Biosocial determinants of persistent schistosomiasis among schoolchildren in Tanzania despite repeated treatment

Donohue, Rose; Mashoto, Kijakazi; Mubyazi, Godfrey; Madon, Shirin; Malecela, Mwele; Michael, Edwin

doi:10.3390/tropicalmed2040061

Cited by 17Parasites and Host InteractionsMollusks and Parasites StudiesParasitic infections in humans and animals

Biosocial determinants of persistent schistosomiasis among schoolchildren in Tanzania despite repeated treatment

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Donohue, Rose, Mashoto, Kijakazi, Mubyazi, Godfrey, Madon, Shirin, Malecela, Mwele, Michael, Edwin·2017·Tropical Medicine and Infectious Disease

DOI 10.3390/tropicalmed2040061PMC PMC6082061

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Abstract

Schistosomiasis is a parasitic disease endemic to Tanzania and other countries of the global south, which is currently being addressed through preventive chemotherapy campaigns. However, there is growing recognition that chemotherapy strategies will need to be supplemented to sustainably control and eventually eliminate the disease. There remains a need to understand the factors contributing to continued transmission in order to ensure the effective configuration and implementation of supplemented programs. We conducted a cross-sectional questionnaire, to evaluate the biosocial determinants facilitating the persistence of schistosomiasis, among 1704 Tanzanian schoolchildren residing in two districts undergoing a preventive chemotherapeutic program: Rufiji and Mkuranga. A meta-analysis was carried out to select the diagnostic questions that provided a likelihood for predicting infection status. We found that self-reported schistosomiasis continues to persist among the schoolchildren, despite multiple rounds of drug administration.Using mixed effects logistic regression modeling, we found biosocial factors, including gender, socio-economic status, and water, sanitation, and hygiene (WASH)-related variables, were associated with this continued schistosomiasis presence. These findings highlight the significant role that social factors may play in the persistence of disease transmission despite multiple treatments, and support the need not only for including integrated technical measures, such as WASH, but also addressing issues of poverty and gender when designing effective and sustainable schistosomiasis control programs.

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Improved sanitation and handwashing reduced under-five mortality, schistosomiasis, and acquiring other soil-transmitted helminths and parasites.
“Other aspects of WASH, including improved sanitation and handwashing, likewise reduced underfive mortality (Ahmed et al., 2016;Dendup et al., 2018), and schistosomiasis (Donohue et al., 2017), or acquiring other soiltransmitted helminths and parasites (Baker et al., 2018).”
From A Systematic Review of Water and Gender Interlinkages: Assessing the Intersection With Health (2020) · cites this paper as Donohue et al., 2017

