Cognitive deficits and educational loss in children with schistosome infection-A systematic review and meta-analysis

Ezeamama, Amara E.; Bustinduy, Amaya L.; Nkwata, Allan K.; Martinez, Leonardo; Pabalan, Noel; Boivin, Michael J.; King, Charles H.

doi:10.1371/journal.pntd.0005524

Cited by 149Parasites and Host InteractionsChild Nutrition and Water AccessMollusks and Parasites Studies

Cognitive deficits and educational loss in children with schistosome infection-A systematic review and meta-analysis

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Ezeamama, Amara E., Bustinduy, Amaya L., Nkwata, Allan K., Martinez, Leonardo, Pabalan, Noel, Boivin, Michael J., King, Charles H.·2018·PLoS neglected tropical diseases

DOI 10.1371/journal.pntd.0005524PMC PMC5766129

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Abstract

BACKGROUND: By means of meta-analysis of information from all relevant epidemiologic studies, we examined the hypothesis that Schistosoma infection in school-aged children (SAC) is associated with educational loss and cognitive deficits. METHODOLOGY/PRINCIPAL FINDINGS: This review was prospectively registered in the PROSPERO database (CRD42016040052). Medline, Biosis, and Web of Science were searched for studies published before August 2016 that evaluated associations between Schistosoma infection and cognitive or educational outcomes. Cognitive function was defined in four domains-learning, memory, reaction time, and innate intelligence. Educational outcome measures were defined as attendance and scholastic achievement. Risk of bias (ROB) was evaluated using the Newcastle-Ottawa quality assessment scale. Standardized mean differences (SMD) and 95% confidence intervals (CI) were calculated to compare cognitive and educational measures for Schistosoma infected /not dewormed vs. uninfected/dewormed children. Sensitivity analyses by study design, ROB, and sequential exclusion of individual studies were implemented. Thirty studies from 14 countries, including 38,992 SAC between 5-19 years old, were identified. Compared to uninfected children and children dewormed with praziquantel, the presence of Schistosoma infection and/or non-dewormed status was associated with deficits in school attendance (SMD = -0.36, 95%CI: -0.60, -0.12), scholastic achievement (SMD = -0.58, 95%CI: -0.96, -0.20), learning (SMD = -0.39, 95%CI: -0.70, -0.09) and memory (SMD = -0.28, 95%CI: -0.52, -0.04) tests. By contrast, Schistosoma-infected/non-dewormed and uninfected/dewormed children were similar with respect to performance in tests of reaction time (SMD = -0.06, 95%CI: -0.42, 0.30) and intelligence (SMD = -0.25, 95%CI: -0.57, 0.06). Schistosoma infection-associated deficits in educational measures were robust among observational studies, but not among interventional studies. The significance of infection-associated deficits in scholastic achievement was sensitive to ROB. Schistosoma infection-related deficits in learning and memory tests were invariant by ROB and study design. CONCLUSION/SIGNIFICANCE: Schistosoma infection/non-treatment was significantly associated with educational, learning, and memory deficits in SAC. Early treatment of children in Schistosoma-endemic regions could potentially mitigate these deficits. TRIAL REGISTRATION: ClinicalTrials.gov CRD42016040052.

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Detrimental effects of helminth infections (both STH and schistosomes) have been previously reported.
“Whilst the detrimental effects of helminth infections (both STH [4] and schistosomes [7]) have been previously reported”
From Assessing early child development and its association with stunting and schistosome infections in rural Zimbabwean children using the Griffiths Scales of Child Development (2021) · cites this paper as [7]
Meta-analysis has indicated that schistosome infections were significantly associated with educational, learning, and memory deficits in school-aged children.
“while meta-analysis has indicated that schistosome infections were significantly associated with educational, learning, and memory deficits in school-aged children [7].”
From Assessing early child development and its association with stunting and schistosome infections in rural Zimbabwean children using the Griffiths Scales of Child Development (2021) · cites this paper as [7]

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Nalugwa, A., Nuwaha, F., Tukahebwa, E. M., & Olsen, A. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003796 · Cited by 34 · cited 3× · see citing works
“However, Schistosoma-infected pre-school children are not routinely treated in such settings, and they constitute a potentially high risk group for accumulation of morbidity [9].”
