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Meta-Analysis
. 2015 Mar 11;2015(3):CD009579.
doi: 10.1002/14651858.CD009579.pub2.

Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas

Eleanor A Ochodo  1 , Gowri Gopalakrishna, Bea Spek, Johannes B Reitsma, Lisette van Lieshout, Katja Polman, Poppy Lamberton, Patrick M M Bossuyt, Mariska M G Leeflang
Affiliations
Meta-Analysis

Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas

Eleanor A Ochodo et al. Cochrane Database Syst Rev. .

Abstract

Background: Point-of-care (POC) tests for diagnosing schistosomiasis include tests based on circulating antigen detection and urine reagent strip tests. If they had sufficient diagnostic accuracy they could replace conventional microscopy as they provide a quicker answer and are easier to use.

Objectives: To summarise the diagnostic accuracy of: a) urine reagent strip tests in detecting active Schistosoma haematobium infection, with microscopy as the reference standard; and b) circulating antigen tests for detecting active Schistosoma infection in geographical regions endemic for Schistosoma mansoni or S. haematobium or both, with microscopy as the reference standard.

Search methods: We searched the electronic databases MEDLINE, EMBASE, BIOSIS, MEDION, and Health Technology Assessment (HTA) without language restriction up to 30 June 2014.

Selection criteria: We included studies that used microscopy as the reference standard: for S. haematobium, microscopy of urine prepared by filtration, centrifugation, or sedimentation methods; and for S. mansoni, microscopy of stool by Kato-Katz thick smear. We included studies on participants residing in endemic areas only.

Data collection and analysis: Two review authors independently extracted data, assessed quality of the data using QUADAS-2, and performed meta-analysis where appropriate. Using the variability of test thresholds, we used the hierarchical summary receiver operating characteristic (HSROC) model for all eligible tests (except the circulating cathodic antigen (CCA) POC for S. mansoni, where the bivariate random-effects model was more appropriate). We investigated heterogeneity, and carried out indirect comparisons where data were sufficient. Results for sensitivity and specificity are presented as percentages with 95% confidence intervals (CI).

Main results: We included 90 studies; 88 from field settings in Africa. The median S. haematobium infection prevalence was 41% (range 1% to 89%) and 36% for S. mansoni (range 8% to 95%). Study design and conduct were poorly reported against current standards. Tests for S. haematobium Urine reagent test strips versus microscopyCompared to microscopy, the detection of microhaematuria on test strips had the highest sensitivity and specificity (sensitivity 75%, 95% CI 71% to 79%; specificity 87%, 95% CI 84% to 90%; 74 studies, 102,447 participants). For proteinuria, sensitivity was 61% and specificity was 82% (82,113 participants); and for leukocyturia, sensitivity was 58% and specificity 61% (1532 participants). However, the difference in overall test accuracy between the urine reagent strips for microhaematuria and proteinuria was not found to be different when we compared separate populations (P = 0.25), or when direct comparisons within the same individuals were performed (paired studies; P = 0.21).When tests were evaluated against the higher quality reference standard (when multiple samples were analysed), sensitivity was marginally lower for microhaematuria (71% vs 75%) and for proteinuria (49% vs 61%). The specificity of these tests was comparable. Antigen assayCompared to microscopy, the CCA test showed considerable heterogeneity; meta-analytic sensitivity estimate was 39%, 95% CI 6% to 73%; specificity 78%, 95% CI 55% to 100% (four studies, 901 participants). Tests for S. mansoni Compared to microscopy, the CCA test meta-analytic estimates for detecting S. mansoni at a single threshold of trace positive were: sensitivity 89% (95% CI 86% to 92%); and specificity 55% (95% CI 46% to 65%; 15 studies, 6091 participants) Against a higher quality reference standard, the sensitivity results were comparable (89% vs 88%) but specificity was higher (66% vs 55%). For the CAA test, sensitivity ranged from 47% to 94%, and specificity from 8% to 100% (4 studies, 1583 participants).

Authors' conclusions: Among the evaluated tests for S. haematobium infection, microhaematuria correctly detected the largest proportions of infections and non-infections identified by microscopy.The CCA POC test for S. mansoni detects a very large proportion of infections identified by microscopy, but it misclassifies a large proportion of microscopy negatives as positives in endemic areas with a moderate to high prevalence of infection, possibly because the test is potentially more sensitive than microscopy.

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Conflict of interest statement

The review authors have reported no conflicts of interest.

