Skip to main content

Advertisement

SpringerLink
Log in

The rapid detection method by polymerase chain reaction for minute intestinal trematodes: Haplorchis taichui in intermediate snail hosts based on 18s ribosomal DNA

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

The minute intestinal trematode, Haplorchis taichui, is an important parasite species that can infect humans and other mammals. This study investigated the outbreak of H. taichui in thiarid snails in the lower part of the Chao Phraya Basin, Thailand by employing morphological and molecular-based methods. In development of a specific primer of H. taichui, the PCR reaction was conducted with no cross-reaction to their hosts and other related trematode species. The highest level of sensitivity that could be amplified was 0.50 ng/μl and this was detected with only one egg in the sample. In terms of the epidemic results, the parapleurolophocercous cercaria infected only two species of thiarid snails (Melanoides tuberculata and Tarebia granifera) with an overall prevalence of 3.80% (23/605). The process of molecular identification revealed positive results indicating that eleven from twenty-three of parapleurolophocercous cercariae specimens in the lower part of the Chao Phraya Basin were H. taichui. In conclusion, this study has developed a rapid detection method, which can discriminate H. taichui from other parapleurolophocercous cercaria in intermediate snail hosts with a high level of sensitivity. Moreover, the high proportion of H. taichui in parapleurolophocercous cercaria (47.83%) indicated that H. taichui was the dominant species of this cercarial type and could infect cyprinoid fish in the lower part of the Chao Phraya Basin leading to public health problems in this area. Thus, a specific primer could be useful in the detection and surveillance of H. taichui outbreaks in their hosts. Recognition of this has resulted in the creation of important prevention programs in these infected areas in the further study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • Boerlage AS, Graat EA, Verreth JA, De Jong MC (2013a) Distribution of trematodes in snails in ponds at integrated small-scale aquaculture farms. Acta Trop 3:276–281

    Article  Google Scholar 

  • Boerlage AS, Graat EA, Verreth JA, De Jong MC (2013b) Survival of heterophyid metacercaria in common carp (Cyprinus carpio). Parasitol Res 7:2759–2762

    Article  Google Scholar 

  • Boerlage AS, Graat EA, Verreth JA, De Jong MC (2014) Transmission of fish-borne zoonotic trematodes (Heterophyidae) to common carp (Cyprinus carpio) is independent of density of fish and trematodes. J Helminthol 2:183–188

    Article  Google Scholar 

  • Boonchot K, Wongsawad C (2005) A survey of helminths in cyprinoid fish from the Mae Ngad Somboonchon Reservoir, Chiang Mai province, Thailand. Southeast Asian J Trop Med Public Health 1:103–107

    Google Scholar 

  • Brandt RA (1974) The non-marine aquatic Mollusca of Thailand. Archiv fur Molluskenkunde 105:1–423

    Google Scholar 

  • Chai JY, Yong TS, Eom KS, Min DY, Jeon HK, Kim TY, Jung BK, Sisabath L, Insisiengmay B, Phommasack B (2013) Hyperendemicity of Haplorchis taichui infection among riparian people in Saravane and Champasak province, Lao PDR. Korean J Parasitol 3:305–311

    Article  Google Scholar 

  • Chontananarth T, Wongsawad C (2010) Prevalence of Haplorchis taichui in field-collected snails: a molecular approach. Korean J Parasitol 4:343–346

    Article  CAS  Google Scholar 

  • Chontananarth T, Wongsawad C (2013) Epidemiology of cercarial stage of trematodes in freshwater snails from Chiang Mai province, Thailand. Asian Pac J Trop Biomed 3:237–243

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1:47–54. https://doi.org/10.3347/kjp.2017.55.1.47

    Article  Google Scholar 

  • Dechruksa W, Krailas D, Ukong S, Inkapatanakul W, Koonchornboon T (2007) Trematode infections of the freshwater snail family Thiaridae in the Khek River, Thailand. Southeast Asian J Trop Med Public Health 38:1016–1028

    PubMed  Google Scholar 

  • Dzikowski R, Levy M, Poore M, Flowers J, Paperna I (2004) Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis Aquat Org 1:35–41

    Article  Google Scholar 

  • Freedman D, Pisani R, Purves R (2007) Statistics (international student edition). Pisani, R. Purves, 4th edn. WW Norton & Company, New York