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Amuta, E., & Houmsou, R. S. (2014) · Asian Pacific Journal of Tropical Medicine · doi:10.1016/s1995-7645(13)60188-1 · Cited by 74 · see citing works
Urinary Tract Morbidity in Schistosomiasis Haematobia: Associations with Age and Intensity of Infection in an Endemic Area of Coast Province, Kenya
King, C. H., Keating, C. E., Muruka, J., Ouma, J. H., Houser, H. B., Siongok, T. K. A., & Mahmoud, A. A. F. (1988) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1988.39.361 · Cited by 73 · cited 1× · see citing works
“School-aged children are particularly vulnerable, as age profiles have shown that prevalence and intensity generally peak among early adolescents, particularly those aged 10–14 years, followed by decreasing prevalence and intensity through adulthood; schistosomiasis-attributed morbidities include anemia and malnutriti…”
Background
Gender-dependent specific immune response during chronic humanSchistosomiasis haematobia
Remoué, F., Van, D., Schacht, A. M., Picquet, M., Garraud, O., Vercruysse, J., Ly, A., Capron, A., & Riveau, G. J. (2001) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2001.01495.x · Cited by 71 · cited 1× · see citing works
“Although studies have suggested that sex-related differences in immunological responses may be a factor in sex-related patterns of infection [107,108], a recent study controlling for cercarial exposure concluded that sex-related differences in S.”
Background
School-based control of urinary schistosomiasis on Zanzibar, Tanzania: Monitoring micro-haematuria with reagent strips as a rapid urological assessment
French, M. D., Rollinson, D., Basáñez, M.-G., Mgeni, A. F., Khamis, I. S., & Stothard, J. R. (2007) · Journal of Pediatric Urology · doi:10.1016/j.jpurol.2007.01.198 · Cited by 70 · see citing works
Schistosoma mansoniInfection and Associated Determinant Factors among School Children in Sanja Town, Northwest Ethiopia
Worku, L., Damte, D., Endris, M., Tesfa, H., & Aemero, M. (2014) · Journal of Parasitology Research · doi:10.1155/2014/792536 · Cited by 69 · see citing works
mada: Meta-Analysis of Diagnostic Accuracy
Doebler, P. (2012) · doi:10.32614/cran.package.mada · Cited by 67 · see citing works
SPATIAL AND TEMPORAL VARIATIONS IN LOCAL TRANSMISSION OF SCHISTOSOMA HAEMATOBIUM IN MSAMBWENI, KENYA
Clennon, J. A., Mungai, P., Muchiri, E. M., King, C. H., & Kitron, U. D. (2006) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2006.75.1034 · Cited by 66 · cited 1× · see citing works
“A study in Kenya, which monitored local water bodies, found that the local perennial river was not cercariae-contaminated, while other local freshwater bodies were contaminated [116].”
Background
The influence of sex and age on antibody isotype responses to Schistosoma mansoni and Schistosoma japonicum in human populations in Kenya and the Philippines
Webster, M. L., LIBRANDA-RAMIREZ, B. D. L., Aligui, G., Olveda, R. M., Ouma, J. H., Kariuki, H. C., KIMANI, G., Olds, G. R., Fulford, A. J. C., Butterworth, A. E., et al. (1997) · Parasitology · doi:10.1017/s003118209600858x · Cited by 65 · cited 1× · see citing works
“Although studies have suggested that sex-related differences in immunological responses may be a factor in sex-related patterns of infection [107,108], a recent study controlling for cercarial exposure concluded that sex-related differences in S.”
Background
Malumfashi Endemic Diseases Research Project, XV
Pugh, R. N. H., Bell, D. R., & Gilles, H. M. (1980) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1980.11687393 · Cited by 61 · see citing works
The role of human water contact patterns in the transmission of schistosomiasis in an informal settlement near a major industrial area
Kvalsvig, J. D., & Schutte, C. H. J. (1986) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1986.11811980 · Cited by 55 · see citing works
A national survey of the prevalence of schistosomiasis and soil transmitted helminths in Malaŵi
Bowie, C., Purcell, B., Shaba, B., Makaula, P., & Perez, M. A. (2004) · BMC Infectious Diseases · doi:10.1186/1471-2334-4-49 · Cited by 53 · see citing works
Schistosomiasis Haematobia in Coast Province Kenya
Warren, K. S., Mahmoud, A. A. F., Muruka, J., Whittaker, L. R., Ouma, J. H., & Siongok, T. K. A. (1979) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1979.28.864 · Cited by 53 · see citing works
Factors related to transmission of and infection with Schistosoma mansoni in a village in the South-eastern Region of Brazil
Enk, M. J., Lima, A. C. L., Barros, H. D. S., Massara, C. L., Coelho, P. M. Z., & Schall, V. T. (2010) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762010000400037 · Cited by 50 · cited 1× · see citing works
“While schistosomiasis is considered a disease of poverty [1], studies have not always found an association between socio-economic status and schistosomiasis [24,62,99], with the predominant explanation being that an individual’s contact with cercariae-infested water may not be borne out of necessity, but for reasons s…”
Background
Geographical and socioeconomic factors relating to the distribution of Schistosoma mansoni infection in an urban area of north-east Brazil.
Barreto, M. L. (1991) · PubMed · Cited by 48 · see citing works
