Author:
- INTRODUCTION
- MATERIALS AND METHODS
- Ethical approval.
- Parasites.
- Identification of Fasciola worms by morphology and molecular techniques.
- Human sera.
- Assessment of the Fasciola IgG ELISA kit produced in the United States and selection of positive control sera.
- Crude worm extract.
- Cystatin capture ELISA with CWE.
- Dot-blot ELISA using recombinant F. gigantica proteins.
- Synthetic peptides design based on FgCB5 sequence.
- Indirect ELISA with synthetic peptide antigen based on FgCB5.
- Statistical analysis.
- RESULTS AND DISCUSSION
- Identification of Fasciola species.
- Assessment of the Fasciola IgG ELISA kit from the United States and selection of positive control sera for subsequent experiments.
- Diagnostic efficacy of CC ELISA using crude worm extract.
- Selection of recombinant proteins using dot-blot analysis.
- Peptide selection and efficacy of synthetic peptide-based ELISA in comparison with other ELISA systems.
- Supplementary Files
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization (WHO) Ntd, 2018. Human Fascioliasis: Review Provides Fresh Perspectives on Infection and Control. Available at: http://www.who.int/neglected_diseases/news/fascioliasis-review-provides-new-perspectives-infection-control/en/. Accessed September 10, 2018.
-
2.
Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41–146.
-
3.
Bui TD, Doanh PN, Saegerman C, Losson B, 2016. Current status of fasciolosis in Vietnam: an update and perspectives. J Helminthol 90: 511–522.
-
4.
Mas-Coma S, Bargues MD, Valero MA, 2018. Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures. Parasitology 145: 1665–1699.
-
5.
World Health Organization (WHO), 2018. Foodborne Trematode Infections. Fascioliasis. Fascioliasis Diagnosis, Treatment and Control Strategy. Available at: http://www.who.int/foodborne_trematode_infections/fascioliasis/fascioliasis_diagnosis/en/. Accessed November 19, 2018.
-
6.
Smooker PM, Jayaraj R, Pike RN, Spithill TW, 2010. Cathepsin B proteases of flukes: the key to facilitating parasite control? Trends Parasitol 26: 506–514.
-
7.
Robinson MW, Menon R, Donnelly SM, Dalton JP, Ranganathan S, 2009. An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Mol Cell Proteomics 8: 1891–1907.
-
8.
Rojas-Caraballo J, López-Abán J, Del Villar LP, Vizcaíno C, Vicente B, Fernández-Soto P, Del Olmo E, Patarroyo MA, Muro A, 2014. In vitro and in vivo studies for assessing the immune response and protection-inducing ability conferred by Fasciola hepatica-derived synthetic peptides containing B-and T-cell epitopes. PLoS One 9: e105323.
-
9.
Rokni MB, Massoud J, Hanilo A, 2003. Comparison of adult somatic and cysteine proteinase antigens of Fasciola gigantica in enzyme linked immunosorbent assay for serodiagnosis of human fasciolosis. Acta Trop 88: 69–75.
-
10.
Ikeda T, 1998. Cystatin capture enzyme-linked immunosorbent assay for immunodiagnosis of human paragonimiasis and fascioliasis. Am J Trop Med Hyg 59: 286–290.
-
11.
Meshgi B, Jalousian F, Fathi S, Jahani Z, 2018. Design and synthesis of a new peptide derived from Fasciola gigantica cathepsin L1 with potential application in serodiagnosis of fascioliasis. Exp Parasitol 189: 76–86.
-
12.
Santana BG, Dalton JP, Camargo FV, Parkinson M, Ndao M, 2013. The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease. PLoS Negl Trop Dis 7: e2414.
-
13.
Tantrawatpan C, Maleewong W, Wongkham C, Wongkham S, Intapan PM, Nakashima K, 2005. Serodiagnosis of human fascioliasis by a cystatin capture enzyme-linked immunosorbent assay with recombinant Fasciola gigantica cathepsin L antigen. Am J Trop Med Hyg 72: 82–86.