BackgroundInfluential
New Antipoverty Drugs, Vaccines, and Diagnostics: A Research Agenda for the US President's Global Health Initiative (GHI)
Hotez, P. J. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001133 · Cited by 34 · cited 3× · see citing works
“Recent reviews of MDA effects have, thus far, focused on the impact of soil-transmitted helminth infections (STH), but health policy discussions–including those at the World Health Organization [30, 31], have tended to generalize findings to all helminths.”
Background
The relationship between Schistosoma haematobium infection and school performance and attendance in Bamako, Mali
CLERCQ, D. D. (1998) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034989858899 · Cited by 30 · see citing works
School-based schistosomiasis control programmes: a comparative study on the prevalence and intensity of urinary schistosomiasis among nigerian school-age children in and out of school
Useh, M., & Gc, E. (1999) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(99)90127-x · Cited by 29 · see citing works
Baseline prevalence and intensity of schistosomiasis at sentinel sites in Madagascar: Informing a national control strategy
Rasoamanamihaja, C. F., Rahetilahy, A. M., Ranjatoarivony, B., Dhanani, N., Andriamaro, L., Andrianarisoa, S. H., & Jourdan, P. M. (2016) · Parasites & Vectors · doi:10.1186/s13071-016-1337-4 · Cited by 29 · see citing works
The effects of Schistosomiasis haematobium on the activity of school children.
Jd, K. (1986) · PubMed · Cited by 28 · see citing works
Schistosoma haematobium in Ajara community of Badagry, Nigeria. A study on prevalence, intensity and morbidity from infection among primary school children.
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Bilharziasis in Tanganyika: Observations on its Effects and the Effects of Treatment in Schoolchildren.
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Effects of Schistosoma haematobium infection on mental test scores of Kenyan school children.
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Schistosomiasis mansoni in school attenders and non-attenders in Northwest Ethiopia
Tiruneh, M., Fantahun, M., Kassu, A., Tiruneh, G., van Lieshout, L., & Polderman, A. M. (2001) · Ethiopian Journal of Health Development · doi:10.4314/ejhd.v15i2.9885 · Cited by 18 · see citing works
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Ekanem, E. E., Asindi, A. A., Gc, E., & Antia-Obong, O. E. (1994) · PubMed · Cited by 15 · see citing works
Schistosoma mansoni infection and cognitive functions of primary school children, in Kafr El Sheikh, Egypt.
Abu-Nazel, M. W., Elmorshedy, H., Farghaly, A., Shatat, H. Z., & Barakat, R. (1999) · PubMed · Cited by 15 · see citing works
Gastro-intestinal symptoms associated with intense Schistosoma mansoni infection affect class-attentiveness of schoolchildren in Ethiopia
Berhe, N. B., Myrvang, B., & Gundersen, S. G. (2009) · Acta Tropica · doi:10.1016/j.actatropica.2009.01.007 · Cited by 12 · see citing works
School non-enrollment and its relation with health and schistosomiasis knowledge, attitudes and practices in rural Egypt.
Mekheimar, S. I., & Talaat, M. (2005) · PubMed · Cited by 12 · see citing works
The relationship between Schistosoma haematobium infection and school performance and attendance in Bamako, Mali
de Clercq, D., Sacko, M., Behnke, J. M., Gilbert, F. S., & Vercruysse, J. (1998) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1998.11813350 · Cited by 12 · see citing works
Schistosomiasis; the effect of the disease on educational attainment.
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The effects of subclinical bilharziasis on mental ability in schoolchildren.
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Treatment of schistosomiasis haematobium with praziquantel in children: its effect on educational performance in rural Nigeria.
