Background With a national program initiated recently to reduce transmission of Schistosoma japonicum in the People's Republic of China (P.R. China), there is an urgent need for accessible, quality-assured diagnostics for case detection, surveillance, and program monitoring of chemotherapy efficacy and other control interventions in areas of low endemicity. We compared the performance of nine immunodiagnostic tests developed in P.R. China for detection of antibodies against S. japonicum and established their priority for further assessment in field settings. Methodology/Principal Findings Using the Kato-Katz technique as the reference standard, 240 well-characterized archived serum specimens (100 positive and 140 negative) were evaluated in nine immunological tests developed in P.R. China. The enzyme-linked immunoelectrotransfer blot assay (EITB), which uses an adult worm extract of S. japonicum, supplied by the Center of Disease Control and Prevention, USA, was also evaluated. The sensitivity and specificity of each test were determined and the reproducibility of each test was assessed by evaluating operator-to-operator and run-to-run variation. In addition the simplicity of use for the end-user was evaluated. All tests showed good sensitivities ranging from 92.0% (95% confidence interval (CI): 86.7–97.3%) to 98.0% (95% CI: 95.3–100.0%). The test specificities varied from 70.0% (95% CI: 62.4–77.6%) to 97.1% (95% CI: 94.4–99.9%). All tests showed excellent reproducibility with a discordant rate in the range of 0–10.0% for operator-to-operator variation and run-to-run variation. All tests, except one magnetic particle-based enzyme-linked immunosorbent assay, were found to be easy to use, especially the dot immunogold filtration assays. Conclusions/Significance Most evaluated tests had acceptable performance characteristics and could make an impact on the schistosomiasis control programs in P.R. China. Three tests with the highest sensitivity, specificity and greatest ease of use, were selected for further evaluation in field settings.
References
[1]
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J (2006) Schistosomiasis and water resources development: systematic review, meta- analysis, and estimates of people at risk. Lancet Infect Dis 6: 411–425. doi: 10.1016/S1473-3099(06)70521-7
[2]
Zhou XN, Wang TP, Wang LY, Guo JG, Yu Q, et al. (2004) The current status of schistosomiasis epidemics in China. Chin J Epidemiol 25: 555–558.
[3]
Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, et al. (2005) The public health significance and control of schistosomiasis in China-then and now. Acta Trop 96: 97–105. doi: 10.1016/j.actatropica.2005.07.005
[4]
Zhou XN, Guo JG, Wu XH, Jiang QW, Zheng J, et al. (2007) Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerg Infect Dis 13: 1470–1476. doi: 10.3201/eid1310.061423
[5]
Wang LD, Utzinger J, Zhou XN (2008) Schistosomiasis control: experiences and lessons from China. Lancet 372: 1793–1795. doi: 10.1016/S0140-6736(08)61358-6
[6]
Wang LD, Chen HG, Guo JG, Zeng XJ, Hong XL, et al. (2009) A strategy to control transmission of Schistosoma japonicum in China. N Engl J Med 360: 121–128. doi: 10.1056/NEJMoa0800135
[7]
Wang LD, Guo JG, Wu XH, Chen HG, Wang TP, et al. (2009) China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop Med Int Health 14: 1475–1483. doi: 10.1111/j.1365-3156.2009.02403.x
[8]
Zhu YC (2005) Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Trop 96: 130–136. doi: 10.1016/j.actatropica.2005.07.007
[9]
Katz N, Chaves A, Pellegrino J (1972) A simple device for quantitative stool thick smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397–400.
[10]
Yu JM, de Vlas SJ, Yuan HC, Gryseels B (1998) Variations in faecal Schistosoma japonicum egg counts. Am J Trop Med Hyg 59: 370–375.
[11]
Zhu HQ, Cao CL, Gao FH, Guo JG, Bao ZP, et al. (2005) Evaluation of effectiveness of modified Kato-Katz technique for diagnosis of schistosomiasis japonica. Chin J Schisto Control 17: 273–277.
