin in Mali with special reference to the intermediate hosts of schistosomes. Hydrobiologia 146:77–88. 10.1007/BF00007580 DOI: 10.1007/BF00007580
Madsen H, Bui TD, Dang TT, Nguyen KV, Dalsgaard A, Phan TV (2015) The role of rice fields, fish ponds and water canals for transmission of fish-borne zoonotic trematodes in aquaculture ponds in Nam Dinh Province, Vietnam. Parasit Vectors 8:625. 10.1186/s13071-015-1237-z DOI: 10.1186/s13071-015-1237-z
Mao SP (1991) Protozoan and helminth parasites of humans in mainland China. Int J Parasitol 21(3):347–351. 10.1016/0020-7519(91)90037-8 DOI: 10.1016/0020-7519(91)90037-8
Mouritsen KN (2002) The Hydrobia ulvae–Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J Helminthol 76:341–347. 10.1079/JOH2002136 DOI: 10.1079/JOH2002136
Mullowney DR, Dawe EG, Morado JF, Cawthorn RJ (2011) Sources of variability in prevalence and distribution of bitter crab disease in snow crab (Chionoecetes opilio) along the northeast coast of Newfoundland. ICES J Mar Sci 68:463–471. 10.1093/icesjms/fsq189 DOI: 10.1093/icesjms/fsq189
Ngo VT (2016) The current state of fish-borne trematodes, involved factors and effectiveness of intervention in Nga Son district, Thanh Hoa province 2013–2014. Doctoral Dissertation. Hanoi Medical University, Vietnam
Nguyen SH (1993) Biological characteristics and performance traits of Anh Dao and Bau ducks and their F1 crossbreed (Bau x Anh Dao) raised in free-rang method in Thanh Hoa Province (doctoral dissertation). Hanoi National University of Education, Vietnam
Nguyen VD (2004) Fish-borne trematodes in Vietnam. Southeast Asian J. Trop. Med Public Health 35:299–301
Nguyen QA (2019) Situation of fish-borne zoonosis trematodes in people over 15 years old in Thac Ba lake region, Yen Bai province in 2016 and some related factors. MSc dissertation. Hanoi Medical University, Hanoi, Vienam
Nguyen VD, Le TH (2011) Human infections of fish-borne trematodes in Vietnam: prevalence and molecular specific identification at an endemic commune in Nam Dinh province. Exp Parasitol 129:355–361. 10.1016/j.exppara.2011.09.005 DOI: 10.1016/j.exppara.2011.09.005
Nguyen VD, Kieu TL, Le VC et al (1996) Liver fluke infection and changes of its infection rates after specific treatment, Summary Record of Scientific Research Works 1991–1996. National Institute of Malariology, Parasitology and Entomology, Hanoi
Nguyen VD, Murrell KD, Le DC, Phung DC, Le VC, Nguyen DT, Dalsgaard A (2003) The food-borne trematode zoonoses of Vietnam. Southeast Asian J Trop Med Public Health 34(Suppl 1):12–34
Nguyen TGT, Nguyen VD, Vercruysse J, Dorny P, Le TH (2009) Genotypic characterization and species identification of Fasciola spp. with implications regarding the isolates infecting goats in Vietnam. Exp Parasitol 123:354–361. 10.1016/j.exppara.2009.09.001 DOI: 10.1016/j.exppara.2009.09.001
Nguyen TP, Le THV, Duong TH, Nguyen TTT, Do TD, Nguyen TH (2018) Prevalence and risk factors for small liver fluke infection (Clonorchiasis) among residents living in Phan Thanh commune, Luc Yen District, Yen Bai province, 2014-2015. J Malar Parasite Dis Control 3:24–29
Nyindo M, Lukambagire A-H (2015) Fascioliasis: an ongoing zoonotic trematode infection. Biomed Res Int 2015:1–8. 10.1155/2015/786195 DOI: 10.1155/2015/786195
Olivier L, Schneiderman M (1956) A method for estimating the density of aquatic snail populations. Exp Parasitol 5:109–117 DOI: 10.1016/0014-4894(56)90008-X
Parsons VL (2017) Stratified sampling, in: Wiley StatsRef: Statistics Reference Online. American Cancer Society, pp. 1–11. 10.1002/9781118445112.stat05999.pub2