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Schistosomiasis in rural Zambia
Goldin, D., & Barclay, R. (1972) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1972.11686816 · Cited by 4 · see citing works
Parasitic Disease and Academic Performance of School Children
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Sorted by citations

Errors in search strategies used in systematic reviews and their effects on information retrieval
Salvador-Oliván, J. A., Marco-Cuenca, G., & Arquero-Avilés, R. (2019) · Journal of the Medical Library Association · doi:10.5195/jmla.2019.567 · Cited by 199 · see citing works
Schistosomiasis Morbidity Hotspots: Roles of the Human Host, the Parasite and Their Interface in the Development of Severe Morbidity
Mawa, P. A., Kincaid-Smith, J., Tukahebwa, E. M., Webster, J. P., & Wilson, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.635869 · Cited by 126 · see citing works
“In children, continued inflammation has been reported to impede, amongst other pathologies, iron metabolism, with consequent disabling systemic morbidities including anemia, malnutrition, physical fitness and impaired physical and cognitive development (9, 10).”
Background
The prevalence of schistosomiasis in Uganda: A nationally representative population estimate to inform control programs and water and sanitation interventions
Exum, N. G., Kibira, S. P. S., Ssenyonga, R., Nobili, J., Shannon, A. K., Ssempebwa, J. C., Tukahebwa, E. M., Radloff, S. R., Schwab, K. J., & Makumbi, F. E. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007617 · Cited by 95 · see citing works
Immune Evasion Strategies of Schistosomes
Hambrook, J. R., & Hanington, P. C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.624178 · Cited by 84 · see citing works
Translating preventive chemotherapy prevalence thresholds for Schistosoma mansoni from the Kato-Katz technique into the point-of-care circulating cathodic antigen diagnostic test
Bärenbold, O., Garba, A., Colley, D. G., Fleming, F. M., Haggag, A. A., Ramzy, R. M. R., Assaré, R. K., Tukahebwa, E. M., Mbonigaba, J. B., Bucumi, V., et al. (2018) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0006941 · Cited by 74 · see citing works
The economic impact of schistosomiasis
Rinaldo, D., Perez‐Saez, J., Vounatsou, P., Utzinger, J., & Arcand, J. (2021) · Infectious Diseases of Poverty · doi:10.1186/s40249-021-00919-z · Cited by 70 · see citing works
“The highest parasite burden is usually borne by school-age children and the disease has been linked to anemia, stunting and cognitive deficits, leading to poor school performance and higher drop-out rates [7].”
Background
Defining elimination as a public health problem for schistosomiasis control programmes: beyond prevalence of heavy-intensity infections
Wiegand, R. E., Fleming, F. M., de Vlas, S. J., Odiere, M. R., Kinung’hi, S., King, C. H., Evans, D. S., French, M. D., Montgomery, S. P., Straily, A., et al. (2022) · The Lancet Global Health · doi:10.1016/s2214-109x(22)00287-x · Cited by 66 · see citing works
Underestimation of the global burden of schistosomiasis
King, C. H., & Galvani, A. P. (2018) · The Lancet · doi:10.1016/s0140-6736(18)30098-9 · Cited by 66 · see citing works
Prevalence and risk factors of schistosomiasis and soil-transmitted helminthiases among preschool aged children (1–5 years) in rural KwaZulu-Natal, South Africa: a cross-sectional study
Sacolo-Gwebu, H., Chimbari, M. J., & Kalinda, C. (2019) · Infectious Diseases of Poverty · doi:10.1186/s40249-019-0561-5 · Cited by 65 · see citing works
Advancing the Development of a Human Schistosomiasis Vaccine
Hotez, P. J., Bottazzi, M. E., Bethony, J. M., & Diemert, D. J. (2018) · Trends in Parasitology · doi:10.1016/j.pt.2018.10.005 · Cited by 63 · see citing works
Malaria and helminth co-infections in children living in endemic countries: A systematic review with meta-analysis
Afolabi, M. O., Ale, B. M., Dabira, E. D., Agbla, S. C., Bustinduy, A. L., Ndiaye, J. L., & Greenwood, B. M. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009138 · Cited by 60 · see citing works
Lactate dehydrogenase and malate dehydrogenase: Potential antiparasitic targets for drug development studies
Kayamba, F., Faya, M. A., Pooe, O. J., Kushwaha, B., Kushwaha, N. D., Obakachi, V. A., Nyamori, V. O., & Karpoormath, R. V. (2021) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2021.116458 · Cited by 46 · see citing works
Intestinal Helminth Infection, Anemia, Undernutrition and Academic Performance among School Children in Northwestern Ethiopia
Degarege, A., Erko, B., Negash, Y., & Animut, A. (2022) · Microorganisms · doi:10.3390/microorganisms10071353 · Cited by 46 · see citing works
“A meta-analysis of 15 studies also reported lower scholastic achievement/academic scores among children infected with Schistosoma and/or those not dewormed with praziquantel compared to uninfected ones [15].”
