Abstract
To know if alkaline phosphatase (AP) from schistosomes other than Schistosoma mansoni can be used as diagnostic marker for schistosomiasis in alkaline phosphatase immunocapture assay (APIA), we comparatively tested n-butanol extracts of adult worm membranes from a Venezuelan (JL) strain of S. mansoni (Ven/AWBE/Sm); a Cameroonian (EDEN) strain of Schistosoma intercalatum (Cam/AWBE/Si) and a Yemeni strain of Schistosoma haematobium (Yem/AWBE/Sh). APIA was evaluated with sera of patients from Venezuela, Senegal, and Gabon infected with S. mansoni, from Gabon infected with S. intercalatum or S. haematobium, from Chine infected with Schistosoma japonicum and from Cambodian patients infected with Schistosoma mekongi. Results indicate that 92.5 % (37/40) of Venezuela sera, 75 % (15/20) of Senegal sera, 39.5 % (17/43) of S. haematobium sera, and 19.2 % (5/26) S. intercalatum sera were APIA-positive with the Ven/AWBE/Sm preparation. APIA with the Cam/AWBE/Si preparation showed that 53.8 % of S. intercalatum-positive sera had anti-AP antibodies, and 51.2 % S. haematobium-positive sera cross-immunocapturing the S. intercalatum AP. APIA performed with Yem/AWBE/Sh showed that 55.8 % S. haematobium sera were positive. Only two out of nine S. japonicum sera were APIA-positive with the Ven/AWBE/Sm and Cam/AWBE/Si, and no reaction was observed with Cambodian S. mekongi-positive sera. AP activity was shown to be present in all the schistosome species/strains studied. The use of APIA as a tool to explore the APs antigenicity and the presence of Schistosoma sp. infections through the detection of anti-Schistosoma sp. AP antibodies in a host, allowed us to demonstrate the antigenicity of APs of S. mansoni, S. intercalatum, and S. haematobium.
Similar content being viewed by others
References
Abdel-Fattah M, Al-Sherbiny M, Osman A, Charmy R, Tsang V (2011) Improving the detection limit of quantitative diagnosis of anti-S. haematobium antibodies using Falcon Assay Screening Test (FAST) ELISA by developing a new standard curve. Parasitol Res 108:1457–1463
Alarcón de Noya B, Cesari IM, Losada S, Colmenares C, Balzán C, Hoebeke J, Noya O (1997) Evaluation of alkaline phosphatase immunoassay and comparison with other diagnostic methods in areas of low transmission of schistosomiasis. Acta Trop 66:69–78
Alarcón de Noya B, Gevara R, Colmenares C, Losada S, Noya O (2006) Low transmission areas of schistosomiasis in Venezuela: consequences on the diagnosis, treatment, and control. Mem Inst Oswaldo Cruz 101:29–35
Alarcón de Noya B, Ruiz R, Losada S, Colmenares C, Contreras R, Cesari IM, Noya O (2007) Detection of schistosomiasis cases in low-transmission areas based on coprologic and serologic criteria the Venezuelan experience. Acta Trop 103:41–49
Al-Sherbiny MM, Osman AM, Hancock K, Deelder AM, Tsang VC (1999) Application of immunodiagnostic assays: detection of antibodies and circulating antigens in human schistosomiasis and correlation with clinical findings. Am J Trop Med Hyg 60:960–966
Ballen D, Théron A, Pointier JP, Coustau C, Cesari IM (2002) Schistosoma mansoni: identification of a possible daughter sporocyst alkaline phosphatase. Exp Parasitol 101:164–167
Bhardwaj R, Skelly PJ (2011) Characterization of schistosome tegumental alkaline phosphatase (SmAP). PLoS Negl Trop Dis 5(4):e1011
Bradford M (1976) A rapid and sensitive method for the quantitation of micrograms quantities of protein utilizing the principle of protein-dye binding. Annal Biochem 72:248–254
Braschi S, Wilson AR (2006) Proteins exposed at the adult Schistosome surface revelaled by biotinylation. Mol Cell Prot 5:347–356
Braschi S, William CB, Wilson AR (2006) Proteomic analysis of the schistosome tegument and its surface membrane. Mem Inst Oswaldo Cruz 101:205–212
Cavalcanti MG, Silva LF, Peralta RHS, Barreto MGM, Peralta JM (2013) Schistosomiasis in areas of low endemicity: a new era in diagnosis. Trends Parasitol 2:75–82
