Species-specific detection of Schistosoma japonicum using the ‘SNAILS’ DNA-based biosensor

  • McManus, D. P. et al. Schistosomiasis. Nat. Rev. Dis. Primers 4, 1–19 (2018).

  • World Health Organization. & UNICEF. Progress on Sanitation and Drinking-Water: 2014 Update.

  • Hotez, P. J. et al. The Global Burden of Disease Study 2010: Interpretation and Implications for the Neglected Tropical Diseases. PLoS Negl. Trop. Dis. 8, e2865 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ferrari, A. J. et al. Global incidence, prevalence, years lived with disability (YLDs), disability-adjusted life-years (DALYs), and healthy life expectancy (HALE) for 371 diseases and injuries in 204 countries and territories and 811 subnational locations, 1990–2021: a systematic analysis for the Global Burden of Disease Study 2021. The Lancet. 403, 2133–2161 (2024).

  • Wang, H. et al. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 388, 1459–1544 (2016).

  • Boissier, J. et al. Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infect. Dis. 16, 971–979 (2016).

    PubMed 

    Google Scholar 

  • He, Y.-X., Salafsky, B. & Ramaswamy, K. Host–parasite relationships of Schistosoma japonicum in mammalian hosts. Trends Parasitol. 17, 320–324 (2001).

    PubMed 

    Google Scholar 

  • Wang, T. P. et al. Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. Int J. Parasitol. 36, 1317–1325 (2006).

    PubMed 

    Google Scholar 

  • Ross, A. G. P. et al. Schistosomiasis in the People’s Republic of China: Prospects and Challenges for the 21st Century. Clin. Microbiol Rev. 14, 270–295 (2001).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Collins, C., Xu, J. & Tang, S. Schistosomiasis control and the health system in P.R. China. Infect. Dis. Poverty 1, 8 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Rollinson, D. et al. Time to set the agenda for schistosomiasis elimination. Acta Trop. 128, 423–440 (2013).

    PubMed 

    Google Scholar 

  • Grimes, J. E. et al. The roles of water, sanitation and hygiene in reducing schistosomiasis: a review. Parasit. Vectors 8, 156 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Webb, A. J. et al. Specific Nucleic AcId Ligation for the detection of Schistosomes: SNAILS. PLoS Negl. Trop. Dis. 16, e0010632 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ying, Z.-M. et al. Spinach-based fluorescent light-up biosensors for multiplexed and label-free detection of microRNAs. Chem. Commun. 54, 3010–3013 (2018).

    Google Scholar 

  • Woo, C. H., Jang, S., Shin, G., Jung, G. Y. & Lee, J. W. Sensitive fluorescence detection of SARS-CoV-2 RNA in clinical samples via one-pot isothermal ligation and transcription. Nat. Biomed. Eng. 4, 1168–1179 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Emery, A. M., Allan, F. E., Rabone, M. E. & Rollinson, D. Schistosomiasis collection at NHM (SCAN). Parasit. Vectors 5, 185 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Xu, J. et al. Evolution of the National Schistosomiasis Control Programmes in The People’s Republic of China. in 1–38 (2016). https://doi.org/10.1016/bs.apar.2016.02.001.

  • Katz, N., Chaves, A. & Pellegrino, J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev. Inst. Med Trop. Sao Paulo 14, 397–400 (1972).

    PubMed 

    Google Scholar 

  • Lin, D.-D. et al. Routine Kato–Katz technique underestimates the prevalence of Schistosoma japonicum: A case study in an endemic area of the People’s Republic of China. Parasitol. Int 57, 281–286 (2008).

    PubMed 

    Google Scholar 

  • Cai, P. et al. Comparison of Kato Katz, antibody-based ELISA and droplet digital PCR diagnosis of schistosomiasis japonica: Lessons learnt from a setting of low infection intensity. PLoS Negl. Trop. Dis. 13, e0007228 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Dang-Trinh, M. A. et al. Analyses of the expression, immunohistochemical properties and serodiagnostic potential of Schistosoma japonicum peroxiredoxin-4. Parasit. Vectors 13, 436 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Angeles, J. et al. Utilization of ELISA Using Thioredoxin Peroxidase-1 and Tandem Repeat Proteins for Diagnosis of Schistosoma japonicum Infection among Water Buffaloes. PLoS Negl. Trop. Dis. 6, e1800 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Angeles, J. et al. Human Antibody Response to Thioredoxin Peroxidase-1 and Tandem Repeat Proteins as Immunodiagnostic Antigen Candidates for Schistosoma japonicum Infection. Am. Soc. Tropical Med. Hyg. 85, 674–679 (2011).

