Skip to main content

Advertisement

SpringerLink
Log in

Meta-analysis of the diagnostic efficiency of the questionnaires screening for schistosomiasis

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Schistosomiasis is the second widespread tropical disease that affects the health of over 240 million people of 78 countries. Questionnaires have been commonly used to diagnose schistosomiasis, while no meta-analysis of their efficacy had been reported previously. This meta-analysis was conducted to assess their diagnostic accuracy of schistosomiasis. Studies published prior to December 1, 2014, that had used questionnaires as a diagnostic tool were searched in PubMed, Medline, EMBASE, and China National Knowledge Infrastructure (CNKI) database. A total of 32 studies with 72,812 cases were identified for the meta-analysis. The best diagnostic odds ratio (DOR) was obtained from Schistosoma haematobium (67.68, 95 % confidence interval (CI) = 31.48 to 145.54), followed by Schistosoma japonicum (11.74, 95 % CI = 4.59 to 30.05) then Schistosoma mansoni (2.98, 95 % CI = 1.95 to 4.54). Pooled sensitivity and specificity were respectively 0.82, 0.88, and 0.46, and 0.59, 0.86, and 0.81 for S. japonicum, S. haematobium, and S. mansoni. The multivariable subgroup analyses showed that the questionnaires which had been pretested and standardized had better diagnostic performance. The result suggested that questionnaires can be used to diagnose schistosomiasis with moderate sensitivity and specificity and the questionnaires for diagnosing S. haematobium performed best.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdel-Wahab MF, Esmat G, Medhat E, Narooz S, Ramzy I, El-Boraey Y, Strickland GT (2000) The epidemiology of schistosomiasis in Egypt: Menofia Governorate. Am J Trop Med Hyg 62:28–34

    CAS  PubMed  Google Scholar 

  • Ansell J, Guyatt H, Hall A, Kihamia C, Kivugo J, Ntimbwa P, Bundy D (1997) The reliability of self-reported blood in urine and schistosomiasis as indicators of Schistosoma haematobium infection in school children: a study in Muhenza district, Tanzania. Trop Med Int Health 2:1180–1189

  • ArapSiongok TK, Mahmoud AA, Ouma JH, Warren KS, Muller AS, Handa AK, Houser HB (1976) Morbidity in Schistosomiasis mansoni in relation to intensity of infection: study of a community in Machakos, Kenya. Am J Trop Med Hyg 25:273–284

    CAS  Google Scholar 

  • Bassiouny HK, Hasab AA, El-Nimr NA, Al-Shibani LA, Al-Waleedi AA (2014) Rapid diagnosis of schistosomiasis in Yemen using a simple questionnaire and urine reagent strips. East Mediterr Health J 20:242–249

    CAS  PubMed  Google Scholar 

  • Bogoch II, Andrews JR, Dadzie Ephraim RK, Utzinger J (2012) Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana. Trop Med Int Health 17:1217–1221

    Article  PubMed  Google Scholar 

  • Barakat R, Farghaly A, El-Masry AG, El-Sayed MK, Hussein MH (2000) The epidemiology of schistosomiasis in Egypt: patterns of Schistosoma mansoni infection and morbidity in Kafer El-Sheikh. Am J Trop Med Hyg 62:21–7

    CAS  PubMed  Google Scholar 

  • Barreto ML (1993) Use of risk factors obtained by questionnaires in the screening for Schistosoma mansoni infection. Am J Trop Med Hyg 48:742–747

    CAS  PubMed  Google Scholar 

  • Barreto ML (1998) Questionnaire approach to diagnosis in developing countries. Lancet 352:1164–1165

    Article  CAS  PubMed  Google Scholar 

  • Bergquist R, Johansen MV, Utzinger J (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 25:151–156

    Article  PubMed  Google Scholar 

  • Booth M, Mayombana C, Machibya H, Masanja H, Odermatt P, Utzinger J, Kilima P (1998) The use of morbidity questionnaires to identify communities with high prevalences of schistosome or geohelminth infections in Tanzania. Trans R Soc Trop Med Hyg 92:484–490

    Article  CAS  PubMed  Google Scholar 

  • De Lima e Costa MF, Rocha RS, Colley D, Gazzinelli G, Katz N (1991) Validity of selected clinical signs and symptoms in diagnosis of Schistosoma mansoni infection. Rev Inst Med Trop Sao Paulo 33:12–17

