Abstract
Schistosomiasis affects more than 4 million school-aged children in Zambia, mostly in rural communities due to unsafe water and inadequate sanitation facilities. Although several studies were done in Zambia between 1976 and 2019, empirical estimates of the disease burden remain unavailable. Therefore, appraisal of the current schistosomiasis burden is pertinent in the re-evaluation of schistosomiasis-control strategies in Zambia. A random-effect model was used to estimate the prevalence of schistosomiasis infection in Zambia across different age groups for the period between 1976 and 2019. A literature search was done in the following databases: PubMed, ISI Web of Science, Google Scholar, CINAHL, and African Journals Online. Twenty-eight studies with relevant prevalence data were identified and included in the analysis. The pooled prevalence estimate of Schistosoma haematobium and Schistosoma mansoni across studies for the entire period was 35.5% (95% CI: 25.8–45.9) and 34.9% (95% CI: 20.7–50.6), respectively. Prevalence estimates among school-aged children for S. haematobium and S. mansoni were 32.2% (95% CI: 21.1–44.7) and 18.1% (95% CI: 3.0–38.4), respectively. The reported pooled prevalence estimate for S. haematobium among the adults was 54% (95% CI: 23.2–83.7). Only two studies collected information from preschool aged children. Substantial heterogeneity (I2 = 100%, p < 0.0001) was observed among the studies. Although a reduction in disease prevalence was observed from 1990 to 2010, this was not sustained after 2010. In this meta-analysis, S. haematobium was more prevalent compared to S. mansoni, with more cases observed among school-aged children (SAC). Thus, control programs should target age groups that are highly infected or are at high risk of infection.
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References
Agnew-Blais J, Carnevale J, Gropper A, Shilika E, Bail R, Ngoma M (2010) Schistosomiasis haematobium prevalence and risk factors in a school-age population of peri-urban Lusaka, Zambia. J Trop Pediatr 56:247–253
Barendregt J, Doi S (2016) MetaXL User Guide version 5.3. EpiGear International Pty Ltd
Bhagwandeen S (1976) Schistosomiasis and carcinoma of the bladder in Zambia. S Afr Med J 50:1616–1620
Blair DM (1956) Bilharziasis survey in British West and East Africa, Nyasaland and the Rhodesias. Bull World Health Organ 15:203–273
Bulsara M, Sukwa T, Wurapa F (1985) Risks of liver and spleen enlargement in schistosomiasis mansoni infection in a rural Zambian community. Trans R Soc Trop Med Hyg 79:535–536
Chimbari M, Dhlomo E, Mwadiwa E, Mubila L (2003) Transmission of schistosomiasis in Kariba, Zimbabwe, and a cross-sectional comparison of schistosomiasis prevalences and intensities in the town with those in Siavonga in Zambia. Ann Trop Med Parasitol 97:605–616
Chisenga C, Sinkala E, Chilengi R, Chitundu H, Zyambo Z, Wandeler G, Vinikoor M (2017) Prevalence and clinical significance of schistosomiasis-chronic Hepatitis B virus co-infection in Zambia. BMJ Glob Health 2:A8–A9
Chomba C, Mutale S (2014) Factors characterising high prevalence rates of urinary schistosomiasis in Mufumbwe district, north western province of Zambia. Glob J Biol Agric Health Sci 3:86–95
Dabo A, Badawi HM, Bary B, Doumbo OK (2011) Urinary schistosomiasis among preschool-aged children in Sahelian rural communities in Mali. Parasit Vectors 4:21–27. https://doi.org/10.1186/1756-3305-4-21
Dersimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188
Downes MJ, Brennan ML, Williams HC, Dean RS (2016) Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open 6:e011458
Ekpo UF, Laja-Deile A, Oluwole AS, Sam-Wobo SO, Mafiana CF (2010) Urinary schistosomiasis among preschool children in a rural community near Abeokuta, Nigeria. Parasit Vectors 3:58
Ezeamama A, Bustinduy A, Nkwata A, Martinez L, Pabalan N, King C (2017) Cognitive deficits and loss of education with human Schistosoma species infection–a systematic review and meta-analysis. PLoS Negl Trop Dis
Fenwick A, Webster JP, Bosque-Oliva E, Blair L, Fleming F, Zhang Y, Garba A, Stothard J, Gabrielli AF, Clements A (2009) The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136:1719–1730
Halwindi H, Magnussen P, Olsen A, Lisulo M (2017) Potential contribution of adult populations to the maintenance of schistosomiasis and soil-transmitted helminth infections in the Siavonga and Mazabuka districts of Zambia. J Biosoc Sci 49:265–275