Schistosoma mansoni, intestinal parasites and perceived morbidity indicators in schoolchildren in a rural endemic area of western Côte d'Ivoire
Utzinger, Utzinger, N'goran, N'goran, Aya, E., Adjoua, A., Lohourignon, Tanner, M., & Lengeler (1998) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.1998.00292.x · Cited by 45 · see citing works
Toward Sustainable and Comprehensive Control of Schistosomiasis in China: Lessons from Sichuan
Seto, E. Y. W., Remais, J. V., Carlton, E. J., Wang, S., Liang, S., Brindley, P. J., Qiu, D., Spear, R. C., Wang, L.-D., Wang, T.-P., et al. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001372 · Cited by 44 · see citing works
Intestinal schistosomiasis among preschool children along the shores of Lake Victoria in Uganda
Nalugwa, A., Olsen, A., Tukahebwa, M. E., & Nuwaha, F. (2014) · Acta Tropica · doi:10.1016/j.actatropica.2014.11.014 · Cited by 44 · see citing works
The performance of school‐based questionnaires of reported blood in urine in diagnosing Schistosoma haematobium infection: patterns by age and sex
Guyatt, H. L., BROOKER, S. J., Lwambo, N. J. S., Siza, J. E., & Bundy, D. A. P. (1999) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.1999.00483.x · Cited by 44 · cited 2× · see citing works
“Reasons hypothesized for this consistent underestimation included anatomical differences, making it more difficult for females to see their urine than males, lower levels of health education, increased reluctance to divulge personal information [105] and menses confounding recognition of symptoms [57].”
Background
Socio-ecological dynamics and challenges to the governance of Neglected Tropical Disease control
Michael, E., & Madon, S. (2017) · Infectious Diseases of Poverty · doi:10.1186/s40249-016-0235-5 · Cited by 44 · see citing works
Socioeconomic determinants of schistosomiasis in an urban area in the Northeast of Brazil
Ximenes, R. A. D. A., Southgate, B., Smith, P. G., & Neto, L. G. (2003) · Revista Panamericana de Salud Pública · doi:10.1590/s1020-49892003001100006 · Cited by 43 · cited 1× · see citing works
“Studies that do report an association generally attribute this finding to lower socioeconomic classes having poorer WASH, health knowledge, healthcare, and access to treatment [19,111]; one would thus expect the measure of socio-economic status to be found insignificant in a multivariable model controlling for these f…”
Background
The epidemiology of schistosomiasis in Egypt: Fayoum Governorate.
Abdel-Wahab, M. F., Esmat, G., Ramzy, I. I., Narooz, S., Medhat, E., Ibrahim, M.-L., El-Boraey, Y., & Strickland, G. T. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.55 · Cited by 43 · see citing works
Association between socio economic status and schistosomiasis infection in Jinja District, Uganda
Muhumuza, S., Kitimbo, G., Oryema-Lalobo, M., & Nuwaha, F. (2009) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2009.02273.x · Cited by 42 · cited 1× · see citing works
“Should wealth index remain an independent predictor, one potential explanation proposed in the literature [112] refers to the poverty-disease cycle ,whereby schistosomiasis is both a cause and an effect of poverty [113].”
Background
Morbidity from Schistosoma Mansoni Infections: an Epidemiologic Study Based on Quantitative Analysis of Egg Excretion in Two Highland Ethiopian Villages
Hiatt, R. A. (1976) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1976.25.808 · Cited by 40 · see citing works
The gender agenda in the control of tropical diseases: A review of current evidence
Allotey, P. A., & Gyapong, M. (2005) · Cited by 40 · see citing works
Morbidity from Schistosoma Mansoni in a Puerto Rican Community: a Population-Based Study
Cline, B. L., Rymzo, W. T., Hiatt, R. A., Knight, W. B., & Berrios-Durán, L. A. (1977) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1977.26.109 · Cited by 39 · see citing works
Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana
Bogoch, I. I., Andrews, J. R., Ephraim, R. K. D., & Utzinger, J. (2012) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2012.03054.x · Cited by 39 · see citing works
The public health significance of urinary schistosomiasis as a cause of morbidity in two districts in Mali.
Traoré, M., Traoré, H. A., Kardorff, R., Diarra, A. S., Landouré, A., Vester, U., Doehring, E., & Bradley, D. J. (1998) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1998.59.407 · Cited by 38 · see citing works
The diagnostic potential of three indirect tests for urinary schistosomiasis in Nigeria
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Modification of behaviour and attitude in the control of schistosomiasis. 1. Observations on water-contact patterns and perception of infection
Useh, M. (1999) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034989957961 · Cited by 37 · see citing works
Schistosoma haematobium infection in Egyptian schoolchildren: demonstration of both hepatic and urinary tract morbidity by ultrasonography
Abdel-Wahab, M. F., Esmat, G., Ramzy, I. I., Fouad, R., Abdel-Rahman, M., Yosery, A., Narooz, S., & Strickland, G. T. (1992) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(92)90241-4 · Cited by 37 · see citing works
Infection with Schistosoma mansoni in the Gezire area of the Sudan.
Omer, A. H. S., Hamilton, P. J. S., Marshall, T. F., & Draper, C. C. (1976) · PubMed · Cited by 37 · see citing works