-
14.
Intapan PM, Tantrawatpan C, Maleewong W, Wongkham S, Wongkham C, Nakashima K, 2005. Potent epitopes derived from Fasciola gigantica cathepsin L1 in peptide-based immunoassay for the serodiagnosis of human fascioliasis. Diagn Microbiol Infect Dis 53: 125–129.
-
15.
O'Neill SM, Parkinson M, Dowd AJ, Strauss W, Angles R, Dalton JP, 1999. Immunodiagnosis of human fascioliasis using recombinant Fasciola hepatica cathepsin L1 cysteine proteinase. Am J Trop Med Hyg 60: 749–751.
-
16.
Creaney J, Wilson L, Dosen M, Sandeman RM, Spithill TW, Parsons JC, 1996. Fasciola hepatica: irradiation-induced alterations in carbohydrate and cathepsin-B protease expression in newly excysted juvenile liver fluke. Exp Parasitol 83: 202–215.
-
17.
Law RH, Smooker PM, Irving JA, Piedrafita D, Ponting R, Kennedy NJ, Whisstock JC, Pike RN, Spithill TW, 2003. Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infect Immun 71: 6921–6932.
-
18.
Meemon K, Grams R, Vichasri-Grams S, Hofmann A, Korge G, Viyanant V, Upatham ES, Habe S, Sobhon P, 2004. Molecular cloning and analysis of stage and tissue-specific expression of cathepsin B encoding genes from Fasciola gigantica. Mol Biochem Parasitol 136: 1–10.
-
19.
Siricoon S, Vichasri Grams S, Lertwongvisarn K, Abdullohfakeeyah M, Smooker PM, Grams R, 2015. Fasciola gigantica cathepsin B5 is an acidic endo- and exopeptidase of the immature and mature parasite. Biochimie 119: 6–15.
-
20.
Quy TM, Yeatman H, Flood V, Chuong NC, Tuan BV, 2015. Prevalence and risks of fascioliasis among adult cohorts in Binh Dinh and Quang Ngai provinces-central Viet Nam. Vietnam J Public Health 3: 46–61.
-
21.
Huong NT, Duong TD, Tinh TT, 2013. Human Fasciola sp infection in community Nghe an province and comparison of an antibody ELISA detection for serodiagnosis of fascioliasis (in Vietnamese, English abstract). J Vietnam Pract Med 11: 156–160.
-
22.
Duong TD, Huong NT, Tinh TT, 2013. Research applicated the technical standards in diagnostic human fascioliasis in hospital of the national institute of malariology, parasitology and entomology (2011–2013) (in Vietnamese, English abstract). J Vietnam Pract Med 11: 67–71.
-
23.
Van De N, Thi Xuan L, Van Chau L, 2003. Prevalence of first survey of human fasciloliasis in Khanh Hoa province, Vietnam (in Vietnamese). J Vietnam Pract Med 3: 77–80.
-
24.
Periago MV, Valero MA, El Sayed M, Ashrafi K, El Wakeel A, Mohamed MY, Desquesnes M, Curtale F, Mas-Coma S, 2008. First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infect Genet Evol 8: 51–58.
-
25.
Itagaki T, Kikawa M, Sakaguchi K, Shimo J, Terasaki K, Shibahara T, Fukuda K, 2005. Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131: 679–685.
-
26.
McVeigh P et al. 2014. RNAi dynamics in Juvenile Fasciola spp. Liver flukes reveals the persistence of gene silencing in vitro. PLoS Negl Trop Dis 8: e3185.
-
27.
Walker JM, 1994. The bicinchoninic acid (BCA) assay for protein quantitation. Walker JM, ed. Basic Protein and Peptide Protocols. Totowa, NJ: Humana Press, 5–8.
-
28.