Figures

1
1
Study flow diagram. * Reasons for exclusion can be found in the table of Characteristics of excluded studies.
2
2
Risk of bias and applicability concerns graph: review authors' judgements about each domain presented as percentages across included studies.
3
3
Forest plot of sensitivity and specificity of the urine reagent strip for microhaematuria. Squares represent sensitivity and specificity of one study, the black line its confidence interval.
4
4
Summary ROC plot of sensitivity versus specificity of the urine reagent strip for microhaematuria. The size of the points is proportional to the study sample size. The solid line shows the summary ROC curve.
5
5
Forest plot of sensitivity and specificity of the urine reagent strip for proteinuria. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
6
6
Summary ROC plot of sensitivity versus specificity of the urine reagent strip for proteinuria. The size of the points is proportional to the study sample size. The solid line shows the summary ROC curve.
7
7
Forest plot of sensitivity and specificity of the urine reagent strip for leukocyturia. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
8
8
Summary ROC plot of sensitivity versus specificity of the urine reagent strip for leukocyturia. The size of the points is proportional to the study sample size. The solid line shows the summary ROC curve.
9
9
Forest plot of the sensitivity and specificity of the urine CCA POC test for S. haematobium. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
10
10
Summary ROC plot of sensitivity versus specificity of the urine CCA POC test for S. haematobium. The size of the points is proportional to the study sample size. The solid line shows the summary ROC curve.
11
11
Forest plot of sensitivity and specificity of the urine CCA POC test for S. mansoni. Squares represent the sensitivity and specificity of one study, the black line its confidence interval. Colley 2013 was a study that included data for 5 studies (done in different countries). Some of the studies had been published earlier (Coulibaly 2011, Erko 2013, Shane 2011, Tchuente 2012). In this case, we used data from Colley 2013, which provided the most recent and updated data.
12
12
Summary ROC plot of sensitivity versus specificity of the urine CCA POC test for S. mansoni. The size of the points is proportional to the study sample size. The thick black point shows the average value for sensitivity and specificity. The inner ellipse around the black spot represents the 95% confidence regions around the summary estimates. The outer ellipse represents the prediction region.
13
13
Summary ROC plot of sensitivity versus specificity showing the indirect comparison between microhaematuria and proteinuria (all studies). The solid lines show the summary ROC curves.
14
14
Summary ROC plot of sensitivity and specificity showing the direct comparison between microhaematuria and proteinuria (paired studies). Study points of microhaematuria and proteinuria from the same study are joined by a dotted line. The solid lines show the summary ROC curves.
15
15
Forest plot of sensitivity and specificity of the urine reagent strip for microhaematuria for studies done after treatment with praziquantel. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
16
16
Summary ROC plot of sensitivity and specificity of the urine reagent strip for microhaematuria for studies done after treatment with praziquantel. The size of the points is proportional to the study sample size
17
17
Diagnostic and treatment strategies. Abbreviations: +ve = positive; ‐ve = negative; CAA = circulating anodic antigen; CCA = circulating cathodic antigen; M+ = microscopy positive; M‐ = microscopy negative; U+ = urine reagent strips positive; U‐ = urine reagent strips negative; Rx = treatment; No Rx = no treatment.
18
18
Risk of bias and applicability concerns summary: review authors' judgements about each domain for each included study. The blank cells refer to information that is not applicable to the stated study.
19
19
Forest plot showing effect of year of study on sensitivity and specificity of microhaematuria.
20
20
Summary ROC plot showing effect of test brand on sensitivity and specificity of microhaematuria.
21
21
Forest plot showing effect of year of study on sensitivity and specificity of proteinuria.
22
22
Summary ROC plot showing effect of test brand on sensitivity and specificity of proteinuria.
23
23
Summary ROC plot showing effect of test brand on sensitivity and specificity of CCA POC mansoni.
24
24
Forest plot of sensitivity and specificity of serum CAA ELISA for S. mansoni. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
25
25
Summary ROC plot of sensitivity versus specificity of serum CAA ELISA for S. mansoni. The size of the points is proportional to the study sample size.
26
26
Forest plot of sensitivity and specificity of serum CAA ELISA for S. haematobium. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
27
27
Summary ROC plot of sensitivity versus specificity of serum CAA ELISA for S. haematobium. The size of the points is proportional to the study sample size
28
28
Forest plot of sensitivity and specificity of serum CCA ELISA for S. mansoni. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
29
29
Forest plot of sensitivity and specificity of urine CCA ELISA for S. mansoni. Squares represent the sensitivity and specificity of one study, the black line its confidence interval.
1
1. Test
Microhaematuria.
2
2. Test
Microhaematuria after treatment.
3
3. Test
CCA POC mansoni trace threshold.
4
4. Test
Proteinuria.
5
5. Test
Leukocyturia.
6
6. Test
CCA POC mansoni +1 threshold.
7
7. Test
CCA POC mansoni with good reference standard.
8
8. Test
CCA POC haematobium.
10
10. Test
CCA POC mixed species.
11
11. Test
Serum CAA ELISA mansoni.
12
12. Test
Serum CAA ELISA haematobium.
13
13. Test
Urine CAA ELISA mansoni.
14
14. Test
Urine CAA ELISA haematobium.
15
15. Test
Serum CCA ELISA mansoni.
16
16. Test
Serum CCA ELISA haematobium.
17
17. Test
Urine CCA ELISA mansoni.
19
19. Test
Urine CCA ELISA haematobium.
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References