    Google Scholar 

  • Angeles, J. et al. Serological evaluation of the schistosome’s secretory enzyme phytochelatin synthase and phosphoglycerate mutase for the detection of human Schistosoma japonicum infection. Parasitol. Res. 121, 2445–2448 (2022).

    PubMed 

    Google Scholar 

  • Champion, T. S., Connelly, S., Smith, C. J. & Lamberton, P. H. L. Monitoring schistosomiasis and sanitation interventions—The potential of environmental DNA < /scp > . WIREs Water 8, (2021).

  • Carlton, E. J., Bates, M. N., Zhong, B., Seto, E. Y. W. & Spear, R. C. Evaluation of Mammalian and Intermediate Host Surveillance Methods for Detecting Schistosomiasis Reemergence in Southwest China. PLoS Negl. Trop. Dis. 5, e987 (2011).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sturrock, R. F., Karamsadkar, S. J. & Ouma, J. Schistosome infection rates in field snails: Schistosoma mansoni in Biomphalaria pfeifferi from Kenya. Ann. Trop. Med Parasitol. 73, 369–375 (1979).

    PubMed 

    Google Scholar 

  • Frandsen, F. & Christensen, N. O. 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, 181–202 (1984).

    PubMed 

    Google Scholar 

  • Allan, F. et al. Use of sentinel snails for the detection of Schistosoma haematobium transmission on Zanzibar and observations on transmission patterns. Acta Trop. 128, 234–240 (2013).

    PubMed 

    Google Scholar 

  • Pennance, T. et al. Development of a Molecular Snail Xenomonitoring Assay to Detect Schistosoma haematobium and Schistosoma bovis Infections in their Bulinus Snail Hosts. Molecules 25, 4011 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Allan, F. et al. Snail-Related Contributions from the Schistosomiasis Consortium for Operational Research and Evaluation Program Including Xenomonitoring, Focal Mollusciciding, Biological Control, and Modeling. Am. J. Trop. Med Hyg. 103, 66–79 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Abbasi, I., King, C. H., Muchiri, E. M. & Hamburger, J. Detection of Schistosoma mansoni and Schistosoma haematobium DNA by Loop-Mediated Isothermal Amplification: Identification of Infected Snails from Early Prepatency. Am. J. Trop. Med Hyg. 83, 427–432 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hamburger, J. et al. Evaluation of Loop-Mediated Isothermal Amplification Suitable for Molecular Monitoring of Schistosome-Infected Snails in Field Laboratories. Am. J. Trop. Med Hyg. 88, 344–351 (2013).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, Y. et al. Circulating cell-free DNA as a biomarker for diagnosis of Schistosomiasis japonica. Parasit. Vectors 17, 114 (2024).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sengupta, M. E. et al. Environmental DNA for improved detection and environmental surveillance of schistosomiasis. Proc. Natl Acad. Sci. 116, 8931–8940 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Alzaylaee, H. et al. Schistosoma species detection by environmental DNA assays in African freshwaters. PLoS Negl. Trop. Dis. 14, e0008129 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Lodh, N., Naples, J. M., Bosompem, K. M., Quartey, J. & Shiff, C. J. Detection of Parasite-Specific DNA in Urine Sediment Obtained by Filtration Differentiates between Single and Mixed Infections of Schistosoma mansoni and S. haematobium from Endemic Areas in Ghana. PLoS One 9, e91144 (2014).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hung, Y. W. & Remais, J. Quantitative Detection of Schistosoma japonicum Cercariae in Water by Real-Time PCR. PLoS Negl. Trop. Dis. 2, e337 (2008).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gordon, C. atherine A. et al. Real-time PCR Demonstrates High Prevalence of Schistosoma japonicum in the Philippines: Implications for Surveillance and Control. PLoS Negl. Trop. Dis. 9, e0003483 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kane, R. A. et al. Detection and quantification of schistosome DNA in freshwater snails using either fluorescent probes in real-time PCR or oligochromatographic dipstick assays targeting the ribosomal intergenic spacer. Acta Trop. 128, 241–249 (2013).