Background
Neglected tropical diseases and disability—what is the link?
Kuper, H. (2019) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1093/trstmh/trz001 · Cited by 46 · see citing works
Effects of water, sanitation and hygiene (WASH) education on childhood intestinal parasitic infections in rural Dembiya, northwest Ethiopia: an uncontrolled before-and-after intervention study
Gizaw, Z., Addisu, A., & Dagne, H. (2019) · Environmental Health and Preventive Medicine · doi:10.1186/s12199-019-0774-z · Cited by 47 · see citing works
Prevalence of Stunting and Relationship between Stunting and Associated Risk Factors with Academic Achievement and Cognitive Function: A Cross-Sectional Study with South African Primary School Children
Beckmann, J., Lang, C., du Randt, R., Gresse, A., Long, K. Z., Ludyga, S., Müller, I., Nqweniso, S., Pühse, U., Utzinger, J., et al. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18084218 · Cited by 52 · see citing works
“School-aged children who are stunted and those infected with soil-transmitted helminths (STHs) are at increased risk of presenting higher school absenteeism and dropout rates, and of underperforming academically [15,16] compared to well-nourished and non-infected peers.”
Background
Prevalence of urogenital and intestinal schistosomiasis among school children in South-west Nigeria
Ojo, J. A., Adedokun, S. A., Akindele, A. A., Olorunfemi, A. B., Otutu, O. A., Ojurongbe, T. A., Thomas, B. N., Velavan, T. P., & Ojurongbe, O. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009628 · Cited by 39 · see citing works
“The impaired physical and cognitive development arising from chronic infection among children is a major concern in many parts of the world [11].”
Background
Prevalence, Intensity, and Correlates of Schistosomiasis and Soil-Transmitted Helminth Infections after Five Rounds of Preventive Chemotherapy among School Children in Southern Ethiopia
Gebreyesus, T. D., Tadele, T., Mekete, K., Barry, A., Gashaw, H., Degefe, W., Tadesse, B. T., Gerba, H., Parthasarathi, G., Makonnen, E., et al. (2020) · Pathogens · doi:10.3390/pathogens9110920 · Cited by 38 · see citing works
“These morbidities result in poor school attendance, poor concentration in class, and poor academic performance, which can negatively affect the quality of life of children, impacting their future growth and development [10,11,25,26].”