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    1. Navaratnam AM, Mutumba‐Nakalembe MJ, Stothard JR, Kabatereine NB, Fenwick A, Sousa‐Figueiredo JC. [Notes on the use of urine‐CCA dipsticks for detection of intestinal schistosomiasis in preschool children.]. Transactions of the Royal Society of Tropical Medicine & Hygiene 2012;106(10):619‐22. - PubMed
Ndamukong 2001 {published data only}
    1. Ndamukong KJ, Ayuk MA, Dinga JS, Akenji TN. [Prevalance and intensity of urinary schistosomiasis in primary school children of the Kotto Barombi]. East African Medical Journal 2001;78(6):287‐9. - PubMed
Ndlovu 1996 {published data only}
    1. Ndhlovu P, Cadman H, Gundersen S, Vennervald BJ, Friis H, Christensen NO, et al. [Circulating anodic antigen (CAA) levels in different age groups in a Zimbabwean rural community endemic for Schistosoma haematobium determined using the magnetic beads antigen‐capture enzyme‐linked immunoassay]. American Journal of Tropical Medicine and Hygiene 1996;54(5):537‐42. - PubMed
Nduka 1995 {published data only}
    1. Nduka FO, Ajaero CM, Nwoke BE. [Urinary schistosomiasis among school children in an endemic community in south‐eastern Nigeria]. Applied Parasitology 1995;36:34‐40. - PubMed
Ndyomugyenyi 2001 {published data only}
    1. Ndyomugyenyi R, Minjas JN. [Urinary schistosomiasis in schoolchildren in Dar‐es‐Salaam, Tanzania, and the factors influencing its transmission]. Annals of Tropical Medicine and Parasitology 2001;95(7):697‐706. - PubMed
Ngándu 1988 {published data only}
    1. Ngándu NH. [The use of Baye's theorem and other indices of agreement in evaluating the use of reagent strips in screening rural school children for Schistosoma haematobium in Zambia]. International Journal of Epidemiology 1988;17(1):202‐8. - PubMed
NGoran 1989 {published data only}
    1. N'Goran KE, Yapi YG, Rey J‐L, Soro B, Coulibaly A, Bellec C. Screening of urinary schistosomiasis by sticks reactive to haematuria study in Ivory Coast [Depistage de la schistosomose urinaire par bandelettes reactives a l'hematurie. Evaluation en zones de moyenne et faible endemie de cote‐d'ivoire]. Bulletin de la Societe de Pathologie Exotique et de Ses Filiales 1989;82(2):236‐42. - PubMed
Nmorsi 2005 {published data only}
    1. Nmorsi OPG, Egwunyenga OA, Ukwandu NCD, Nwokolo NQ. [Urinary schistosomiasis in a rural community in Edo state, Nigeria: eosinophiluria as a diagnostic marker]. African Journal of Biotechnology 2005;4(2):183‐6.
Nwaorgu 1992 {published data only}
    1. Nwaorgu OC, Anigbo EU. [The diagnostic value of haematuria and proteinuria in Schistosoma haematobium infection in southern Nigeria]. Journal of Helminthology 1992;66(3):177‐85. - PubMed
Ofori 1986 {published data only}
    1. Ofori‐Adjei D, Adjepon‐Yamoah KK, Ashitey GA, Osei‐Tutu E. [Screening methods for urinary schistosomiasis in an endemic area (the Kraboa/Coaltar district of Ghana)]. Annals of Tropical Medicine and Parasitology 1986;80(3):365‐6. - PubMed
Okeke 2014_settingA {published data only}
    1. Okeke OC, Obachukwu PO. [Performance of three rapid screening methods in the detection of Schistosoma haematobium infection in school‐age children in Southeastern Nigeria]. Pathogens and Global Health 2014;108(2):111‐7. - PMC - PubMed
Okeke 2014_settingB {published data only}
    1. Okeke OC, Obachukwu PO. [Performance of three rapid screening methods in the detection of Schistosoma haematobium infection in school‐age children in Southeastern Nigeria]. Pathogens and Global Health 2014;108(2):111‐7. - PMC - PubMed