    Google Scholar 

  • Gibson DI, Jones A, Bray RA (2005) Keys to the trematoda, vol 2. CABI Publishing, United Kindom

    Google Scholar 

  • Hung NM, Anh NTL, Van PT, Thanh BN, Van Ha N, Van Hien H (2015) Current status of fish-borne zoonotic trematode infections in Gia Vien district, Ninh Binh province, Vietnam. Parasit Vectors 1:21. https://doi.org/10.1186/s13071-015-0643-6

    Article  Google Scholar 

  • Krailas D, Namchote S, Rattanathai P (2011) Human intestinal flukes Haplorchris taichui and Haplorchris pumilio in their intermediate hosts, freshwater snails of the families Thiaridae and Pachychilidae, in Southern Thailand. Zoosyst Evol 2:349–360

    Article  Google Scholar 

  • Krailas D, Chotesaengsri S, Dechruksa W, Namchote S, Chuanprasit C, Veeraveebsakij N, Boonmekam D, Koonchornboon T (2012) Species diversity of aquatic mollusks and their cercarial infections; Khao Yai National Park, Thailand. J Trop Med Parasitol 35:37–47

    Google Scholar 

  • Krailas D, Namchote S, Koonchornboon T, Dechruksa W, Boonmekam D (2014) Trematodes obtained from the thiarid freshwater snail Melanoides tuberculata (Müller, 1774) as vector of human infections in Thailand. Zoosyst Evol 90:57–86

    Article  Google Scholar 

  • Krailas D, Veeravechsukij N, Chuanprasit C, Boonmekam D, Namchote S (2016) Prevalence of fish-borne trematodes of the family Heterophyidae at Pasak Cholasid Reservoir, Thailand. Acta Trop 156:79–86

    Article  PubMed  CAS  Google Scholar 

  • Kumchoo K, Wongsawad C, Chai J-Y, Vanittanakom P, Rojanapaibul A (2005) High prevalence of Haplorchis taichui metacercariae in cyprinoid fish from Chiang Mai province, Thailand. Southeast Asian J Trop Med Public Health 2:451–455

    Google Scholar 

  • Le TH, Nguyen KT, Nguyen NTB, Doan HTT, Blair D (2017) The ribosomal transcription units of Haplorchis pumilio and H. taichui and the use of 28S rDNA sequences for phylogenetic identification of common heterophyids in Vietnam. Parasit Vectors 1:17

    Article  CAS  Google Scholar 

  • Mohammadi R, Hosseini-Safa A, Ardakani MJE, Rostami-Nejad M (2015) The relationship between intestinal parasites and some immune-mediated intestinal conditions. Gastroenterol Hepatol Bed Bench 2:123–131

    Google Scholar 

  • Ondračková M, Hudcová I, Dávidová M, Adámek Z, Kašný M, Jurajda P (2015) Non-native gobies facilitate the transmission of Bucephalus polymorphus (Trematoda). Parasit Vectors 1:382. https://doi.org/10.1186/s13071-015-0999-7

    Article  Google Scholar 

  • Onsurathum S, Pinlaor P, Charoensuk L, Haonon O, Chaidee A, Intuyod K, Laummaunwai P, Boonmars T, Kaewkes W, Pinlaor S (2016) Contamination of Opisthorchis viverrini and Haplorchis taichui metacercariae in fermented fish products in northeastern Thailand markets. Food Control 59:493–498

    Article  CAS  Google Scholar 

  • Pinlaor S, Onsurathum S, Boonmars T, Pinlaor P, Hongsrichan N, Chaidee A, Haonon O, Limviroj W, Tesana S, Kaewkes S (2013) Distribution and abundance of Opisthorchis viverrini metacercariae in cyprinid fish in Northeastern Thailand. Korean J Parasitol 6:703–710

    Article  Google Scholar 

  • Pinto HA, Mati VL, de Melo AL (2015) Experimental centrocestiasis: worm burden, morphology and fecundity of Centrocestus formosanus (Trematoda: Heterophyidae) in dexamethasone immunosuppressed mice. Parasitol Int 5:236–239. https://doi.org/10.1016/j.parint.2015.02.002