Background
Assessing the Burden of Neglected Tropical Diseases in Low-Income Communities: Challenges and Solutions
Branda, F., Ali, A. Y., Ceccarelli, G., Albanese, M., Binetti, E., Giovanetti, M., Ciccozzi, M., & Scarpa, F. (2024) · Viruses · doi:10.3390/v17010029 · Cited by 35 · see citing works
A meta-analysis of changes in schistosomiasis prevalence in Zambia: implications on the 2020 elimination target
Kalinda, C., Mutengo, M. M., & Chimbari, M. J. (2019) · Parasitology Research · doi:10.1007/s00436-019-06534-0 · Cited by 32 · see citing works
SCORE Studies on the Impact of Drug Treatment on Morbidity due to Schistosoma mansoni and Schistosoma haematobium Infection
King, C. H., Binder, S., Shen, Y., Whalen, C. C., Campbell, C. H., Wiegand, R. E., Olsen, A., Secor, W. E., Montgomery, S. P., Musuva, R., et al. (2020) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.19-0830 · Cited by 32 · see citing works
Self-citation
Spirorchiidiasis in marine turtles: the current state of knowledge
Chapman, P. A., Cribb, T. H., Flint, M., Traub, R. J., Blair, D., Kyaw-Tanner, M. T., & Mills, P. C. (2019) · Diseases of Aquatic Organisms · doi:10.3354/dao03348 · Cited by 31 · see citing works
A systematic review and meta-analysis quantifying schistosomiasis infection burden in pre-school aged children (PreSAC) in sub-Saharan Africa for the period 2000–2020
Kalinda, C., Mindu, T., & Chimbari, M. J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0244695 · Cited by 30 · see citing works
Helminthiasis Epidemiology and Control
King, C. H. (2018) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2018.08.001 · Cited by 29 · see citing works
Environmental Predictors of Schistosomiasis Persistent Hotspots following Mass Treatment with Praziquantel
Walker, J. W., Kittur, N. D., Binder, S., Castleman, J. D., Drake, J. M., Campbell, C. H., King, C. H., & Colley, D. G. (2019) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.19-0658 · Cited by 29 · see citing works
Zoonotic transmission of intestinal helminths in southeast Asia: Implications for control and elimination.
Betson, M., Alonte, A. I., Ancog, R., Aquino, A. M. O., Belizario, V., Bordado, A. M., Clark, J., Corales, M. C. G., Dacuma, M. G., Divina, B. P., et al. (2020) · Advances in Parasitology · doi:10.1016/bs.apar.2020.01.036 · Cited by 23 · see citing works
A Rapid Appraisal of Factors Influencing Praziquantel Treatment Compliance in Two Communities Endemic for Schistosomiasis in Côte d’Ivoire
Coulibaly, J. T., Ouattara, M., Barda, B., Utzinger, J., N'Goran, E. K., & Keiser, J. (2018) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed3020069 · Cited by 28 · see citing works
“There is growing evidence of a positive relationship between schistosome infections and subtle morbidity, including educational, learning and memory deficits [5].”
Background
Negative Association of Interleukin-33 Plasma Levels and Schistosomiasis Infection in a Site of Polyparasitism in Rural Cameroon
Kamdem, S. D., Konhawa, F., Kuemkon, E. M., Kamguia, L. M., Tchanana, G. K., Nche, F., Oumarou, A., Hamza, M., Ouratou, Y., Tcheutchoua, M. N., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02827 · Cited by 25 · see citing works
“Morbidity has been evaluated by hematological assays (for anemia), intellectual performance (for cognitive impairment) (43) and ultrasonography (for tissue destruction) (37).”
Background
NLRP3 inflammasome of microglia promotes A1 astrocyte transformation, neo-neuron decline and cognition impairment in endotoxemia
Xiao, T., Ji, H., Shangguan, X., Qu, S., Cui, Y., & Xu, J. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.02.092 · Cited by 26 · see citing works
Assessing early child development and its association with stunting and schistosome infections in rural Zimbabwean children using the Griffiths Scales of Child Development
Mutapi, F., Pfavayi, L., Osakunor, D., Lim, R., Kasambala, M., Mutemeri, A., Rusakaniko, S., Chibanda, D., & Mduluza, T. (2021) · PLOS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0009660 · Cited by 25 · see citing works
“Whilst the detrimental effects of helminth infections (both STH [4] and schistosomes [7]) have been previously reported, to date there has been no study investigating the impact of schistosome infection on ECD focusing on children aged 5 years and below.”