Simple anamnestic questions and recalled water-contact patterns for self-diagnosis of Schistosoma mansoni infection among schoolchildren in western Côte d'Ivoire.
Utzinger, J., N'Goran, E. K., Tanner, M., & Lengeler, C. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.649 · Cited by 35 · see citing works
Morbidity from Schistosoma mansoni Infections: an Epidemiologic Study Based on Quantitative Analysis of Egg Excretion in Ethiopian Children
Hiatt, R. A., & GEBRE‐MEDHIN, M. (1977) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1977.26.473 · Cited by 35 · see citing works
Adam's rib awry? Women and schistosomiasis
Michelson, E. H. (1993) · Social Science & Medicine · doi:10.1016/0277-9536(93)90284-b · Cited by 34 · see citing works
The epidemiology of schistosomiasis in Egypt: patterns of Schistosoma mansoni infection and morbidity in Kafer El-Sheikh.
Barakat, R., Farghaly, A., Masry, A. G. E., El-Sayed, M. K., & Hussein, M. H. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.21 · Cited by 34 · see citing works
Factors associated with schistosomiasis mansoni in a population from the municipality of Jaboticatubas, State of Minas Gerais, Brazil
Massara, C. L., Peixoto, S. V., Barros, H. D. S., Enk, M. J., Carvalho, O. D. S., & Schall, V. T. (2004) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762004000900023 · Cited by 34 · see citing works
Current status of Schistosoma mansoni and the factors associated with infection two years following mass drug administration programme among primary school children in Mwea irrigation scheme: A cross-sectional study
Masaku, J., Madigu, N., Okoyo, C. O., & Njenga, S. M. (2015) · BMC Public Health · doi:10.1186/s12889-015-1991-z · Cited by 33 · cited 1× · see citing works
“For example, studies evaluating the effects of exclusive MDA control programs have found that while schistosomiasis prevalence may dramatically drop during the control programs, marked rebounding of infection to near or exceeding the baseline prevalence can occur within years of MDA cessation [17,18].”
Background
Schistosomiasis infection among primary school students in a war zone, Southern Kordofan State, Sudan: a cross-sectional study
Abou-Zeid, A., Abkar, T. A., & Mohamed, R. O. (2013) · BMC Public Health · doi:10.1186/1471-2458-13-643 · Cited by 31 · see citing works
The epidemiology of schistosomiasis in Egypt: Qena governorate.
Hammam, H. M., Zarzour, A., Moftah, F. M., Abdel-Aty, M. A., Hany, A. H., El-Kady, A. Y., Nasr, A. M., Abd-El-Samie, A., Qayed, M. H., Mikhail, N. N. H., et al. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.80 · Cited by 31 · see citing works
Combined methods for the study of water contact behavior in a rural schistosomiasis-endemic area in Brazil
Kloos, H., Rodrigues, J. C. A. P., Pereira, W. R., Velásquez-Meléndez, G., LoVerde, P., Corrêa‐Oliveira, R., & Gazzinelli, A. (2005) · Acta Tropica · doi:10.1016/j.actatropica.2005.08.006 · Cited by 30 · see citing works
The epidemiology of schistosomiasis in Egypt: Gharbia Governorate.
El-Hawey, A. M., Amr, M. M., Abdel-Rahman, A. H., Elibiary, S. A., Agina, A. A., Abdel-Hafez, M. A., Waheeb, A. A., Hussein, M. H., & Strickland, G. T. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.42 · Cited by 30 · see citing works
Long term study on the effect of mollusciciding with niclosamide in streamhabitats on the transmission of schistosomiasis mansoni after community-basedchemotherapy in Makueni District, Kenya
Kariuki, H. C., Madsen, H., Ouma, J. H., Butterworth, A. E., Dunne, D. W., Booth, M., Kimani, G. K., Mwatha, J. K., Muchiri, E. M., & Vennervald, B. J. (2013) · Parasites & Vectors · doi:10.1186/1756-3305-6-107 · Cited by 29 · see citing works
The Relationship Between Morbidity and Intensity of Schistosoma mansoni Infection in a Rural Zambian Community
Sukwa, T. Y., Bulsara, M., & Wurapa, F. (1986) · International Journal of Epidemiology · doi:10.1093/ije/15.2.248 · Cited by 28 · see citing works
Access to, and use of, water by populations living in a schistosomiasis and fascioliasis co-endemic area of northern Côte d’Ivoire
Krauth, S. J., Musard, C., Traoré, S. I., Zinsstag, J., Achi, L. Y., N'Goran, E. K., & Utzinger, J. (2015) · Acta Tropica · doi:10.1016/j.actatropica.2015.05.019 · Cited by 28 · cited 1× · see citing works
“In evaluating potential applications of the individual level questionnaire that have been proposed or used in the literature, including targeting of drug treatment, monitoring effects of schistosomiasis control [29], and as an inexpensive and less invasive method for conducting research [97], the low sensitivities are…”
The morbidity of schistosomiasis mansoni in the Rusizi Plain (Burundi)
Gryseels, B. (1988) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(88)90519-6 · Cited by 26 · see citing works
Sensitivity, Specificity and Positive Predictive Value of Selected Clinical Sings and Symptoms Associated with Schistosomiasis Mansoni
Proietti, F. A., & Antunes, C. M. F. (1989) · International Journal of Epidemiology · doi:10.1093/ije/18.3.680 · Cited by 25 · see citing works
glmmLasso: Variable Selection for Generalized Linear Mixed Models by L1-Penalized Estimation
Groll, A. (2011) · doi:10.32614/cran.package.glmmlasso · Cited by 23 · see citing works