Onayade 1996 {published data only}
    1. Onayade AA, Abayomi IO, Fabiyi AK. [Urinary schistosomiasis: options for control within endemic rural communities. A case study in south‐west Nigeria]. Public Health 1996;110(4):221‐7. - PubMed
Poggensee 2000_settingA {published data only}
    1. Poggensee G, Krantz I, Kiwelu I, Feldmeier H. [Screening of Tanzanian women of childbearing age for urinary schistosomiasis: validity of urine reagent strip readings and self‐reported symptoms]. Bulletin of the World Health Organization 2000;78(4):542‐8. - PMC - PubMed
Poggensee 2000_settingB {published data only}
    1. Poggensee G, Krantz I, Kiwelu I, Feldmeier H. [Screening of Tanzanian women of childbearing age for urinary schistosomiasis: validity of urine reagent strip readings and self‐reported symptoms]. Bulletin of the World Health Organization 2000;78(4):542‐8. - PMC - PubMed
Polman 1995 {published data only}
    1. Polman K, Stelma FF, Gryseels B, Dam GJ, Talla I, Niang M, et al. [Epidemiologic application of circulating antigen detection in a recent Schistosoma mansoni focus in Northern Senegal]. American Journal of Tropical Medicine and Hygiene 1995;53(2):152‐7. - PubMed
Pugh 1980 {published data only}
    1. Pugh RNH, Bell DR, Gilles HM. [The potential medical importance of bilharzia in northern Nigeria: a suggested rapid, cheap and effective solution for control of Schistosoma haematobium infection]. Annals of Tropical Medicine and Parasitology 1980;74(6):597‐613. - PubMed
Rasendramino 1998 {published data only}
    1. Rasendramino MH, Rajaona HR, Ramarokoto CE, Ravaoalimalala VE, Leutscher P, Cordonnier D, et al. [Prevalence of uro‐nephrologic complications of urinary bilharziasis in hyperendemic focus in Madagascar]. Nephrologie 1998;19(6). - PubMed
Robinson 2009 {published data only}
    1. Robinson E, Picon D, Sturrock HJ, Sabasio A, Lado M, Kolaczinski J, et al. [The performance of haematuria reagent strips for the rapid mapping of urinary schistosomiasis: field experience from Southern Sudan]. Tropical Medicine and International Health 2009;14(12):1484‐7. - PMC - PubMed
Rollinson 2005 {published data only}
    1. Rollinson D, Klinger EV, Mgeni AF, Khamis IS, Stothard JR. [Urinary schistosomiasis on Zanzibar: application of two novel assays for the detection of excreted albumin and haemoglobin in urine]. Journal of Helminthology 2005;79(3):199‐206. - PubMed
Sarda 1985 {published data only}
    1. Sarda RK, Simonsen PE, Mahikwano LF. [Urban transmission of urinary schistosomaisis in Dar es Salaam, Tanzania]. Acta Tropica 1985;42:71‐8. - PubMed
Sarda 1986 {published data only}
    1. Sarda RK. [Frequency of haematuria and proteinuria in relation to prevalence and intensity of Schistosoma haematobium infection in Dar es Salaam, Tanzania]. East African Medical Journal 1986;63(2):105‐8. - PubMed
Savioli 1990 {published data only}
    1. Savioli L, Hatz C, Dixon H, Kisumku UM, Mott KE. [Control of morbidity due to Schistosoma haematobium on Pemba Island:Egg excretion and hematuria as indicators of infection]. American Journal of Tropical Medicine and Hygiene 1990;43(3):289‐95. - PubMed
Sellin 1982 {published data only}