Phadungsil W, Smooker PM, Vichasri-Grams S, Grams R, 2016. Characterization of a Fasciola gigantica protein carrying two DM9 domains reveals cellular relocalization property. Mol Biochem Parasitol 205: 6–15.
-
29.
Geadkaew A, Kosa N, Siricoon S, Grams SV, Grams R, 2014. A 170 kDa multi-domain cystatin of Fasciola gigantica is active in the male reproductive system. Mol Biochem Parasitol 196: 100–107.
-
30.
Siricoon S, Grams SV, Grams R, 2012. Efficient inhibition of cathepsin B by a secreted type 1 cystatin of Fasciola gigantica. Mol Biochem Parasitol 186: 126–133.
-
31.
Tarasuk M, Grams SV, Viyanant V, Grams R, 2009. Type I cystatin (stefin) is a major component of Fasciola gigantica excretion/secretion product. Mol Biochem Parasitol 167: 60–71.
-
32.
Vichasri-Grams S, Subpipattana P, Sobhon P, Viyanant V, Grams R, 2006. An analysis of the calcium-binding protein 1 of Fasciola gigantica with a comparison to its homologs in the phylum Platyhelminthes. Mol Biochem Parasitol 146: 10–23.
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Evaluation of a Commercial Enzyme-Linked Immunosorbent Assay Kit and In-House Fasciola gigantica Cysteine Proteinases-Based Enzyme-Linked Immunosorbent Assays for Diagnosis of Human Fascioliasis
Na T. D. Tran
Na T. D. Tran
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Department of Parasitology, Hue University of Medicine and Pharmacy, Hue, Vietnam;
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Department of Parasitology, Hue University of Medicine and Pharmacy, Hue, Vietnam;
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Phuong Anh Ton Nu
Phuong Anh Ton Nu
Department of Parasitology, Hue University of Medicine and Pharmacy, Hue, Vietnam;
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Kitti Intuyod
Kitti Intuyod
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Ly T. K. Dao
Ly T. K. Dao
Institute of Malariology, Parasitology and Entomology Quy Nhon, Quy Nhon, Vietnam;
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Porntip Pinlaor
Porntip Pinlaor
Faculty of Associated Medical Sciences, Centre for Research and Development of Medical Diagnostic Laboratories, Khon Kaen University, Khon Kaen, Thailand;
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Yukifumi Nawa
Yukifumi Nawa
Faculty of Medicine, Tropical Diseases Research Centre, Khon Kaen University, Khon Kaen, Thailand;
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Kiattawee Choowongkomon
Kiattawee Choowongkomon
Department of Biochemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand;
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Amornrat Geadkaew-Krenc
Amornrat Geadkaew-Krenc
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Pathumthani, Thailand
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Nanthawat Kosa
Nanthawat Kosa
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Pathumthani, Thailand
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Rudi Grams
Rudi Grams
Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Pathumthani, Thailand
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Somchai Pinlaor
Somchai Pinlaor
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Fascioliasis, caused by Fasciola hepatica and Fasciola gigantica infection, is a major food-borne trematodiasis in many places of the world, with the central region of Vietnam being reported as a highly endemic area. Stool examination for Fasciola eggs is not a sensitive method, and immunodiagnostic methods are preferable. We investigated various enzyme-linked immunosorbent assays (ELISAs) to evaluate their efficacy for fascioliasis diagnosis. Test sera used are primarily screened using an ELISA kit produced in Vietnam (VN kit; Viet Sinh Chemical Producing & Trading Co. Ltd., Ho Chi Minh City, Vietnam): Seropositive individuals having symptoms compatible with fascioliasis were regarded as clinically diagnosed fascioliasis cases. A commercial Fasciola IgG ELISA kit from Diagnostic Automation/Cortez Diagnostics, Inc. (USA kit; Woodland Hills, CA), which has been commonly used in Vietnam, was assessed and compared with in-house ELISA systems, including a cystatin-capture (CC) ELISA using crude worm extract (CWE) and an indirect ELISA using a synthetic peptide Ac-TPTCHWECQVGYNKTYDEE-NHMe designed from the F. gigantica cathepsin B (FgCB5) molecule. The USA kit was suitable for routine diagnosis after recalibration of the manufacturer’s suggested cutoff point. Cystatin-capture ELISA with CWE provided good sensitivity and specificity with perfect agreement to the results of the USA kit. In dot-blot ELISA, recombinant FgCB5 reacted more strongly with human antisera than did other F. gigantica antigens tested. Enzyme-linked immunosorbent assay using the synthetic peptide fragment of the FgCB5 exhibited nearly 80% sensitivity and specificity, but the test results showed low agreement with CC-ELISA or the USA kit. In conclusion, the commercially available Fasciola IgG ELISA kit from the United States and the in-house CC ELISA using CWE are suitable for practical diagnosis for fascioliasis.