Background
The Genetics of Human Schistosomiasis Infection Intensity and Liver Disease: A Review
Mewamba, E. M., Nyangiri, O. A., Noyes, H. A., Egesa, M., Matovu, E., & Simo, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.613468 · Cited by 24 · see citing works
The Ubiquity of Cognitive Impairment in Human Illness: a Systematic Review of Meta-Analyses
Schretlen, D. J., Finley, J. A., Bene, V. A. D., & Varvaris, M. (2024) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acae113 · Cited by 22 · see citing works
Resolving "worm wars": An extended comparison review of findings from key economics and epidemiological studies
Majid, M. F., Kang, S. J., & Hotez, P. J. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0006940 · Cited by 23 · see citing works
A review on innovative optical devices for the diagnosis of human soil-transmitted helminthiasis and schistosomiasis: from research and development to commercialization
Meulah, B., Bengtson, M., van Lieshout, L., Hokke, C. H., Kreidenweiss, A., Diehl, J. C., Adégnika, A. A., & Agbana, T. (2022) · Parasitology · doi:10.1017/s0031182022001664 · Cited by 21 · see citing works
“These helminth infections have a considerable public health impact when left untreated with opposing effects on both physical and cognitive development in children and adolescents (Ezeamama et al., 2018; Pabalan et al., 2018).”
Evidence of reduced academic performance among schoolchildren with helminth infection
Donkoh, E. T., Berkoh, D., Gyasi, S. F., Boadu, W. I. O., Raji, A. S., Asamoah, S., Otabil, K. B., Otoo, J. E., Yeboah, M. T., Aganbire, B. A., et al. (2022) · International Health · doi:10.1093/inthealth/ihac044 · Cited by 19 · see citing works
Five-Year Impact of Different Multi-Year Mass Drug Administration Strategies on Childhood Schistosoma mansoni–Associated Morbidity: A Combined Analysis from the Schistosomiasis Consortium for Operational Research and Evaluation Cohort Studies in the Lake Victoria Regions of Kenya and Tanzania
Shen, Y., Wiegand, R. E., Olsen, A., King, C. H., Kittur, N. D., Binder, S., Zhang, F., Whalen, C. C., Secor, W. E., Montgomery, S. P., et al. (2019) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.19-0273 · Cited by 19 · see citing works
Efficacy and safety of praziquantel preventive chemotherapy in Schistosoma mansoni infected school children in Southern Ethiopia: A prospective cohort study
Gebreyesus, T. D., Makonnen, E., Tadele, T., Mekete, K., Gashaw, H., Gerba, H., & Aklillu, E. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.968106 · Cited by 18 · see citing works
“Schistosomiasis mainly affects children, and its chronic infection can lead to various health complications, including anemia, malnutrition, impaired childhood development, poor cognitive function, fatigue, and exercise intolerance (King and Dangerfield-Cha, 2008; Ezeamama et al., 2018).”
Background
A comprehensive exploration of schistosomiasis: Global impact, molecular characterization, drug discovery, artificial intelligence and future prospects
Ekloh, W., Asafu-Adjaye, A., Tawiah‐Mensah, C. N. L., Ayivi-Tosuh, S. M., Quartey, N. K.-A., Aiduenu, A. F., Gayi, B. K., Koudonu, J. A. M., Basing, L. A., Yamoah, J. A. A., et al. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e33070 · Cited by 18 · see citing works
“In Zimbabwe, high prevalence rates lead to reduced educational attainment, hindering human capital development and limiting long-term economic opportunities [68].”
Background
Economic evaluations of human schistosomiasis interventions: a systematic review and identification of associated research needs
Turner, H. C., French, M. D., Montresor, A., King, C. H., Rollinson, D., & Toor, J. (2020) · Wellcome Open Research · doi:10.12688/wellcomeopenres.15754.2 · Cited by 28 · see citing works
The praziquantel in preschoolers (PIP) trial: study protocol for a phase II PK/PD-driven randomised controlled trial of praziquantel in children under 4 years of age
Webb, E. L., Edielu, A., Wu, H. W., Kabatereine, N. B., Tukahebwa, E. M., Mubangizi, A., Adriko, M., Elliott, A. M., Hope, W. W., Mawa, P. A., et al. (2021) · Trials · doi:10.1186/s13063-021-05558-1 · Cited by 18 · see citing works
Intestinal schistosomiasis among schoolchildren in Sana’a Governorate, Yemen: Prevalence, associated factors and its effect on nutritional status and anemia
Al-Haidari, S. A., Mahdy, M. A. K., Al-Mekhlafi, A. M., Al-Murisi, W. M. S., Thabit, A. A. Q., Amad, M. A. A., Al-Shamahy, H. A., Bahashwan, O. S., & Serouri, A. A. A. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009757 · Cited by 18 · see citing works
Effect of Schistosoma haematobium infection on the cognitive functions of preschool age children and benefits of treatment from an endemic area in Zimbabwe
Kasambala, M., Mduluza, T., Vengesai, A., Mduluza-Jokonya, T. L., Jokonya, L., Midzi, H., Makota, R. B., Mutemeri, A., Maziti, E., Dube-Marimbe, B., et al. (2022) · BMC Infectious Diseases · doi:10.1186/s12879-022-07784-7 · Cited by 17 · see citing works
“A meta-analysis conducted in 2018 reported on the negative associations of schistosomiasis and cognitive deficits in school aged going children, particularly in the educational, learning and memory domain [8].”