[12]
Lin DD, Liu JX, Liu YM, Hu F, Zhang YY, et al. (2008) 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. doi: 10.1016/j.parint.2008.04.005
[13]
Hubbard A, Liang S, Maszle D, Qiu D, Gu X, et al. (2003) Estimating the distribution of worm burden and egg excretion of Schistosoma japonicum by risk group in Sichuan province, China. Parasitology 125: 221–231. doi: 10.1017/S003118200200207X
[14]
Lier T, Simonsen GS, Haaheim H, Hjelmevoll SO, Vennervald BJ, et al. (2006) Novel real-time PCR for detection of Schistosoma japonicum in stool. Southeast Asian J Trop Med Public Health 37: 257–264.
[15]
Lier T, Johansen MV, Hjelmevoll SO, Vennervald BJ, Simonsen GS (2008) PCR for detection of low intensity Schistosoma japonicum infections in a pig model. Acta Trop 105: 74–80. doi: 10.1016/j.actatropica.2007.10.004
[16]
Xia CM, Rong R, Lu ZX, Shi CJ, Xu J, et al. (2009) Schistosoma japonicum: a PCR assay for the early detection and evaluation of treatment in a rabbit model. Exp Parasitol 121: 175–179. doi: 10.1016/j.exppara.2008.10.017
[17]
Xu J, Rong R, Zhang HQ, Shi CJ, Zhu XQ, et al. (2010) Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). Int J Parasitol 40: 327–331. doi: 10.1016/j.ijpara.2009.08.010
[18]
Mott KE, Dixon H (1982) Collaborative study on antigens for immunodiagnosis of schistosomiasis. Bull World Health Organ 60: 729–753.
[19]
Mott KE, Dixon H, Carter CE, Garcia E, Ishii A, et al. (1987) Collaborative study on antigens for immunodiagnosis of Schistosoma japonicum infection. Bull World Health Organ 65: 233–244.
[20]
Wu GL (2002) A historical perspective on the immunodiagnosis of schistosomiasis in China. Acta Trop 82: 193–198. doi: 10.1016/S0001-706X(02)00010-4
[21]
Zhu R, Dang H, Zhang LJ, Li HZ, Zheng CJ, et al. (2009) National surveillance of schistosomiasis in China, 2005-2008. Chin J Schisto Control 21: 358–362.
[22]
World Health Organization (2009) Accessible quality-assured diagnostics. Available: http://dosei.who.int/uhtbin/cgisirsi/vMC？qTyBvfI/307430055/5/0. Accessed 2010 May 17.
[23]
Wang EM, Xu Q, Zhang SQ, Zhang LS, Xie JF, et al. (2007) Advance development of standardized indirect hemagglutination assay kit for detection of Schistosoma japonicum antibody. J Pathogen Biol 2: 421–423, 403.
[24]
Zhou YB, Yang MX, Wang QZ, Zhao GM, Wei JG, et al. (2007) Field comparison of immunodiagnostic and parasitological techniques for the detection of schistosomiasis japonica in the people's republic of China. Am J Trop Med Hyg 76: 1138–1143.
[25]
Yuan MZ, Wang JS, Peng XW, Chen LC, He J, et al. (2008) Effect of IHA and NP30 for screening schistosomiasis. Chin J Schisto Control 2: 76–77.
[26]
Zhu L, Zhu JJ, Wang J (2007) Clinical application of two diagnostic kits for schistosomiasis japonica. Shi Yong Yu Fang Yi Xue 14: 1912–1913.
[27]
Wu FD, Xie ZM, Yuan SJ, Zhao QH, Guo JG, et al. (1991) Study on the diagnosis of schistosomiasis with IHA. Chin J Schisto Control 3: 138–141.
[28]
Yu JM, Yuan HC, Yang QJ, Vlas SD, Gryseels B (2001) Comparison of common methods in the field diagnosis of Schistosoma japonicum infection. Tongji Da Xue Xue Bao 22: 1–4.
[29]
Jiang SF, Qiu JW, Liu Jing, Zhang XP, He YY, et al. (2009) Development of dot immunogold filtration assay kit for rapid detection of antibody to schistosome in human sera. Chin J Schisto Control 21: 500–502.
[30]
Yu XL, Liu ZW, Liu Y, Hu PC, He YK, et al. (2009) Application of DIGFA for detection of antibodies to schistosomiasis japonica. Shi Yong Yu Fang Yi Xue 16: 333–334.