Cesari IM (1974) Schistosoma mansoni: distribution and characteristics of alkalines and acid phosphatase. Exp Parasitol 36:405–414
Cesari IM, Simpson AJH, Evans WH (1981) Properties of a series of tegumental membrane bound phosphohydrolase activities of Schistosoma mansoni. Biochem J 198:467–473
Cesari IM, Pujol FH, Rodríguez M, Alarcón De Noya B (1987) Possible use of Schistosoma mansoni enzymes as antigens for immunodiagnosis. Mem Inst Oswaldo Cruz 82(IV):175–177
Cesari IM, Ferrer A, Kombila M, Pichard E, Decam E, Li-Shu Q, Bout D, Richard-Lenoble D (1998) Specificity of the solid phase alkaline phosphatase immunocapture assay for the diagnosis of human Schistosoma mansoni infection. Trans R Soc Trop Med Hyg 9:38–39
Cesari IM, Mendoza L, Ballen DE, Alarcón de Noya B (2002) Evaluación del “IEFA” como técnica de inmunodiagnóstico en el programa de lucha contra la bilharziosis. Bol Mal San Amb XLII:29–32
Cesari IM, Ballen DE, Mendoza L, Matos C (2005) Detection of Schistosoma mansoni membrane antigens by immunoblot analysis of sera of patients from low-transmission areas. Clin Diag Lab Immunol 2:280–286
Cesari IM, Ballen DE, Mendoza L, Ferrer A, Pointier JP, Kombila M, Richard-Lenoble D, Théron A (2010) Immunoblot analysis of membrane antigens of Schistosoma mansoni, Schistosoma intercalatum, and Schistosoma haematobium against Schistosoma-infected patient sera. Parasitol Res 106:1225–1231
Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77:41–51
Deelder AM, Qian ZL, Kremsner PG, Acosta L, Rabello AL et al (1994) Quantitative diagnosis of Schistosoma infections by measurement of circulating antigens in serum and urine. Trop Geogr Med 46:233–238
Fallon PG, Mcneice C, Probert A, Doenhoff MJ (1994) Quantification of praziquantel-induced damage on the surface of adult Schistosoma mansoni worms: estimation of esterase and alkaline phosphatase activity. Parasitol Res 80:623–625
Farias LP, Tararam CA, Miyasato PA, Nishiyama MY Jr, Oliveira KC, Kawano T, Verjovski-Almeida S, Leite LC (2011) Screening the Schistosoma mansoni transcriptome for genes differentially expressed in the schistosomulum stage in search for vaccine candidates. Parasitol Res 108:123–135
Feldmeier H, Poggensee G (1993) Diagnostic techniques in schistosomiasis control. A review. Acta Trop 52:205–220
Fillié YE, Van Lieshout L, Kornelis D, Deelder AM (1994) Evaluation of an ELISA for combined measurement of CAA and CCA in schistosomiasis mansoni. Acta Trop 57:279–287
Gomes LI, Marques LH, Enk MJ, Coelho PM, Rabello A (2009) Further evaluation of an updated PCR assay for the detection of Schistosoma mansoni DNA in human stool samples. Mem Inst Oswaldo Cruz 8:1194–1196
Hassan MM, Hegab MH, Soliman SZ, Gaber OA, Shalaby MM, Kamel FM (1999) Relationship between circulating antigen level and morbidity in Schistosoma mansoni-infected children evaluated by ultrasonography. Am J Trop Med Hyg 61:635–638
Kusel JR, Mackensie PE, McLaren DD (1975) The release of membrane antigens into culture by adult Schistosoma mansoni. Parasitology 71:247–259
Kongs A, Marks G, Verlé P, Van Der Stuyft P (2001) The unreliability of the Kato–Katz technique limits its usefulness for evaluating Schistosoma mansoni infections. Trop Med Int Health 6:163–169
Lier T, Simonsen GS, Haaheim H, Hjelmevoll SO, Vennervald BJ, Johansen MV (2006) Novel real-time PCr for detection of Schistosoma japonicum in stool. Southeast Asian J Trop Med Public Health 2:257–264
Li YL, Idris MA, Corachan M, Han JJ, Kirschfink M, Ruppel A (1996) Circulating antigens in schistosomiasis: detection of 31/32-kDa proteins in sera from patients infected with Schistosoma japonicum, S. mansoni, S. haematobium, or S. intercalatum. Parasitol Res 82:14–18
Losada S, Chacón N, Colmenares C, Bermúdez H, Lorenzo A, Pointier JP, Theron A, Alarcón De Noya B, Noya O (2005) Schistosoma: Cross-reactivity and antigenic community among different species. Exp Parasitol 3:182–190