Author Notes
Financial support: This research was supported by Invitation Research, Faculty of Medicine (IN61241), and the Postgraduate Scholarship for International Students, Faculty of Medicine, Khon Kaen University.
Authors’ addresses: Na T. D. Tran, Kitti Intuyod, and Somchai Pinlaor, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mails: t.tranthidiemna@kkumail.com, kitti.i@kkumail.com, and psomec@kku.ac.th. Phuong Anh Ton Nu, Department of Parasitology, Hue University of Medicine and Pharmacy, Hue, Vietnam, E-mail: tnpanh@huemed-univ.edu.vn. Ly T. K. Dao, Institute of Malariology, Parasitology and Entomology Quy Nhon, Quy Nhon, Vietnam, E-mail: khanhly75@yahoo.com. Porntip Pinlaor, Faculty of Associated Medical Sciences, Centre for Research and Development of Medical Diagnostic Laboratories, Khon Kaen University, Khon Kaen, Thailand, E-mail: porawa@kku.ac.th. Yukifumi Nawa, Faculty of Medicine, Tropical Diseases Research Centre, Khon Kaen University, Thailand, E-mail: yukinawa@kku.ac.th. Kiattawee Choowongkomon, Department of Biochemistry, Faculty of Science, Kasetsart University, Bangkok, Thailand, E-mail: kiattawee.c@ku.th. Amornrat Geadkaew-Krenc, Nanthawat Kosa, and Rudi Grams, Graduate Program in Biomedical Sciences, Faculty of Allied Health Sciences, Thammasat University, Pathumthani, Thailand, E-mails: amornrut_gead@hotmail.com, nantha.ko@hotmail.com, and rgrams@tu.ac.th.
- INTRODUCTION
- MATERIALS AND METHODS
- Ethical approval.
- Parasites.
- Identification of Fasciola worms by morphology and molecular techniques.
- Human sera.
- Assessment of the Fasciola IgG ELISA kit produced in the United States and selection of positive control sera.
- Crude worm extract.
- Cystatin capture ELISA with CWE.
- Dot-blot ELISA using recombinant F. gigantica proteins.
- Synthetic peptides design based on FgCB5 sequence.
- Indirect ELISA with synthetic peptide antigen based on FgCB5.
- Statistical analysis.
- RESULTS AND DISCUSSION
- Identification of Fasciola species.
- Assessment of the Fasciola IgG ELISA kit from the United States and selection of positive control sera for subsequent experiments.
- Diagnostic efficacy of CC ELISA using crude worm extract.
- Selection of recombinant proteins using dot-blot analysis.
- Peptide selection and efficacy of synthetic peptide-based ELISA in comparison with other ELISA systems.
- Supplementary Files
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization (WHO) Ntd, 2018. Human Fascioliasis: Review Provides Fresh Perspectives on Infection and Control. Available at: http://www.who.int/neglected_diseases/news/fascioliasis-review-provides-new-perspectives-infection-control/en/. Accessed September 10, 2018.