Method
Neurological impairment caused by Schistosoma mansoni systemic infection exhibits early features of idiopathic neurodegenerative disease
Gasparotto, J., Senger, M. R., Moreira, E. T. D. S., Brum, P. O., Kessler, F. G. C., Peixoto, D. O., Panzenhagen, A. C., Ong, L. K., Soares, M. C., Reis, P. A., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100979 · Cited by 16 · see citing works
“adults (9, 10), and thus the present model may serve as a parallel for such context.”
Background
Impact of a Novel, Low-Cost and Sustainable Health Education Program on the Knowledge, Attitudes, and Practices Related to Intestinal Schistosomiasis in School Children in a Hard-to-Reach District of Madagascar
Spencer, S. A., Andriamasy, H. E., Linder, C., Penney, J. M. S., Henstridge-Blows, J., Russell, H. J., Hyde, K., Sheehy, C., Young, I. L., Sjoflot, B., et al. (2022) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.21-0220 · Cited by 16 · see citing works
“4 million disabilityadjusted life years lost each year.(10,11) Schistosoma mansoni infection causes intestinal schistosomiasis, which can lead to anemia, stunting, wasting, reduced exercise performance, and potentially fatal conditions such as liver fibrosis.”
Evaluation of a Physical Activity and Multi-Micronutrient Intervention on Cognitive and Academic Performance in South African Primary Schoolchildren
Beckmann, J., Nqweniso, S., Ludyga, S., du Randt, R., Gresse, A., Long, K. Z., Nienaber, M., Seelig, H., Pühse, U., Steinmann, P., et al. (2022) · Nutrients · doi:10.3390/nu14132609 · Cited by 17 · see citing works
“Children from low- and middle-income countries (LMICs) are especially at risk of food insecurity [6,7], multiple micronutrient deficiencies [8], malnutrition (including both overnutrition/obesity and undernutrition/stunting), as well as diseases such as soil-transmitted helminthic infections [9,10], which are linked t…”
Background
Tungiasis among children in Kenya is associated with poor nutrition status, absenteeism, poor school performance and high impact on quality of life
Elson, L. H., Kamau, C., Koech, S., Muthama, C., Gachomba, G., Sinoti, E., Chondo, E., Mburu, E., Wakio, M., Lore, J., et al. (2024) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0011800 · Cited by 16 · see citing works
Protocol and baseline data for a multi-year cohort study of the effects of different mass drug treatment approaches on functional morbidities from schistosomiasis in four African countries
Shen, Y., King, C. H., Binder, S., Zhang, F., Whalen, C. C., Secor, W. E., Montgomery, S. P., Mwinzi, P. N. M., Olsen, A., Magnussen, P., et al. (2017) · BMC Infectious Diseases · doi:10.1186/s12879-017-2738-5 · Cited by 16 · see citing works
Change in children’s school behavior after mass administration of praziquantel for Schistosoma mansoni infection in endemic areas of western Kenya: A pilot study using the Behavioral Assessment System for Children (BASC-2)
Musuva, R., Shen, Y., Wei, X., Binder, S., Ivy, J. A., Secor, W. E., Montgomery, S. P., King, C. H., & Mwinzi, P. N. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181975 · Cited by 16 · see citing works
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Background
Optimisation of the DNA dipstick as a rapid extraction method for Schistosoma japonicum in infected mice samples and spiked human clinical samples
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Background
Performance of Urine Reagent Strips in Detecting the Presence and Estimating the Prevalence and Intensity of Schistosoma haematobium Infection
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Background
Neurocognitive and mental health outcomes in children with tungiasis: a cross-sectional study in rural Kenya and Uganda
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Background