    1. Sellin B, Simonkovich E, Ovazza L, Sellin E, Desfontaine M, Rey JL. Value of macroscopic urine examination and reagent strips for the detection of hematuria and proteinuria in the mass diagnosis of urinary schistosomiasis, before and after treatment [Valeur de l'examen macroscopique des urines et des bandelettes reactives pour la detection de l'hematurie et de la proteinurie dans le diagnostic de masse de la schistosomiase urinaire, avant et apres traitement]. Medecine Tropicale 1982;42(5):521‐6. - PubMed
Shane2011_Colley2013 {published data only}
    1. Colley DG, Binder S, Campbell C, King CH, Tchuem Tchuente LA, N'goran EK, et al. [A five‐country evaluation of a point‐of‐care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni]. American Journal of Tropical Medicine and Hygiene 2013;88(3):426‐32. - PMC - PubMed
Shaw 1998 {published data only}
    1. Shaw DJ, Picquet M, Ly A, Sambou B, Vercruysse J. [Evaluation of dipsticks in Schistosoma haematobium infections in four villages in the middle valley of the Senegal River Basin, Senegal]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1998;92(6):634‐5. - PubMed
Standley 2010 {published data only}
    1. Standley CJ, Lwambo NJS, Lange CN, Kariuki HC, Adriko M, Stothard JR. [Performance of circulating cathodic antigen (CCA) urine‐dipsticks for rapid detection of intestinal schistosomiasis in schoolchildren from shoreline communities of Lake Victoria]. Parasites and Vectors 2010;3(1). - PMC - PubMed
Stephenson 1984 {published data only}
    1. Stephenson LS, Latham MC, Kinoti SN, Oduori ML. [Sensitivity and specificity of reagent strips in screening of Kenyan children for Schistosoma haematobium infection]. American Journal of Tropical Medicine and Hygiene 1984;33(5):862‐71. - PubMed
Stothard 2006 {published data only}
    1. Stothard JR, Kabatereine NB, Tukahebwa EM, Kazibwe F, Rollinson D, Mathieson W, et al. [Use of circulating cathodic antigen (CCA) dipsticks for detection of intestinal and urinary schistosomiasis]. Acta Tropica 2006;97(2):219‐28. - PubMed
Stothard 2009a {published data only}
    1. Stothard JR, Sousa‐Figueiredo JC, Standley C, Dam GJ, Knopp S, Utzinger J, et al. [An evaluation of urine‐CCA strip test and fingerprick blood SEA‐ELISA for detection of urinary schistosomiasis in schoolchildren in Zanzibar]. Acta Tropica 2009;111(1):64‐70. - PubMed
Stothard 2009b {published data only}
    1. Russell SJ, Sousa‐Figueiredo JC, Simba KI, Garba A, Rollinson D. [Urinary schistosomiasis‐associated morbidity in schoolchildren detected with urine albumin‐to‐creatinine ratio (UACR) reagent strips]. Journal of Pediatric Urology 2009;5(4):287‐91. - PubMed
Tanner 1983_1 {published data only}
    1. Tanner M, Holzer B, Marti HP, Saladin B, Degremont AA. [Frequency of haematuria and proteinuria among Schistosoma haematobium infected children of two communities from Liberia and Tanzania]. Acta Tropica 1983;40(3):231‐7. - PubMed
Tanner 1983_2 {published data only}
    1. Tanner M, Holzer B, Marti HP, Saladin B, Degremont AA. [Frequency of haematuria and proteinuria among Schistosoma haematobium infected children of two communities from Liberia and Tanzania]. Acta Tropica 1983;40(3):231‐7. - PubMed
Tchuente 2012_9KK {published data only}
    1. Tchuem Tchuente LA, Kuete Fouodo CJ, Kamwa Ngassam RI, Sumo L, Dongmo NC, Kenfack CM, et al. [Evaluation of circulating cathodic antigen (CCA) urine‐tests for diagnosis of Schistosoma mansoni infection in Cameroon]. PLoS Neglected Tropical Diseases 2012;6(7):e1758. - PMC - PubMed
Tchuente 2012_Colley2013 {published data only}