Petney TN, Andrews RH, Saijuntha W, Wenz-Mücke A, Sithithaworn P (2013) The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini. Int. J. Parasitol Zoonoses Special Issue 43:1031–1046. 10.1016/j.ijpara.2013.07.007 DOI: 10.1016/j.ijpara.2013.07.007
Pham ND, Nawa Y (2016) Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Trans R Soc Trop Med Hyg 110:13–20. 10.1093/trstmh/trv103 DOI: 10.1093/trstmh/trv103
Pham ND, Shinohara A, Horii Y, Habe S, Nawa Y, Dang TT, Nguyen TL (2007) Morphological and molecular identification of two Paragonimus spp., of which metacercariae concurrently found in a land crab, Potamiscus tannanti, collected in Yenbai Province, Vietnam. Parasitol Res 100:1075–1082. 10.1007/s00436-006-0411-9 DOI: 10.1007/s00436-006-0411-9
Phan VT, Ersbøll AK, Do DT, Dalsgaard A (2011) Raw-fish-eating behavior and fishborne zoonotic trematode infection in people of northern Vietnam. Foodborne Pathog Dis 8:255–260. 10.1089/fpd.2010.0670 DOI: 10.1089/fpd.2010.0670
Phi TTN (2018) Foodborne zoonotic trematode infections in Yen Bai, Vietnam Integrated Approach (Master of Health Sciences). University of Twente
Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151. 10.1017/S0031182005008693 DOI: 10.1017/S0031182005008693
Prasad PK, Goswami L, Mohan, Tandon V, Chatterjee A (2011) PCR-based molecular characterization and in silico analysis of food-borne trematode parasites Paragonimus westermani, Fasciolopsis buski and Fasciola gigantica from Northeast India using ITS2 rDNA. Bioinformation 6:64–68 DOI: 10.6026/97320630006064
Saijuntha W, Tantrawatpan C, Sithithaworn P, Andrews HR, Petney NT (2011) Genetic characterization of Echinostoma revolutum and Echinoparyphium recurvatum (Trematoda: Echinostomatidae) in Thailand and phylogenetic relationships with other isolates inferred by ITS1 sequence. Parasitol Res 108(3):751–755. 10.1007/s00436-010-2180-8 DOI: 10.1007/s00436-010-2180-8
Sayasone S, Tesana S, Utzinger J, Hatz C, Akkhavong K, Odermatt P (2009) Rare human infection with the trematode Echinochasmus japonicus in Lao PDR. Parasitol Int 58(1):106–109. 10.1016/j.parint.2008.11.001 DOI: 10.1016/j.parint.2008.11.001
Schell SC (1970) How to know the trematodes. W. C. Brown Co.
Seo BS, Lee SH, Chai JY, Hong SJ (1985) Studies on intestinal trematodes in Korea XX. Four cases of natural human infection by Echinochasmus japonicus. Kisaengchunghak Chapchi 23(2):214–220. 10.3347/kjp.1985.23.2.214 DOI: 10.3347/kjp.1985.23.2.214
Soldánová M, Kuris AM, Scholz T, Lafferty KD (2012) The role of spatial and temporal heterogeneity and competition in structuring trematode communities in the great pond snail, Lymnaea stagnalis (L.). J Parasitol 98:460–471. 10.1645/GE-2964.1 DOI: 10.1645/GE-2964.1
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 DOI: 10.1093/molbev/mst197
Thaenkham U, Dekumyoy P, Komalamisra C, Sato M, Dung DT, Waikagul J (2010) Systematics of the subfamily Haplorchiinae (Trematoda: Heterphyidae), based on nuclear ribosomal DNA genes and ITS2 region. Parasitol Int 59:460–465. 10.1016/j.parint.2010.06.009 DOI: 10.1016/j.parint.2010.06.009
Wang Y-C, Ho RCY, Feng C-C, Namsanor J, Sithithaworn P (2015) An ecological study of Bithynia snails, the first intermediate host of Opisthorchis viverrini in Northeast Thailand. Acta Trop 141:244–252. 10.1016/j.actatropica.2014.02.009 DOI: 10.1016/j.actatropica.2014.02.009
Williams BD, Schrank B, Huynh C, Shownkeen R, Waterston RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics 131:609–624 DOI: 10.1093/genetics/131.3.609
Yoshida Y (2012) Clonorchiasis--a historical review of contributions of Japanese parasitologists. Parasitol Int 61:5–9. 10.1016/j.parint.2011.06.003 DOI: 10.1016/j.parint.2011.06.003