    PubMed 

    Google Scholar 

  • Cnops, L., Tannich, E., Polman, K., Clerinx, J. & Van Esbroeck, M. Schistosoma real-time PCR as diagnostic tool for international travellers and migrants. Tropical Med. Int. Health 17, 1208–1216 (2012).

    Google Scholar 

  • ten Hove, R. J. et al. Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans. R. Soc. Trop. Med Hyg. 102, 179–185 (2008).

    PubMed 

    Google Scholar 

  • Sun, K. et al. Recombinase polymerase amplification combined with a lateral flow dipstick for rapid and visual detection of Schistosoma japonicum. Parasit. Vectors 9, 476 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Deng, W. et al. Laboratory Evaluation of a Basic Recombinase Polymerase Amplification (RPA) Assay for Early Detection of Schistosoma japonicum. Pathogens 11, 319 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Qin, Z.-Q. et al. Field Evaluation of a Loop-Mediated Isothermal Amplification (LAMP) Platform for the Detection of Schistosoma japonicum Infection in Oncomelania hupensis Snails. Trop. Med Infect. Dis. 3, 124 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Xu, J. et al. Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). Int J. Parasitol. 40, 327–331 (2010).

    PubMed 

    Google Scholar 

  • Young, N. D. et al. Exploring molecular variation in Schistosoma japonicum in China. Sci. Rep. 5, 17345 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Souza, A. A. et al. Diagnostics and the neglected tropical diseases roadmap: setting the agenda for 2030. Trans. R. Soc. Trop. Med Hyg. 115, 129–135 (2021).

    PubMed 

    Google Scholar 

  • Valentim, C. L. L. et al. Genetic and Molecular Basis of Drug Resistance and Species-Specific Drug Action in Schistosome Parasites. Science (1979) 342, 1385–1389 (2013).

    Google Scholar 

  • Chevalier, F. D. et al. Oxamniquine resistance alleles are widespread in Old World Schistosoma mansoni and predate drug deployment. PLoS Pathog. 15, e1007881 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Marchant, J. S. Progress interrogating TRPMPZQ as the target of praziquantel. PLoS Negl. Trop. Dis. 18, e0011929 (2024).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Geneva: World Health Organization. Diagnostic Target Product Profiles for Monitoring, Evaluation and Surveillance of Schistosomiasis Control Programmes. (2021).

  • Attwood, S. W., Fatih, F. A. & Upatham, E. S. DNA-Sequence Variation Among Schistosoma mekongi Populations and Related Taxa; Phylogeography and the Current Distribution of Asian Schistosomiasis. PLoS Negl. Trop. Dis. 2, e200 (2008).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kane, R. A. et al. A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species. Parasitology 127, 131–137 (2003).

    PubMed 

    Google Scholar 

  • Lockyer, A. E. et al. The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224 (2003).

    PubMed 

    Google Scholar 

  • Webster, B. L. et al. DNA barcoding of Schistosoma haematobium on Zanzibar reveals substantial genetic diversity and two major phylogenetic groups. Acta Trop. 128, 206–217 (2013).

    PubMed 

    Google Scholar 

  • Djuikwo-Teukeng, F. F. et al. Population genetic structure of Schistosoma bovis in Cameroon. Parasit. Vectors 12, 56 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hanelt, B. et al. Schistosoma kisumuensis n. sp. (Digenea: Schistosomatidae) from murid rodents in the Lake Victoria Basin, Kenya and its phylogenetic position within the S. haematobium species group. Parasitology 136, 987–1001 (2009).

    PubMed 

    Google Scholar 

  • Moore, L. et al. The mutational landscape of normal human endometrial epithelium. Nature 580, 640–646 (2020).

    PubMed 

    Google Scholar 

  • Doyle, S. R. et al. Evaluation of DNA Extraction Methods on Individual Helminth Egg and Larval Stages for Whole-Genome Sequencing. Front Genet 10, 826 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

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