    1. Colley DG, Binder S, Campbell C, King CH, Tchuem Tchuente LA, N'goran EK, et al. [A five‐country evaluation of a point‐of‐care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni]. American Journal of Tropical Medicine and Hygiene 2013;88(3):426‐32. - PMC - PubMed
Traore 1998 {published data only}
    1. Traore M, Traore HA, Kardorff R, Diarra A, Landoure Vester U, Doehring E, et al. [The public health significance of urinary schistosomiasis as a cause of morbidity in 2 districts in Mali]. American Journal of Tropical Medicine and Hygiene 1998;59(3):407‐13. - PubMed
Ugbomoiko 2009a {published data only}
    1. Ugbomoiko U.S, Dalumo V, Ariza L, Bezerra FSM, Heukelbach J. [A simple approach improving the performance of urine reagent strips for rapid diagnosis of urinary schistosomiasis in Nigerian schoolchildren]. Memorias do Instituto Oswaldo Cruz 2009;104(3):456‐61. - PubMed
Ugbomoiko 2009b_1 {published data only}
    1. Ugbomoiko US, Obiezue RNN, Ogunniyi TAB, Ofoezie IE. [Diagnostic accuracy of different urine dipsticks to detect urinary schistosomiasis: a comparative study in five endemic communities in Osun and Ogun States, Nigeria]. Journal of Helminthology 2009;83(3):203‐9. - PubMed
Ugbomoiko 2009b_2 {published data only}
    1. Ugbomoiko US, Obiezue RNN, Ogunniyi TAB, Ofoezie IE. [Diagnostic accuracy of different urine dipsticks to detect urinary schistosomiasis: a comparative study in five endemic communities in Osun and Ogun States, Nigeria]. Journal of Helminthology 2009;83(3):203‐9. - PubMed
Van Lieshout 1995 {published data only}
    1. Lieshout L, Panday UG, Jonge N, Krijger FW, Oostburg BF, Polderman AM, et al. [Immunodiagnosis of schistosomiasis mansoni in a low endemic area in Surinam by determination of the circulating antigens CAA and CCA]. Acta Tropica 1995;59(1):19‐29. - PubMed
Van Lieshout 1998_1 {published data only}
    1. Lieshout L, Polman K, Gryseels B, Deelder AM. [Circulating anodic antigen levels in two areas endemic for schistosomiasis mansoni indicate differences in worm fecundity]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1998;92(1):115‐9. - PubMed
Van Lieshout 1998_2 {published data only}
    1. Lieshout L, Polman K, Gryseels B, Deelder AM. [Circulating anodic antigen levels in two areas endemic for schistosomiasis mansoni indicate differences in worm fecundity]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1998;92(1):115‐9. - PubMed
Verle 1994 {published data only}
    1. Verle P, Stelma F, Desreumaux P, Dieng A, Diaw O, Kongs A, et al. [Preliminary study of urinary schistosomiasis in a village in the delta of the Senegal river basin, Senegal]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1994;88(4):401‐5. - PubMed
Warren 1979 {published data only}
    1. Warren KS, Mahmoud AAF, Muruka JF, Whittaker LR, Ouma JH, Arap Siongok TK. [Schistosomaisis haematobia in Coast province Kenya]. American Journal of Tropical Medicine and Hygiene 1979;28(5):864‐70. - PubMed
Wilkins 1979 {published data only}
    1. Wilkins HA, Goll P, Marshall TF, Moore P. [The significance of proteinuria and haematuria in Schistosoma haematobium infection]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1979;73(1):74‐80. - PubMed
Zumstein 1983 {published data only}
    1. Zumstein A. [A study of some factors influencing the epidemiology of urinary schistosomiasis at Ifakara (Kilombero Districy, Morogoro Region, Tanzania)]. Acta Tropica 1983;40:187‐204. - PubMed