-
2.
Mas-Coma S, Valero MA, Bargues MD, 2009. Chapter 2. Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69: 41–146.
-
3.
Bui TD, Doanh PN, Saegerman C, Losson B, 2016. Current status of fasciolosis in Vietnam: an update and perspectives. J Helminthol 90: 511–522.
-
4.
Mas-Coma S, Bargues MD, Valero MA, 2018. Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures. Parasitology 145: 1665–1699.
-
5.
World Health Organization (WHO), 2018. Foodborne Trematode Infections. Fascioliasis. Fascioliasis Diagnosis, Treatment and Control Strategy. Available at: http://www.who.int/foodborne_trematode_infections/fascioliasis/fascioliasis_diagnosis/en/. Accessed November 19, 2018.
-
6.
Smooker PM, Jayaraj R, Pike RN, Spithill TW, 2010. Cathepsin B proteases of flukes: the key to facilitating parasite control? Trends Parasitol 26: 506–514.
-
7.
Robinson MW, Menon R, Donnelly SM, Dalton JP, Ranganathan S, 2009. An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Mol Cell Proteomics 8: 1891–1907.
-
8.
Rojas-Caraballo J, López-Abán J, Del Villar LP, Vizcaíno C, Vicente B, Fernández-Soto P, Del Olmo E, Patarroyo MA, Muro A, 2014. In vitro and in vivo studies for assessing the immune response and protection-inducing ability conferred by Fasciola hepatica-derived synthetic peptides containing B-and T-cell epitopes. PLoS One 9: e105323.
-
9.
Rokni MB, Massoud J, Hanilo A, 2003. Comparison of adult somatic and cysteine proteinase antigens of Fasciola gigantica in enzyme linked immunosorbent assay for serodiagnosis of human fasciolosis. Acta Trop 88: 69–75.
-
10.
Ikeda T, 1998. Cystatin capture enzyme-linked immunosorbent assay for immunodiagnosis of human paragonimiasis and fascioliasis. Am J Trop Med Hyg 59: 286–290.
-
11.
Meshgi B, Jalousian F, Fathi S, Jahani Z, 2018. Design and synthesis of a new peptide derived from Fasciola gigantica cathepsin L1 with potential application in serodiagnosis of fascioliasis. Exp Parasitol 189: 76–86.
-
12.
Santana BG, Dalton JP, Camargo FV, Parkinson M, Ndao M, 2013. The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease. PLoS Negl Trop Dis 7: e2414.
-
13.
Tantrawatpan C, Maleewong W, Wongkham C, Wongkham S, Intapan PM, Nakashima K, 2005. Serodiagnosis of human fascioliasis by a cystatin capture enzyme-linked immunosorbent assay with recombinant Fasciola gigantica cathepsin L antigen. Am J Trop Med Hyg 72: 82–86.
-
14.
Intapan PM, Tantrawatpan C, Maleewong W, Wongkham S, Wongkham C, Nakashima K, 2005. Potent epitopes derived from Fasciola gigantica cathepsin L1 in peptide-based immunoassay for the serodiagnosis of human fascioliasis. Diagn Microbiol Infect Dis 53: 125–129.
-
15.
O'Neill SM, Parkinson M, Dowd AJ, Strauss W, Angles R, Dalton JP, 1999. Immunodiagnosis of human fascioliasis using recombinant Fasciola hepatica cathepsin L1 cysteine proteinase. Am J Trop Med Hyg 60: 749–751.
-
16.
Creaney J, Wilson L, Dosen M, Sandeman RM, Spithill TW, Parsons JC, 1996. Fasciola hepatica: irradiation-induced alterations in carbohydrate and cathepsin-B protease expression in newly excysted juvenile liver fluke. Exp Parasitol 83: 202–215.
-
17.
Law RH, Smooker PM, Irving JA, Piedrafita D, Ponting R, Kennedy NJ, Whisstock JC, Pike RN, Spithill TW, 2003. Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infect Immun 71: 6921–6932.