Hessler MJ, Cyrs A, Krenzke SC, Mahmoud ES, Sikasunge C, Mwansa J, Lodh N (2017) Detection of duo-schistosome infection from filtered urine samples from school children in Zambia after MDA. PLoS One 12:e0189400
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ Br Med J 327:557
Hira B (1981) Transmission of schistosomiasis in a rural area in Zambia. Cent Afr J Med 27:244–249
Hotez PJ, Kamath A (2009) Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 3:e412
Hu G-H, Jia H, Song K-Y, Lin D-D, Zhang J, Cao C-L, Xu J, Li D, Jiang W-S (2005) The role of health education and health promotion in the control of schistosomiasis: experiences from a 12-year intervention study in the Poyang Lake area. Acta Trop 96:232–241
Jordan P, Webbe G (1969) Human schistosomiasis. Human schistosomiasis
Kabatereine NB, Fleming FM, Nyandindi U, Mwanza JC, Blair L (2006) The control of schistosomiasis and soil-transmitted helminths in East Africa. Trends Parasitol 22:332–339
Kalinda C, Chimbari MJ, Mukaratirwa S (2018) Schistosomiasis in Zambia: a systematic review of past and present experiences. Infect Dis Poverty 7:41. https://doi.org/10.1186/s40249-018-0424-5
King CH, Dangerfield-Cha M (2008) The unacknowledged impact of chronic schistosomiasis. Chronic Illn 4:65–79
Lai Y-S, Biedermann P, Ekpo UF, Garba A, Mathieu E, Midzi N, Mwinzi P, N'goran EK, Raso G, Assaré RK (2015) Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. Lancet Infect Dis 15:927–940
Leta S, Alemayehu G, Seyoum Z, Bezie M (2016) Prevalence of bovine trypanosomosis in Ethiopia: a meta-analysis. Parasit Vectors 9:139
Lubeya M, Muloshi C, Baboo KS, Sianongo S, Kelly P (2010) Hepatosplenic schistosomiasis. Lancet 376:1645
Moh (2016) The 2017-2021 National Health Sector Strategic Plan (NHSP).
Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–269
Monde C, Syampungani S, Van Den Brink PJ (2016) Natural and human induced factors influencing the abundance of Schistosoma host snails in Zambia. Environ Monit Assess 188:1–14
Mott K, Dixon H, Osei-Tutu E, England E, Ekue K, Tekle A (1985) Indirect screening for Schistosoma haematobium infection: a comparative study in Ghana and Zambia. Bull World Health Organ 63:135
Mubila L, Rollinson D (2002) Snail-parasite compatibility and prevalence of Schistosoma haematobium on the shores of Lake Kariba, Zambia. Ann Trop Med Parasitol 96:165–173
Mungomba L, Kalumba K (1995) Validation of schistosomiasis morbidity symptoms in schoolchildren of Siavonga, Lake Kariba, Zambia. Ann Trop Med Parasitol 89:439–442
Mungomba L, Michelson E (1995) Urban schistosomiasis in Lusaka, Zambia: a preliminary study. J Trop Med Hyg 98:199–203
Mungomba L, Chandiwana S, Madesen H (1993) Schistosomiasis around Siavonga, on the shores of Lake Kariba, Zambia. Ann Trop Med Parasitol 87:365–371
Mungomba L, Chandiwana S, Sukwa T, Marshall I (1998) Effect of human immigration on the age distribution of schistosome infections in Siavonga community, Lake Kariba, Zambia. Ann Trop Med Parasitol 92:279–283
Mutapi F (2015) Changing policy and practice in the control of pediatric schistosomiasis. Pediatrics:peds. 2014–3189
Mutengo MM, Mwansa JC, Mduluza T, Sianongo S, Chipeta J (2014) High Schistosoma mansoni disease burden in a rural district of western Zambia. Am J Trop Med Hyg 91:965–972
Ng'andu N (1988) The use of Baye's theorem and other indices of agreement in evaluating the use of reagent strips in screening rural schoolchildren for Schistosoma haematobium in Zambia. Int J Epidemiol 17:202–208
Ng'andu N, Nkowane B, Watts T (1991) The health status of rural primary schoolchildren in Central Zambia. J Trop Med Hyg 94:169–174
Njenga SM, Mwandawiro CS, Muniu E, Mwanje MT, Haji FM, Bockarie MJ (2011) Adult population as potential reservoir of NTD infections in rural villages of Kwale district, Coastal Kenya: implications for preventive chemotherapy interventions policy. Parasit Vectors 4:175
Osakunor DNM, Mduluza T, Midzi N, Chase-Topping M, Mutsaka-Makuvaza MJ, Chimponda T, Eyoh E, Mduluza T, Pfavayi LT, Wami WM (2018) Dynamics of paediatric urogenital schistosome infection, morbidity and treatment: a longitudinal study among preschool children in Zimbabwe. BMJ Glob Health 3:e000661
Payne L, Turner-Moss E, Mutengo M, Asombang AW, Kelly P (2013) Prevalence of schistosome antibodies with hepatosplenic signs and symptoms among patients from Kaoma, Western Province, Zambia. BMC Res Notes 6:344