[31]
Wen LY, Chen JH, Ding JZ, Zhang JF, Lu SH, et al. (2005) Evaluation on the applied value of the dot immunogold filtration assay (DIGFA) for rapid detection of anti-Schistosoma japonicum antibody. Acta Trop 96: 142–147. doi: 10.1016/j.actatropica.2005.07.025
[32]
Lin DD, Xu JM, Zhang YY, Liu YM, Hu F, et al. (2008) Evaluation of IgG-ELISA for the diagnosis of Schistosoma japonicum in a high prevalence, low endemicity endemic area of China. Acta Trop 107: 128–133. doi: 10.1016/j.actatropica.2008.05.005
[33]
Huang J, Liu ZS, Yao L, Dong SJ, He Qi, et al. (2009) Application of magnetic particle antibody immunoassay in detection of anti-Schistosoma japonicum egg antibody. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27: 223–226.
Wang XH, Wu XH, Zhou XN (2006) Bayesian estimation of community prevalences of Schistosoma japonicum infection in China. Int J Parasitol 36: 895–902. doi: 10.1016/j.ijpara.2006.04.003
[36]
Guan XH, Shi Y (1996) Collaborative study on evaluation of immunodiagnostic assays in schistosomiasis japonica by treatment efficacy assessment. Chin Med J 109: 659–664.
[37]
Qiu LS, Feng Z, Zhang YH, Li H (2000) Circulating antigen detection in schistosomiasis japonica patients by sandwich ELISA using polyclonal and monoclonal antibodies. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 18: 92–93.
[38]
Chen HG, Zeng XJ, Ge J, Jiang WS, Kikuchi M, et al. (2006) Study of the efficacy of a monoclonal antibody biotin-avidin system for the diagnosis of schistosomiasis japonica. Zhonghua Yu Fang Yi Xue Za Zhi 40: 244–247.
[39]
Doenhoff MJ, Chiodini PL, Hamilton JV (2004) Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends Parasitol 20: 35–39. doi: 10.1016/j.pt.2003.10.019
[40]
Utzinger J, Zhou XN, Chen MG, Bergquist R (2005) Conquering schistosomiasis in China: the long march. Acta Trop 96: 69–96. doi: 10.1016/j.actatropica.2005.08.004
[41]
Bergquist R, Johansen MV, Utzinger J (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25: 151–156. doi: 10.1016/j.pt.2009.01.004
[42]
Tsang VC, Hancock K, Kelly MA, Wilson BC, Madison SE (1983) Schistosoma mansoni adult microsomal antigens, a serologic reagent. II. Specificity of antibody responses to the S. mansoni microsomal antigen (MAMA). J Immunol 130: 1366–1370.
[43]
Xu J, Feng T, Guo JG, Zheng H, Wang Q, et al. (2005) Comprehensive evaluation of several diagnosis agents of schistosomiasis japonica in China. Chin J Schisto Control 17: 116–119.
[44]
Mabey D, Peeling RW, Ustianowski (2004) Diagnostics for the developing world. Nat Rev Microbio l2: 231–240. doi: 10.1038/nrmicro841
[45]
Johansen MV, Sithithaworn P, Bergquist R, Utzinger J (2010) Towards improved diagnosis of zoonotic trematode infections in Southeast Asia. Adv Parasitol 73: 171–195. doi: 10.1016/S0065-308X(10)73007-4
[46]
Banoo S, Bell D, Bossuyt P, Herring A, Mabey D, et al. (2006) Evaluation of diagnostic tests for infectious diseases: general principles. Nat Rev Microbiol 4: 20–32.
[47]
Zhou XN, Bergquist R, Leonardo L, Yang GJ, Yang K, Sodomo M, Olveda R (2010) Schistosomiasis japonica: control and research needs. Adv Parasitol 72: 145–178. doi: 10.1016/S0065-308X(10)72006-6
[48]
Utzinger J, Bergquist R, Olveda R, Zhou XN (2010) Important helminth infections in Southeast Asia: diversity, potential for control and prospects for elimination. Adv Parasitol 72: 1–30. doi: 10.1016/S0065-308X(10)72001-7