References to studies excluded from this review

Adesola 2012 {published data only}
    1. Adesola H, Uduak N, Olajumoke M, Roseangela N, Chiaka A, Sunday A, et al. [Urine turbidity and microhaematuria as rapid assessment indicators for Schistosoma haematobium infection among school children in endemic areas]. American Journal of Infectious Diseases 2012;8(1).
Brouwer 2004 {published data only}
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Coulibaly 2013_3 {published data only}
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Deelder 1989 {published data only}
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de Jonge 1988 {published data only}
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de Jonge 1989_a {published data only}
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de Jonge 1989_b {published data only}
    1. Jonge N, Fillie YE, Hilberath GW, Krijger FW, Lengeler C, Savigny DH, et al. [Presence of the schistosome circulating anodic antigen (CAA) in urine of patients with Schistosoma mansoni or S. haematobium infections]. American Journal of Tropical Medicine and Hygiene 1989;41(5):563‐9. - PubMed
de Jonge 1990_1 {published data only}
    1. Jonge N, Schommer G, Feldmeier H, Krijger FW, Dafalla AA, Bienzle U, et al. [Mixed Schistosoma haematobium and S. mansoni infection: effect of different treatments on the serum level of circulating anodic antigen (CAA)]. Acta Tropica 1990;48(1):25‐35. - PubMed
de Jonge 1990_2 {published data only}
    1. Jonge N, Kremsner PG, Krijger FW, Schommer G, Fillie YE, Kornelis D, et al. [Detection of the schistosome circulating cathodic antigen by enzyme immunoassay using biotinylated monoclonal antibodies]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1990;84(6):815‐8. - PubMed
Disch 1997 {published data only}
    1. Disch J, Garcia MMA, Krijger GW, Amorim MN, Katz N, Deelder AM, et al. [Daily fluctuation of levels of circulating cathodic antigen in urine of children infected with Schistosoma mansoni in Brazil]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1997;91(2):222‐5. - PubMed
Doehring 1985 {published data only}
    1. Doehring E, Ehrich JH, Vester U, Feldmeier H, Poggensee U, Brodehl J. [Proteinuria, hematuria, and leukocyturia in children with mixed urinary and intestinal schistosomiasis]. Kidney International 1985;28(3):520‐5. - PubMed
Eltoum 1992_b {published data only}
    1. Eltoum IA, Suliaman SM, Ismail BM, Ismail AIA, Ali MMM, Homeida MMA. [Evaluation of eosinophiluria in the diagnosis of schistosomiasis haematobium: a field study]. American Journal of Tropical Medicine and Hygiene 1992;46(6):732‐6. - PubMed
Eyo 2012 {published data only}
    1. Eyo JE, Onyishi GC, Okafor FC. [Urinary schistosomiasis among pregnant women in some endemic tropical semi‐urban communities of Anambra State, Nigeria]. Tropical Biomedicine 2012;29(4):575‐9. - PubMed
Feldmeier 1982 {published data only}
    1. Feldmeier H, Doehring E, Daffalla AA. [Simultaneous use of a sensitive filtration technique and reagent strips in urinary schistosomiasis]. Transactions of the Royal Society of Tropical Medicine and Hygiene 1982;76(3):416‐21. - PubMed
Feldmeier 1986 {published data only}
    1. Feldmeier H, Nogueira‐Queiroz JA, Peixoto‐Queiroz MA, Doehring E, Dessaint JP, Alencar JE, et al. [Detection and quantification of circulating antigen in schistosomiasis by monoclonal antibody. II. The quantification of circulating antigens in human schistosomiasis mansoni and haematobium: relationship to intensity of infection and disease status]. Clinical and Experimental Immunology 1986;65(2):232‐43. - PMC - PubMed
Fillie 1994 {published data only}
    1. Fillie YE, Lieshout L, Kornelis D, Deelder AM. [Evaluation of an ELISA for combined measurement of CAA and CCA in schistosomiasis mansoni]. Acta Tropica 1994;57(4):279‐87. - PubMed
Grenfell 2013 {published data only}
    1. Grenfell R, Harn DA, Tundup S, Da'dara A, Siqueira L, Coelho PM. [New approaches with different types of circulating cathodic antigen for the diagnosis of patients with low Schistosoma mansoni load]. PLoS Neglected Tropical Diseases 2013;7(2):e2054. - PMC - PubMed
Gundersen 1992 {published data only}
    1. Gundersen SG, Haagensen I, Jonassen TO, Figenschau KJ, Jonge N, Deelder AM. [Magnetic bead antigen capture enzyme‐linked immunoassay in microtitre trays for rapid detection of schistosomal circulating anodic antigen]. Journal of Immunological Methods 1992;148(1‐2):1‐8. - PubMed
Hakangard 1996 {published data only}
    1. Hakangard C, Deelder AM, Gabone RM, Nilsson LA, Ouchterlony O. [A comparative study on specific antibodies and circulating antigen (CAA) in serum and parasitological findings for diagnosis of schistosomiasis mansoni in an endemic area in Tanzania]. Acta Tropica 1996;61(3):213‐22. - PubMed