    PubMed  Google Scholar 

  • El-Hawey AM, Amr MM, Abdel-Rahman AH, El-Ibiary SA, Agina AM, Abdel-Hafez MA, Waheeb AA, Hussein MH, Strickland GT (2000) The epidemiology of schistosomiasis in Egypt: Gharbia Governorate. Am J Trop Med Hyg 62:42–48

    CAS  PubMed  Google Scholar 

  • Fürst T, Ouattara M, Silue KD, N’Goran DN, Adiossan LG, Bogoch II, N’Guessan Y, Kone S, Utzinger J, N’Goran EK (2013) Scope and Limits of an anamnestic questionnaire in a control-induced low-endemicity helminthiasis setting in South-Central Côte d’Ivoire. PLoS One 8:e64380

    Article  PubMed Central  PubMed  Google Scholar 

  • Gryseels B (1992) Morbidity due to infection with Schistosoma mansoni: an update. Trop Geogr Med 44:189–200

    CAS  PubMed  Google Scholar 

  • Guyatt H, Brooker S, Lwambo NJ, Siza JE, Bundy DA (1999) The performance of school-based questionnaires of reported blood in urine in diagnosing Schistosoma haematobium infection: patterns by age and sex. Trop Med Int Health 4:751–757

    Article  CAS  PubMed  Google Scholar 

  • Habib M, Abdel Aziz F, Gamil F, Cline BL (2000) The epidemiology of schistosomiasis in Egypt: Qalyubia Governorate. Am J Trop Med Hyg 62:49–54

    CAS  PubMed  Google Scholar 

  • Hailu M, Jemaneh L, Kebede D (1995) The use of questionnaires for the identification of communities at risk for intestinal schistosomiasis in western Gojam. Ethiop Med J 33:103–113

    CAS  PubMed  Google Scholar 

  • Hua HY, Liang YS, Zhang Y, Wei JF, Guo HX (2010) The sensitivity of artesunate against Schistosoma japonicum decreased after 10 years of use in China. Parasitol Res 107:873–878

    Article  PubMed  Google Scholar 

  • He JX, Zhang XG, Zheng BQ, Fang GR, Wan SK, Wang QZ, Xia CG, Dong XZ, Wu WZ, Ge JH (1999) Moderately endemic area of schistosomiasis in contaminated water contact as indicators of chemotherapy evaluation research. J Trop Dise Parasit 28:25–28

    Google Scholar 

  • Jemaneh L, Shewakena F, Tedla S (1996) The use of questionnaires for the identification of high risk areas for urinary schistosomiasis: the Ethiopian experience. Ethiop Med J 34:93–105

    CAS  PubMed  Google Scholar 

  • Kihara J, Mwandawiro C, Waweru B, Gitonga CW, Brooker S (2011) Preparing for national school-based deworming in Kenya: the validation and large-scale distribution of school questionnaires with urinary schistosomiasis. Trop Med Int Health 16:1326–1333

    Article  PubMed Central  PubMed  Google Scholar 

  • Lengeler C, Kilima P, Mshinda H, Morona D, Hatz C, Tanner M (1991a) Rapid, low-cost, two-step method to screen for urinary schistosomiasis at the district level: the Kilosa experience. Bull World Health Organ 69:179–189

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lengeler C, De-Savigny D, Mshinda H, Mayombana C, Tayari S, Hatz C, Degre’mont A, Tanner M (1991b) Community-based questionnaires and health statistics as tools for the cost-efficient identification of communities at risk of urinary schistosomiasis. Int J Epidemio 20:796–807

    Article  CAS  Google Scholar 

  • Lengeler C, Mshinda H, De Savigny D, Kilima P, Morona D, Tanner M (1991c) The value of questionnaires aimed at key informants, and distributed through an existing administrative system, for rapid and cost-effective health assessment. World Health Stat Q 44:150–159

    CAS  PubMed  Google Scholar 

  • Lengeler C, Sala-Diakanda D, Tanner M (1992) Using questionnaires through an existing administrative system: a new approach to health interview surveys. Health Pol Plann 7:10–21

    Article  Google Scholar 

  • Lengeler C, Makwala J, Ngimbi D, Utzinger J (2000) Simple school questionnaires can map both schistosoma mansoni and Schistosoma haematobium in the Democratic Republic of Congo. Acta Trop 74:77–87