Age and gender effects in self‐reported urinary schistosomiasis in Tanzania
Clements, A., Barnett, A. G., Nyandindi, U., Lwambo, N. J. S., Kihamia, C. M., & Blair, L. (2008) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2008.02048.x · Cited by 21 · cited 2× · see citing works
“Reasons hypothesized for this consistent underestimation included anatomical differences, making it more difficult for females to see their urine than males, lower levels of health education, increased reluctance to divulge personal information [105] and menses confounding recognition of symptoms [57].”
Background
The epidemiology of schistosomiasis in Egypt: Ismailia governorate.
Nooman, Z. M., Hasan, A. H., Waheeb, Y., Mishriky, A. M., Ragheb, M., Abu-Saif, A. N., Abaza, S., Serwah, A.-H. A., El-Gohary, A. H., Saad, A., et al. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.35 · Cited by 21 · see citing works
Rapid diagnosis of schistosomiasis in Yemen using a simple questionnaire and urine reagent strips
Bassiouny, H. K., Hasab, A., Nimr, N. A. E., Al-Shibani, L. A., & Al-Waleedi, A. A. (2014) · Eastern Mediterranean Health Journal · doi:10.26719/2014.20.4.242 · Cited by 19 · see citing works
The epidemiology of schistosomiasis in Egypt: Assiut governorate.
Hammam, H. M., Allam, F. A., Moftah, F. M., Abdel-Aty, M. A., Hany, A. H., Abd-El-Motagaly, K. F., Nafeh, M. A., Khalifa, R. M. A., Mikhail, N. N. H., Talaat, M., et al. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.2_suppl.10813503 · Cited by 19 · see citing works
The epidemiology of schistosomiasis in Egypt: Minya Governorate.
Gabr, N. S., Hammad, T. A., Orieby, A., Shawky, E., Khattab, M. A., & Strickland, G. T. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.2_suppl.10813502 · Cited by 19 · see citing works
Schistosomiasis in northern Mozambique
Traquinho, G. A., Quintó, L., Nalá, R., Vaz, R. G., & Corachan, M. (1998) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(98)91011-2 · Cited by 18 · see citing works
Cost-effectiveness of screening methods for urinary schistosomiasis in a school-based control programme in Ibadan, Nigeria
Fatiregun, A. A., Osungbade, K. O., & Olumide, A. E. (2008) · Health Policy · doi:10.1016/j.healthpol.2008.05.004 · Cited by 17 · see citing works
Preparing for national school‐based deworming in Kenya: the validation and large‐scale distribution of school questionnaires with urinary schistosomiasis
Kihara, J. H., Mwandawiro, C. S., Waweru, B., Gitonga, C. W., & BROOKER, S. J. (2011) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2011.02829.x · Cited by 17 · see citing works
The epidemiology of schistosomiasis in Egypt: Menofia Governorate.
Abdel-Wahab, M. F., Esmat, G., Medhat, E., Narooz, S., Ramzy, I. I., El-Boraey, Y., & Strickland, G. T. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.28 · Cited by 17 · see citing works
Evaluation of selected symptoms in the diagnosis of Schistosoma mansoni infection.
Sukwa, T. Y., Mk, B., & Fk, W. (1985) · PubMed · Cited by 17 · see citing works
Hematuria and dysuria in the self-diagnosis of urinary chistosomiasis among school-children in Northern Cameroon
Takougang, I., Meli, J., Fotso, S., Angwafo, F., Kamajeu, R., & Ndumbe, P. M. (2005) · African Journal of Health Sciences · doi:10.4314/ajhs.v11i3.30790 · Cited by 15 · see citing works
Validation of reagent sticks in diagnosing urinary schistosomiasis in an urban setting.
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Diagnostic performance of screening methods for urinary schistosomiasis in a school-based control programme, in Ibadan, Nigeria
Fatiregun, A., Osungbade, K., & Olumide, E. (2005) · Journal of Community Medicine and Primary Health Care · doi:10.4314/jcmphc.v17i1.32421 · Cited by 14 · see citing works
Challenges of accountability in resource-poor contexts: lessons about invited spaces from Karnataka’s village health committees
Madon, S., & Krishna, S. (2017) · Oxford Development Studies · doi:10.1080/13600818.2017.1313397 · Cited by 14 · cited 1× · see citing works
“Recent work on socio-ecological systems and biocomplexity [25,122], ecosystem approaches to health [123], and the notion of ‘invited spaces’, where mechanisms to facilitate community participation in population health decisions are purposefully created [124,125], may serve as possible paradigms and conceptual framewor…”
Background
The epidemiology of schistosomiasis in Egypt: Qalyubia Governorate.
Habib, M., Aziz, F. A., Gamil, F. M., & Cline, B. L. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.49 · Cited by 13 · see citing works
Modification of behaviour and attitude in the control of schistosomiasis. 1. Observations on water-contact patterns and perception of infection
Useh, M., & Gc, E. (1999) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1999.11813476 · Cited by 13 · see citing works
Validity of selected clinical signs and symptoms in diagnosis of Schistosoma mansoni infection
Lima‐Costa, M. F., Rocha, R. S., Colley, D. G., Gazzenelli, G., & Katz, N. (1991) · Revista do Instituto de Medicina Tropical de São Paulo · doi:10.1590/s0036-46651991000100003 · Cited by 12 · see citing works
Two Practical and Cost Effective Methods for Urinary Schistosomiasis Screening in Yemeni Schoolchildren
Ahmed, B. A. (2009) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 9 · see citing works