Planchart S, Incani RN, Cesari IM (2007) Preliminary characterization of an adult worm “vomit” preparation of Schistosoma mansoni and its potential use as antigen for diagnosis. Parasitol Res 101:301–309
Pontes LA, Dias-Neto E, Rabello A (2002) Detection by polymerase chain reaction of Schistosoma mansoni DNA in human serum and feces. Am J Trop Med Hyg 66:157–162
Pujol FH, Alarcón de Noya B, Cesari IM (1989) Immunodiagnosis of Schistosoma mansoni with APIA (alkaline phosphatase immunoassay). Immunol Invest 18:1071–1080
Pujol FH, Cesari IM (1990) Antigenicity of adult Schistosoma mansoni alkaline phosphatase. Parasite Immunol 12:189–198
Rabello A, Pontes LA, Dias-Neto E (2002) Recent advances in the diagnosis of Schistosoma infection: the detection of parasite DNA. Mem Inst Oswaldo Cruz 97(Suppl 1):171–172
Ruppel A, McLaren DJ (1986) Schistosoma mansoni: surface membrane stability in vitro and in vivo. Exp Parasitol 2:223–236
Shane HL, Verani JR, Abudho B, Montgomery SP, Blackstock AJ, Mwinzi PN, Butler SE, Karanja DM, Secor WE (2011) Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS Negl Trop Dis 5(1):e951
Smith H, Doenhoff M, Aitken C, Bailey W, Ji M, Dawson E, Gilis H, Spence G, Alexander C, van Gool T (2012) Comparison of Schistosoma mansoni soluble cercarial antigens and soluble egg antigens for serodiagnosing schistosome infections. PLoS Negl Trop Dis 6(9):e1815
Stettler M, Siles-Lucas M, Sarciron E, Lawton P, Gottstein B, Hemphill A (2001) Echinococcus multilocularis alkaline phosphatase as a marker for metacestode damage induced by in vitro drug treatment with albendazole sulfoxide and albendazole sulfone. Antimicrob Agents Chemother 8:2256–2262
Sulbarán G, Noya O, Brito B, Ballén DE, Cesari IM (2013) Immunoprotection of mice against Schistosomiasis mansoni using solubilized membrane antigens. PLoS Negl Trop Dis 7(6):e2254
Ten Hove RJ, Verweij JJ, Vereecken K, Polman K, Dieye L, Van Lieshout L, Hove et al (2008) 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
Tsang VC, Wilkins PP (1997) Immunodiagnosis of schistosomiasis. Immunol Invest 26:175–188
Turner P, Lalloo K, Bligh J, Armstrong M, Whitty CJ, Doenhoff MJ, Chiodini PL (2004) Serological speciation of human schistosome infections by ELISA with a panel of three antigens. J Clin Pathol 57:1193–1196
Van Lieshout L, De Jonge N, el Masry NA, Mansour MM, Krijger FW, Deelder AM (1992) Improved diagnostic performance of the circulating antigen assay in human schistosomiasis by parallel testing for circulating anodic and cathodic antigens in serum and urine. Am J Trop Med Hyg 47:463–469
Van Lieshout L, Polderman AM, Deelder AM (2000) Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Trop 77:69–80
Van’t Wout AB, De Jonge N, Wood SM, Van Lieshout L, Mitchell GF, Deelder AM (1995) Serum levels of circulating anodic antigen and circulating cathodic antigen detected in mice infected with Schistosoma japonicum or S. mansoni. Parasitol Res 81:434–437
World Health Organization—WHO (2005) WHO.org: Tropical Disease Research. Schistosomiasis disease information. Retrieved April 26, 2008, from http://www.who.int/tdr/diseases/schisto/diseaseinfo.htm
Acknowledgments
We thank the CNRS (France)-FONACIT (Venezuela) convention for the financial support of travels between France and Venezuela and ECOS-Nord V06A01. We thank César Matos and Anne Rognon for their contribution to maintenance of the life cycles of the schistosome species.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cesari, I.M., Ballén, D.E., Mendoza, L. et al. Comparative evaluation of Schistosoma mansoni, Schistosoma intercalatum, and Schistosoma haematobium alkaline phosphatase antigenicity by the alkaline phosphatase immunoassay (APIA). Parasitol Res 113, 1395–1403 (2014). https://doi.org/10.1007/s00436-014-3780-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-014-3780-5