    Article  CAS  PubMed  Google Scholar 

  • Lengeler C, Utzinger J, Tanner M (2002a) Screening for schistosomiasis with questionnaires. Trends Parasitol 18:375–377

    Article  PubMed  Google Scholar 

  • Lengeler C, Utzinger J, Tanner M (2002b) Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull World Health Organ 80:235–242

    PubMed Central  PubMed  Google Scholar 

  • Lima e Costa MF, Rocha RS, Firmo JO, Guerra HL, Passos VA, Katz N (1998) Questionnaires in the screening for Schistosoma mansoni infection: a study of socio demographic and water contact variables in four communities in Brazil. Rev Inst Med Trop Sao Paulo 40:93–99

    Article  PubMed  Google Scholar 

  • Li JH, Wang TP, Xiao X, Wu WD, Lu DD, Fang GR, Cai W, Zheng J, Xu J, Wang RR (2002) Screening schemes for determining the subjects of chemotherapy in areas with moderate epidemic of schistosomiasis. Chin J Schisto Contr 14:418–421

    Google Scholar 

  • Mafe MA, von Stamm T, Utzinger J, N’Goran EK (2000) Control of urinary schistosomiasis: an investigation into the effective use of questionnaires to identify high risk communities and individuals in Niger State, Nigeria. Trop Med Int Health 5:53–63

    Article  CAS  PubMed  Google Scholar 

  • Malone JB, Abdel-Rahman MS, El Bahy MM, Huh OK, Shafik M, Bavia M (1997) Geographic information systems and the distribution of Schistosoma mansoniin the Nile delta. Parasitol Today 13:112–119

    Article  CAS  PubMed  Google Scholar 

  • Macaskill P, Gatsonis C, Deeks JJ, Harbord RM, Takwoingi Y (2010) Analysing and Presenting Results. In: Deeks JJ, Bossuyt PM, Gatsonis C, editors. Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy, Version 10, The Cochrane Collaboration. Available from: http://srdta.cochrane.org/

  • Moendeg KJ, Angeles JMM, Goto Y, Leonardo LR, Kirinoki M, Villacorte EA, Rivera PT, Inoue N, Chigusa Y, Kawazu S (2015) Development and optimization of cocktail-ELISA for a unified surveillance of zoonotic schistosomiasis in multiple host species. Parasitol Res 114:1225–1228

    Article  PubMed  Google Scholar 

  • N’Goran EK, Utzinger J, Traore M, Lengeler C, Tanner M (1998) Use of a questionnaire for quick identification of the principal foci of urinary bilharziasis in central Ivory Coast. Med Trop 58:253–260

    Google Scholar 

  • Ndamba J, Makura O, Gwatirisa PR, Makaza N, Kaondera KC (1998) A cost effective two step rapid diagnosis of urinary schistosomiasis in Zimbabwe. Cent Afr J Med 44:167–171

    CAS  PubMed  Google Scholar 

  • Nduka FO, Nwosu EC (2008) Validation of the World Health Organization’s Rapid Assessment method for urinary schistosomiasis in southeastern Nigeria. J Parasitol 94:533–536

    Article  PubMed  Google Scholar 

  • Nooman ZM, Hasan AH, Waheeb Y, Mishriky AM, Ragheb M, Abu-Saif AN, Abaza SM, Serwah AA, El-Gohary A, Saad A, El-Sayed M, Fouad M (2000) The epidemiology of schistosomiasis in Egypt: Ismailia governorate. Am J Trop Med Hyg 62:35–41

    CAS  PubMed  Google Scholar 

  • Ongom VL, Bradley DJ (1972) The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. I. Field studies of a community at Panyagoro. Trans R Soc Trop Med Hyg 66:835–851

    Article  CAS  PubMed  Google Scholar 

  • Proietti FA, Antunes CM (1989) Sensitivity, specificity and positive predictive value of selected clinical signs and symptoms associated with schistosomiasis mansoni. Int J Epidemiol 18:680–683

    Article  CAS  PubMed  Google Scholar 

  • Randrianasolo BS, Rabarijaona LP, Ravaoalimalala VA, Ravoniarimbinina P, Migliani R (2002) Validation of questionnaire methods to identify Schistosoma haematobium bilharziasis hyperendemic zones in Madagascar. Arch Inst Pasteur Madagascar 68:59–62