A clinical epidemiologic study in a schistosomiasis mansoni endemic area (Tuparecê, Minas Gerais)
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Urinary schistosomiasis: options for control within endemic ruralcommunities: a case study in south-west Nigeria
Onayade, A. A., Abayomi, I. O., & Fabiyi, A. K. (1996) · Public Health · doi:10.1016/s0033-3506(96)80107-7 · Cited by 9 · see citing works
Urinary symptoms and blood pressure of children with Schistosoma haematobium infection in south-eastern Nigeria.
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Prevalence of urinary schistosomiasis in school-aged children in Langai, Plateau State: pre- and post-intervention.
Banwat, M., Ogbonna, C., Daboer, J. C., Chingle, M. P., Envuladu, E. A., Audu, S., & Lar, L. (2012) · PubMed · Cited by 6 · see citing works
Effect of skin colour and selected physical characteristics on Schistosoma mansoni dependent morbidity
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Parasitological survey of schistosoma haematobium infection among school children in Mkuranga district, Tanzania
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A Systematic Review of Water and Gender Interlinkages: Assessing the Intersection With Health
Pouramin, P., Nagabhatla, N., & Miletto, M. (2020) · Frontiers in Water · doi:10.3389/frwa.2020.00006 · Cited by 96 · see citing works
Prevalence, Intensity, and Factors Associated with Urogenital Schistosomiasis among Women of Reproductive Age in Mbogwe District Council, Geita Region, Tanzania
Rite, E. E., Ng’weshemi, S. K., & Munisi, D. Z. (2020) · BioMed Research International · doi:10.1155/2020/5923025 · Cited by 20 · see citing works
Schistosomiasis mansoni in families of fishing workers of endemic area of Alagoas
de Melo, A. G. S., Irmão, J. J. D. M., Jeraldo, V. D. L. S., & de Melo, C. M. (2018) · Escola Anna Nery · doi:10.1590/2177-9465-ean-2018-0150 · Cited by 23 · see citing works
Impact of Drinking Water Source and Sanitation Facility on Malnutrition Prevalence in Children under Three: A Gender-Disaggregated Analysis Using PDHS 2017–18
Saheed, R., Shahid, M., Wang, J., Qureshi, M. G., Sun, X., Bibi, A., Zia, S., & Tang, K. (2022) · Children · doi:10.3390/children9111674 · Cited by 18 · see citing works
“borne disease) and stunting because of unimproved water [32,59,60].”
Background
Defining schistosomiasis hotspots based on literature and shareholder interviews
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“Other studies have also shown that persistent schistosomiasis prevalence among school children could be attributed to socioeconomic inequality [9].”
BackgroundResult
Association between Schistosoma mansoni infection and access to improved water and sanitation facilities in Mwea, Kirinyaga County, Kenya
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“Variation in socioeconomic, cultural, and political factors influences the participation in MDA programs in communities [24, 45].”
BackgroundInfluential
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Prevalence, intensity, and associated factors of soil-transmitted helminth and schistosome infections after multiple rounds of preventive chemotherapy among schoolchildren in five selected district councils in Tanzania
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“73 74 This will help eliminate this parasitic disease as a public health problem in endemic countries.”
Knowledge and factors influencing schistosomiasis control interventions in the hyperendemic health district of Kalabancoro in Mali, 2020
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“However, the modes of Schistosomiasis is a parasitic disease caused by trematodes of the genus Schistosoma [1].”
Background
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Exploring community perceptions of gender roles as a predisposing factor in schistosomiasis infection in southwestern Uganda
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Prevalence of Schistosomiasis among Pupils of Umunya Central School, Oyi Local Government, Anambra State, Nigeria
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Persistence of Schistosoma haematobium transmission among school children and its implication for the control of urogenital schistosomiasis in Lindi, Tanzania
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反復治療にもかかわらずタンザニアの学童における持続性住血吸虫症の生物社会学的決定因子【JST・京大機械翻訳】
Rose, E. D., Kijakazi, O. M., Godfrey, M. M., Shirin, M., Mwele, N. M., & Edwin, M. (2017)
Fatores sócio-demográficos e comportamentais relacionados à esquistossomose em uma agrovila da zona canavieira de Pernambuco, Brasil
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Prevalence and factors associated with ongoing transmission of Schistosoma haematobium after 12 rounds of Praziquantel Mass Drug Administration among school age children in Southern Tanzania
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Prevalence, intensity, and associated factors of soil-transmitted helminth and schistosome infections after multiple rounds of preventive chemotherapy among schoolchildren in five selected district councils in Tanzania
Jones, C., Nyati, M. M., Zacharia, A., Mbwambo, S. G., Omary, H., & Ngasala, B. (2025) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0013310 · Cited by 4 · see citing works