Baseline Liver Ultrasound Findings in Preschool Children From the Praziquantel in Preschoolers Trial in Lake Albert, Uganda
Pach, S., Webb, E. L., Edielu, A., Nagawa, R., Anguajibi, V., Mpooya, S., Wu, H. W., Colt, S., Mawa, P. A., Richter, J., et al. (2023) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000004119 · Cited by 10 · see citing works
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Agricultural Innovations to Reduce the Health Impacts of Dams
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Five-Year Follow-Up on the Prevalence and Intensity of Infections of Schistosoma mansoni in a Hard-to-Reach District of Madagascar
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BackgroundResultInfluential
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Background
Serum ferritin as a candidate diagnostic biomarker of polycystic ovarian syndrome: a meta-analysis
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Background
Schistosoma Infection Burden and Risk Factors among School-Aged Children in a Rural Area of the Democratic Republic of the Congo
Linsuke, S., Ilombe, G., Disonama, M., Nzita, J. D., Kingebeni, P. M., Lutumba, P. T., & Geertruyden, J. V. (2023) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed8090455 · Cited by 5 · see citing works
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Safety Surveillance of Mass Praziquantel and Albendazole Co-Administration in School Children from Southern Ethiopia: An Active Cohort Event Monitoring
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Authors: Ezeamama, A. E., Bustinduy, A. L., Nkwata, A. K., Martinez, L., Pabalan, N., Boivin, M. J., & King, C. H.
Affiliations: University of Georgia (US)
London School of Hygiene & Tropical Medicine (GB)
Angeles University Foundation (PH)
Michigan State University (US)
Case Western Reserve University (US)
Corresponding author: Ezeamama, Amara E.
ORCID: Ezeamama, Amara E.
Bustinduy, Amaya L.
Nkwata, Allan K.
Pabalan, Noel
Boivin, Michael J.
King, Charles H.
Venue: PLoS neglected tropical diseases
Publisher: Public Library of Science (PLoS)
Published: 2018-01-12
Volume: 12
Issue: 1
Pages: e0005524
ISSN: 1935-2727 (ISSN-L)
1935-2735
DOI: 10.1371/journal.pntd.0005524
PMC: PMC5766129
OpenAlex: W2783986784
Cited by: 149
References: 77
Citations by year: 2026: 19 · 2025: 13 · 2024: 15 · 2023: 16 · 2022: 20 · 2021: 27 · 2020: 15 · 2019: 15 · 2018: 7 · 2017: 2
FWCI: 2.72
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: PLoS neglected tropical diseases (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Figshare (submittedVersion, cc-by)
Funders: Schistosomiasis Consortium for Operational Research and Evaluation (SCORE).
Topics: Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
Health Sciences › Nursing › Nutrition and Dietetics › Child Nutrition and Water Access
Life Sciences › Agricultural and Biological Sciences › Insect Science › Mollusks and Parasites Studies
Keywords: schistosomiasis, cognitive impairment, educational losses, school attendance, academic performance, praziquantel, anthelmintic treatment, school-aged children, learning, memory, reaction time, intelligence, intellectual disability, neuropsychological outcomes, neglected tropical diseases, neuroschistosomiasis, risk of bias
MeSH terms: Memory and Learning Tests, Adolescent, Animals, Anthelmintics, Child, Child, Preschool, Cognition, Humans, Intelligence, Learning Disabilities, Memory, Memory Disorders, Praziquantel, Reaction Time, Schistosoma, Schistosomiasis, Cognitive Dysfunction

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Cognitive deficits and educational loss in children with schistosome infection-A systematic review and meta-analysis

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