    Article  Google Scholar 

  • Rim HJ, Sohn WM, Yong TS, Eom KS, Chai JY, Min DY, Lee SH, Hoang EH, Phommasack B, Insisiengmay S (2013) Fishborne trematode metacercariae in Luang Prabang, Khammouane, and Saravane Province, Lao PDR. Korean J Parasitol 1:107–114

    Article  Google Scholar 

  • Saenphet S, Wongsawad C, Saenphet K, Rojanapaibul A, Vanittanakom P, Chai J-Y (2008) Haplorchis taichui: worm recovery rate and immune responses in infected rats (Rattus norvegicus). Exp Parasitol 2:175–179

    Article  CAS  Google Scholar 

  • Sohn W-M, Yong T-S, Eom KS, Min D-Y, Lee D, Jung B-K, Banouvong V, Insisiengmay B, Phommasack B, Rim H-J (2014) Prevalence of Haplorchis taichui among humans and fish in Luang Prabang Province, Lao PDR. Acta Tropica 74–80

  • Tantachamrun T, Kliks M (1978) Heterophyid infection in human ileum: report of three cases. Southeast Asian J Trop Med Public Health 2:228–231

    Google Scholar 

  • Tum S, Puotinen M, Copeman D (2004) A geographic information systems model for mapping risk of fasciolosis in cattle and buffaloes in Cambodia. Vet Parasitol 2:141–149

    Article  Google Scholar 

  • Ukong S, Krailas D, Dangprasert T, Channgarm P (2007) Studies on the morphology of cercariae obtained from freshwater snails at Erawan Waterfall, Erawan National Park, Thailand. Southeast Asian J Trop Med Public Health 2:302–312

    Google Scholar 

  • Van Van K, 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 2:146–151

    Article  CAS  Google Scholar 

  • Watthanakulpanich D, Waikagul J, Maipanich W, Nuamtanong S, Sanguankiat S, Pubampen S, Praevanit R, Mongkhonmu S, Nawa Y (2010) Haplorchis taichui as a possible etiologic agent of irritable bowel syndrome-like symptoms. Korean J Parasitol 3:225–229

    Article  Google Scholar 

  • Wongsawad C, Wongsawad P, Chai J-Y, Paratasilpin T, Anuntalabhochai S (2006) Dna quantities and qualities from various stages of some trematodes using optical and HAT-RAPD methods. Southeast Asian J Trop Med Public Health 37:62–68

    PubMed  CAS  Google Scholar 

  • Wongsawad C, Phalee A, Noikong W, Chuboon S, Nithikathkul C (2012) Co-infection with Opisthorchis viverrini and Haplorchis taichui detected by human fecal examination in Chomtong district, Chiang Mai province, Thailand. Parasitol Int 1:56–59

    Article  Google Scholar 

Download references

Acknowledgements

We greatly acknowledge the Faculty of Science, Srinakharinwirot University for providing funding. Special thanks are extended to all members in The Applied Parasitology Research, Department of Biology, Faculty of Science, Srinakharinwirot University for many facilities. Finally, I would like to thank Simon McIver for his assistance in editing and grammatical proofreading this manuscript.

Author information

Authors and Affiliations

  1. Applied Parasitology Research Laboratory, Department of Biology, Faculty of Science, Srinakharinwirot University, Bangkok, 10110, Thailand

    Thapana Chontananarth, Sothorn Anucherngchai & Thanawan Tejangkura

  2. Center of Excellence in Animal, Plant and Parasitic Biotechnology, Srinakharinwirot University, Bangkok, 10110, Thailand

    Thapana Chontananarth & Thanawan Tejangkura

Authors
  1. Thapana Chontananarth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sothorn Anucherngchai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thanawan Tejangkura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CT: Conception and design of study, CT: Acquisition of data, AS and TT: Analysis and/or interpretation of data, AS and TT: Drafting the manuscript, CT: Revising the manuscript critically for important intellectual content. AS, TT, CT: Approval of the version of the manuscript to be published (the names of all authors must be listed).

Corresponding author

Correspondence to Thapana Chontananarth.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chontananarth, T., Anucherngchai, S. & Tejangkura, T. The rapid detection method by polymerase chain reaction for minute intestinal trematodes: Haplorchis taichui in intermediate snail hosts based on 18s ribosomal DNA. J Parasit Dis 42, 423–432 (2018). https://doi.org/10.1007/s12639-018-1020-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-018-1020-0

Keywords

Search

Navigation