Rollinson D, Knopp S, Levitz S, Stothard JR, Tchuenté L-aT, Garba A, Mohammed KA, Schur N, Person B, Colley DG (2013) Time to set the agenda for schistosomiasis elimination. Acta Trop 128:423–440
Rutagwera DG, Tylleskär T (2012) Co-infection with malaria, hookworm and schistosomiasis among school children in Zambezi: a school-based rapid survey. Med J Zambia 39:18–23
Shawa S, Mwase E, Simonsen PE (2014) Surveys for schistosomiasis and soil transmitted helminths in Luangwa, Kalabo and Serenje Districts of Zambia. Med J Zambia 41:174–180
Shehata MA, Chama MF, Funjika E (2018) Prevalence and intensity of Schistosoma haematobium infection among schoolchildren in central Zambia before and after mass treatment with a single dose of praziquantel. Trop Parasitol 8:12
Simoonga C, Kazembe LN, Kristensen TK, Olsen A, Appleton CC, Mubita P, Mubila L (2008) The epidemiology and small-scale spatial heterogeneity of urinary schistosomiasis in Lusaka province, Zambia. Geospat Health 3:57–67
Siwila J, Phiri IG, Enemark HL, Nchito M, Olsen A (2010) Intestinal helminths and protozoa in children in pre-schools in Kafue district, Zambia. Trans R Soc Trop Med Hyg 104:122–128
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. https://doi.org/10.1016/S1473-3099(06)70521-7
Strahan R, Chiyesu KO, Schneider-Kolsky ME (2012) Ultrasound study of liver disease caused by Schistosoma mansoni in rural Zambian schoolchildren. J Med Imaging Radiat Oncol 56:390–397
Sukwa T, Bulsara M, Wurapa F (1986) The relationship between morbidity and intensity of Schistosoma mansoni infection in a rural Zambian community. Int J Epidemiol 15:248–251
Sukwa T, Boatin B, Wurapa F (1988) A three year follow-up of chemotherapy with praziquantel in a rural Zambian community endemic for schistosomiasis mansoni. Trans R Soc Trop Med Hyg 82:258–260
Van Der Werf MJ, De Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, Habbema JDF, Engels D (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86:125–139
Wall KM, Kilembe W, Vwalika B, Dinh C, Livingston P, Lee Y-M, Lakhi S, Boeras D, Naw HK, Brill I (2018) Schistosomiasis is associated with incident HIV transmission and death in Zambia. PLoS Negl Trop Dis 12:e0006902
Who (2016) Mass treatment coverage for ntds - 2016: Zambia and neglected tropical diseases. doi:https://unitingtocombatntds.org/wp-content/uploads/2018/01/Zambia_eng.pdf
Who (2019) Expanded Special Project for Elimination of Neglected Tropical Diseases (ESPEN): Zambia [Online]. Katima Mulilo, Namibia: WHO. Available: http://espen.afro.who.int/countries/zambia 2019]
Zbcp 2009. Baseline survey for Schistosomiasis and soil transmitted Helminthiasis. Baseline survey for Schistosomiasis and soil-transmitted Helminthiasis. Zambia Bilharzia Control Programme
Zhu X, Zhang J, Fan W, Gong Y, Yan J, Yuan Z, Wu L, Cui H, Luo H, Kong Q (2014) MAPKAP1 rs10118570 polymorphism is associated with anti-infection and anti-hepatic fibrogenesis in schistosomiasis japonica. PLoS One 9:e105995
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CK developed the concept, conducted the literature search, performed statistical analysis, and wrote the initial draft of the manuscript. MMM and MJC contributed to the writing and editing of the paper. All authors approved the final paper for publication.
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Supplementary file S1:
Quality Assessment checklist for eligible studies. (DOCX 27 kb)
Supplementary file S2:
Forest plots of the prevalence estimates. (A) Overall prevalence, (B) S. mansoni, (C) S. haematobium, (D) co-infection of S. mansoni and S. haematobium stratified according to age class. (DOCX 1413 kb)
Supplementary file S3:
Assessment of publication bias. (A) Funnel plot of the double arcsine transformed prevalence estimates of schistosomiasis in SAC, PSAC, and adults, (B) Doi plot the double arcsine transformed prevalence of schistosomiasis in SAC, PSAC, and Adults (LFK index: 2.06). (DOCX 100 kb)
Supplementary file S4:
Prevalence data sets for studies included in the meta-analysis (XLSX 14 kb)
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Kalinda, C., Mutengo, M. & Chimbari, M. A meta-analysis of changes in schistosomiasis prevalence in Zambia: implications on the 2020 elimination target. Parasitol Res 119, 1–10 (2020). https://doi.org/10.1007/s00436-019-06534-0
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DOI: https://doi.org/10.1007/s00436-019-06534-0