    CAS  PubMed  Google Scholar 

  • Red Urine Study Group (1995) Identification of high-risk communities for schistosomiasis in Africa: A multi-country study. WHO TDR: SER Report Series, No. 15

  • Sarhan RM, Aminou HA, Saad GAR, Ahmed OA (2014) Comparative analysis of the diagnostic performance of adult, cercarial and egg antigens assessed by ELISA, in the diagnosis of chronic human Schistosoma mansoni infection. Parasitol Res 113:3467–3476

    Article  PubMed  Google Scholar 

  • Stothard JR, Mgeni AF, Khamis S, Seto E, Ramsan M, Rollinson D (2002) Urinary schistosomiasis in schoolchildren on Zanzibar Island (Unguja), Tanzania: a parasitological survey supplemented with questionnaires. Trans R Soc Trop Med Hyg 96:507–514

    Article  CAS  PubMed  Google Scholar 

  • Sukwa TY, Bulsara MK, Wurapa FK (1985) Evaluation of selected symptoms in the diagnosis of Schistosoma mansoni infection. Trop Geogr Med 37:295–297

    CAS  PubMed  Google Scholar 

  • Sukwa TY, Bulsara MK, Wurapa FK (1986) The relationship between morbidity and intensity of Schistosoma mansoni infection in a rural Zambian community. Int J Epidemiol 15:248–251

    Article  CAS  PubMed  Google Scholar 

  • Siziya S, Mushanga M, Marufu T, Mudyarabikwa O (1996) Diagnostic and cost comparison of a questionnaire against a chemical reagent strip test in identifying high risk communities for Schistosoma haematobium infection in northern Zambia. Cent Afr J Med 42:40–42

    CAS  PubMed  Google Scholar 

  • Tan H, Yang M, Wu Z, Zhou J, Liu A, Li S, Yang T, Zhou Y, Sun Z (2004) Rapid screening method for Schistosoma japonicum infection using questionnaires in flood area of the People’s Republic of China. Acta Trop 90:1–9

    Article  PubMed  Google Scholar 

  • Tan D, Yu D, Li Y, Xie M, Wen H, Cai W, He W (2001) Two strategic cost and effect of chemotherapies in severe epidemic village of schistosomiasis. Pract Prev Med 8:165–168

    Google Scholar 

  • Utzinger J, N’Goran EK, EsseAya CM, AckaAdjoua C, Lohourignon KL, Tanner M, Lengeler C (1998) Schistosoma mansoni, intestinal parasites and perceived morbidity indicators in schoolchildren in a rural endemic area of western Côte d’Ivoire. Trop Med Int Health 3:711–720

    Article  CAS  PubMed  Google Scholar 

  • Utzinger J, N’Goran EK, Ossey YA, Booth M, Traore M, Lohourignon KL, Allangba A, Ahiba LA, Tanner M, Lengeler C (2000a) Rapid screening for Schistosoma mansoni in western Côte d’Ivoire using a simple school questionnaire. Bull World Health Organ 78:389–398

    PubMed Central  CAS  PubMed  Google Scholar 

  • Utzinger J, N’Goran EK, Tanner M, Lengeler C (2000b) Simple anamnestic questions and recalled water-contact patterns for self-diagnosis Schistosoma manasoni infection among schoolchildren in western Côte d’Ivoire. Am J Trop Med Hyg 62:649–655

    CAS  PubMed  Google Scholar 

  • Vlassoff C, Tanner M (1992) The relevance of rapid assessment to health research and interventions. Health Pol Plann 7:1–9

    Article  Google Scholar 

  • WHO Fact Sheet on Schistosomiasis (2014) Schistosomiasis. Available at: http://www.who.int/schistosomiasis/en/. Accessed 14 November 2014

  • WHO Expert Committee (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of the WHO expert committee. WHO Tech Rep Ser 912:1–57

    Google Scholar 

  • Webbe G, Jordan P (1993) Control. In: Jordan P, Webbe G, Sturrock RF (eds) Human Schistosomiasis. CAB International, Wallingford, pp 405–451

    Google Scholar 

  • Yu LP, Sun X, Yang F, Yang J, Shen J, Wu ZD (2012) Inflammatory cytokines IFN-γ, IL-4, IL-13 and TNF-α alterations in schistosomiasis: a meta-analysis. Parasitol Res 110:1547–1552