Hassan 1992 {published data only}
    1. Hassan MM, Badawi MA, Strand M. [Circulating schistosomal antigen in diagnosis and assessment of cure in individuals infected with Schistosoma mansoni]. American Journal of Tropical Medicine and Hygiene 1992;46(6):737‐44. - PubMed
Hassan 1994 {published data only}
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Hassan 1999 {published data only}
    1. Hassan MM, Hegab MH, Soliman SZ, Gaber OA, Shalaby MM, Kamel FM. [Relationship between circulating antigen level and morbidity in Schistosoma mansoni‐infected children evaluated by ultrasonography]. American Journal of Tropical Medicine and Hygiene 1999;61(4):635‐8. - PubMed
Jemaneh 1994 {published data only}
    1. Jemaneh L, Tedla S, Birrie H. [The use of reagent strips for detection of urinary schistosomiasis infection in the middle Awash Valley, Ethiopia]. East African Medical Journal 1994;71(10):679‐83. - PubMed
Kahama 1998 {published data only}
    1. Kahama AI, Nibbeling HAM, Zeyl RJM, Vennervald BJ, Ouma JH, Deelder AM. [Detection and quantification of soluble egg antigen in urine of Schistosoma haematobium‐infected children from Kenya]. American Journal of Tropical Medicine and Hygiene 1998;59(5):769‐74. - PubMed
Kahama 1999 {published data only}
    1. Kahama AI, Odek AE, Kihara RW, Vennervald BJ, Kombe Y, Nkulila T, et al. [Urine circulating soluble egg antigen in relation to egg counts, hematuria, and urinary tract pathology before and after treatment in children infected with Schistosoma haematobium in Kenya]. American Journal of Tropical Medicine and Hygiene 1999;61(2):215‐9. - PubMed
Kaiser 1992 {published data only}
    1. Kaiser C, Bergel F, Doehring‐Schwerdtfeger E, Feldmeier H, Ehrich JH. [Urine test strips: reliability of semi‐quantitative findings under tropical conditions]. Pediatric Nephrology 1992;6(2):145‐8. - PubMed
Kassim 1983 {published data only}
    1. Kassim OO, Stek M. [Bacteriuria and hematuria in Infections due to Schistosoma haematobium]. The Journal of Infectious Diseases 1983;147(5):960. - PubMed
Kosinski 2011 {published data only}
    1. Kosinski KC, Bosompem KM, Stadecker MJ, Wagner AD, Plummer J, Durant JL, et al. [Diagnostic accuracy of urine filtration and dipstick tests for Schistosoma haematobium infection in a lightly infected population of Ghanaian schoolchildren]. Acta Tropica 2011;118(2):123‐7. - PubMed
Koukounari 2009 {published data only}
    1. Koukounari A, Webster JP, Donnelly CA, Bray BC, Naples J, Bosompem K, et al. [Sensitivities and specificities of diagnostic tests and infection prevalence of Schistosoma haematobium estimated from data on adults in villages northwest of Accra, Ghana]. American Journal of Tropical Medicine and Hygiene 2009;80(3):435‐41. - PMC - PubMed
Kremsner 1994 {published data only}
    1. Kremsner PG, Enyong P, Krijger FW, Jonge N, Zotter GM, Thalhammer F, et al. [Circulating anodic and cathodic antigen in serum and urine from Schistosoma haematobium‐infected Cameroonian children receiving praziquantel: a longitudinal study]. Clinical Infectious Diseases 1994;18(3):408‐13. - PubMed
Krijger 1994 {published data only}
    1. Krijger FW, Lieshout L, Deelder AM. [A simple technique to pretreat urine and serum samples for quantitation of schistosome circulating anodic and cathodic antigen]. Acta Tropica 1994;56(1):55‐63. - PubMed
Lengeler 1991 {published data only}
    1. Lengeler C, Komba S, Morona D. [Urinary schistosomiasis: influence of the circadian variation of hematuria and proteinuria on reagent stick testing]. Acta Tropica 1991;48(4):313‐7. - PubMed
Leutscher 2008 {published data only}
    1. Leutscher PDC, Dam GTJ, Reimert CM, Ramarakoto C‐E, Deelder AM, Ornbjerg N. [Eosinophil cationic protein, soluble egg antigen, circulating anodic antigen, and egg excretion in male urogenital schistosomiasis]. American Journal of Tropical Medicine and Hygiene 2008;79(3):422‐6. - PubMed
Lodh 2013 {published data only}
    1. Lodh N, Mwansa JC, Mutengo MM, Shiff CJ. [Diagnosis of Schistosoma mansoni without the stool: comparison of three diagnostic tests to detect Schistosoma [corrected] mansoni infection from filtered urine in Zambia]. American Journal of Tropical Medicine and Hygiene 2013;89(1):46‐50. - PMC - PubMed
Lwambo 1997 {published data only}
    1. Lwambo NJ, Savioli L, Kisumku UM, Alawi KS, Bundy DA. [Control of Schistosoma haematobium morbidity on Pemba Island: validity and efficiency of indirect screening tests]. Bulletin of the World Health Organization 1997;75(3):247‐52. - PMC - PubMed
Madwar 1988 {published data only}
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Melchers 2014 {published data only}
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Mott 1983 {published data only}
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