-
18.
Meemon K, Grams R, Vichasri-Grams S, Hofmann A, Korge G, Viyanant V, Upatham ES, Habe S, Sobhon P, 2004. Molecular cloning and analysis of stage and tissue-specific expression of cathepsin B encoding genes from Fasciola gigantica. Mol Biochem Parasitol 136: 1–10.
-
19.
Siricoon S, Vichasri Grams S, Lertwongvisarn K, Abdullohfakeeyah M, Smooker PM, Grams R, 2015. Fasciola gigantica cathepsin B5 is an acidic endo- and exopeptidase of the immature and mature parasite. Biochimie 119: 6–15.
-
20.
Quy TM, Yeatman H, Flood V, Chuong NC, Tuan BV, 2015. Prevalence and risks of fascioliasis among adult cohorts in Binh Dinh and Quang Ngai provinces-central Viet Nam. Vietnam J Public Health 3: 46–61.
-
21.
Huong NT, Duong TD, Tinh TT, 2013. Human Fasciola sp infection in community Nghe an province and comparison of an antibody ELISA detection for serodiagnosis of fascioliasis (in Vietnamese, English abstract). J Vietnam Pract Med 11: 156–160.
-
22.
Duong TD, Huong NT, Tinh TT, 2013. Research applicated the technical standards in diagnostic human fascioliasis in hospital of the national institute of malariology, parasitology and entomology (2011–2013) (in Vietnamese, English abstract). J Vietnam Pract Med 11: 67–71.
-
23.
Van De N, Thi Xuan L, Van Chau L, 2003. Prevalence of first survey of human fasciloliasis in Khanh Hoa province, Vietnam (in Vietnamese). J Vietnam Pract Med 3: 77–80.
-
24.
Periago MV, Valero MA, El Sayed M, Ashrafi K, El Wakeel A, Mohamed MY, Desquesnes M, Curtale F, Mas-Coma S, 2008. First phenotypic description of Fasciola hepatica/Fasciola gigantica intermediate forms from the human endemic area of the Nile Delta, Egypt. Infect Genet Evol 8: 51–58.
-
25.
Itagaki T, Kikawa M, Sakaguchi K, Shimo J, Terasaki K, Shibahara T, Fukuda K, 2005. Genetic characterization of parthenogenic Fasciola sp. in Japan on the basis of the sequences of ribosomal and mitochondrial DNA. Parasitology 131: 679–685.
-
26.
McVeigh P et al. 2014. RNAi dynamics in Juvenile Fasciola spp. Liver flukes reveals the persistence of gene silencing in vitro. PLoS Negl Trop Dis 8: e3185.
-
27.
Walker JM, 1994. The bicinchoninic acid (BCA) assay for protein quantitation. Walker JM, ed. Basic Protein and Peptide Protocols. Totowa, NJ: Humana Press, 5–8.
-
28.
Phadungsil W, Smooker PM, Vichasri-Grams S, Grams R, 2016. Characterization of a Fasciola gigantica protein carrying two DM9 domains reveals cellular relocalization property. Mol Biochem Parasitol 205: 6–15.
-
29.
Geadkaew A, Kosa N, Siricoon S, Grams SV, Grams R, 2014. A 170 kDa multi-domain cystatin of Fasciola gigantica is active in the male reproductive system. Mol Biochem Parasitol 196: 100–107.
-
30.
Siricoon S, Grams SV, Grams R, 2012. Efficient inhibition of cathepsin B by a secreted type 1 cystatin of Fasciola gigantica. Mol Biochem Parasitol 186: 126–133.
-
31.
Tarasuk M, Grams SV, Viyanant V, Grams R, 2009. Type I cystatin (stefin) is a major component of Fasciola gigantica excretion/secretion product. Mol Biochem Parasitol 167: 60–71.
-
32.
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