    Article  PubMed  Google Scholar 

  • Zhou H, Ross AG, Hartel GF, Sleigh AC, Williams GM, McManus DP, Luo XS, He Y, Li YS (1998) Diagnosis of Schistosomiasis japonica in Chinese schoolchildren by administration of a questionnaire. Trans R Soc Trop Med Hyg 92:245–250

    Article  CAS  PubMed  Google Scholar 

  • Zhou YB, Zhao GM, Jiang QW, Li XJ, Xia ZG (2002) To explore the rapid screening sensitive indicators for Schistosomiasis japonica. Chin J Schisto Contr 15:129–134

    Google Scholar 

  • Zhu HP, Yu CH, Xia X, Dong GY, Tang J, Fang L, Du YK (2010) Assessing the diagnostic accuracy of immunodiagnostic techniques in the diagnosis of Schistosomiasis japonica: a meta-analysis. Parasitol Res 107:1067–1073

    Article  PubMed  Google Scholar 

  • Zhong FY, Liu CX, Zhang XP (2014) Guideline adherence for the treatment of advanced Schistosomiasis japonica in Hubei, China. Parasitol Res 113:4535–4541

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Occupational and Environmental Health, School of Public Health, Wuhan University, Wuhan, China

    Fen Yang, Xiao-dong Tan, Bei Liu, Zi-ling Ni, Xu-dong Gao & Ying Wang

  2. Department of Nursing, Hubei University of Chinese Medicine, Wuhan, China

    Fen Yang

  3. Research Support Center, Brigham Young University, Provo, UT, USA

    Chongming Yang

Authors
  1. Fen Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-dong Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chongming Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zi-ling Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xu-dong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao-dong Tan.

Appendix

Appendix

A. Common questions about schistosomiasis (choices for answers)

  1. 1.

    What is your status of schistosomiasis infection?

  2. 2.

    Past schistosomiasis infection (yes, no)?

  3. 3.

    Have you been treated for schistosomiasis (yes, no)? If yes, answer: type of treatment, last time treated, and number of times treated?

B. Common questions about signs and symptoms of schistosomiasis infection

  1. 1.

    Itchy skin after water contact, weakness, fever, flatulence, abdominal pain, diarrhea, and blood in stool in the last 2 weeks?(S. japonicum)

  2. 2.

    Have you had any blood in stool, bloody diarrhea, abdominal pain, headache, and fever during the past month?(S. mansoni and S. haematobium)

C. Common questions about contact with potentially infected water

  1. 1.

    What water-contact patterns have you had in the infection season (anti-flood, recreational activities, occupational activities, swimming and paddling, wading, or other type)?

  2. 2.

    How often do you have water-contact activities?

D. Unique questions about S. japonicum

  1. 1.

    How many minutes were you exposed to contagious water each time and in each activity?

  2. 2.

    How large in area was your body exposed to contagious water each time and in each activity?

  3. 3.

    Which body part mainly contacted the water (hand, foot, four limbs, entire body, no contact)?

  4. 4.

    Season of highest recreational water contact (spring, summer, autumn, no contact)?

  5. 5.

    Distance from your home to infected water (<200 m, 200-500 m, >500 m)?

E. Unique questions about S. haematobium for school head-teachers

  1. 1.

    Rank most prevalent disease among schoolchildren (abdominal pain, diarrhoea, malaria, skin diseases, eye diseases, schistosomiasis, respiratory infections, measles, nutritional problems, worms, or other).

  2. 2.

    Rank the signs and symptoms most prevalent among schoolchildren (coughing, itching, headache, fever, abdominal pain, wounds, blood in urine, blood in stool, convulsions, joint pains, diarrhea, other).

  3. 3.

    Which diseases should be prioritized for control (no proposed list)?

F. Unique questions about S. haematobium for children

  1. 1.

    Have you had any blood in urine in the last month?

  2. 2.

    Have you had any pain while urinating in the last 2 weeks (yes, no, don’t know)?

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, F., Tan, Xd., Liu, B. et al. Meta-analysis of the diagnostic efficiency of the questionnaires screening for schistosomiasis. Parasitol Res 114, 3509–3519 (2015). https://doi.org/10.1007/s00436-015-4579-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4579-8

Keywords

Search

Navigation