Authors: Donohue, R., Mashoto, K., Mubyazi, G., Madon, S., Malecela, M., & Michael, E.
Affiliations: University of Notre Dame (US)
National Institute for Medical Research (TZ)
London School of Economics and Political Science (GB)
Tanzania Commission for Science and Technology (TZ)
Corresponding author: Michael, Edwin
ORCID: Donohue, Rose
Mashoto, Kijakazi
Madon, Shirin
Michael, Edwin
Venue: Tropical Medicine and Infectious Disease
Publisher: MDPI AG
Published: 2017-12-04
Volume: 2
Issue: 4
Pages: 61
ISSN: 2414-6366 (ISSN-L)
DOI: 10.3390/tropicalmed2040061
PMC: PMC6082061
OpenAlex: W2773007662
Cited by: 17
References: 130
Citations by year: 2026: 1 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 1
FWCI: 0.89
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Tropical Medicine and Infectious Disease (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Bill and Melinda Gates Foundation (ID OPP1119126)
Topics: Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
Life Sciences › Agricultural and Biological Sciences › Insect Science › Mollusks and Parasites Studies
Health Sciences › Medicine › Pathology and Forensic Medicine › Parasitic infections in humans and animals
Keywords: schistosomiasis, persistent infection, elementary school students, preventive chemotherapy, water, sanitation and hygiene, socioeconomic status, gender, poverty, schistosomiasis transmission, disease control, Tanzania

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Biosocial determinants of persistent schistosomiasis among schoolchildren in Tanzania despite repeated treatment

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