Infection
Co-infection of Plasmodium falciparum and Schistosoma mansoni is associated with anaemia
Sep
WHO. World malaria report 2022. Geneva: World Health Organization; 2022.
Mawa PA, Kincaid-Smith J, Tukahebwa EM, Webster JP, Wilson S. Schistosomiasis morbidity hotspots: roles of the human host, the parasite and their interface in the development of severe morbidity. Front Immunol. 2021;12: 635869.
Google Scholar
LoVerde PT. Schistosomiasis. Adv Exp Med Biol. 2019;1154:45–70.
Google Scholar
WHO. Schistosomiasis (Bilharzia). Geneva: World Health Organization; 2022.
Kamau E, Yates A, Maisiba R, Singoei V, Opot B, Adeny R, et al. Epidemiological and clinical implications of asymptomatic malaria and schistosomiasis co-infections in a rural community in western Kenya. BMC Infect Dis. 2021;21:937.
Google Scholar
Kinung’hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ. Malaria and helminth co-infections in school and preschool children: a cross-sectional study in Magu district, north-western Tanzania. PLoS ONE. 2014;9:86510.
Rinaldo D, Perez-Saez J, Vounatsou P, Utzinger J, Arcand JL. The economic impact of schistosomiasis. Infect Dis Poverty. 2021;10:134.
Google Scholar
Ismail N, Jimam NS, Goh KW, Tan CS, Ming LC. Economic burdens of uncomplicated malaria in primary health care (PHC) facilities of Plateau State, Nigeria: patients’ perspectives. Int J Environ Res Public Health. 2023;20:1093.
Google Scholar
Dassah S, Asiamah GK, Harun V, Appiah-Kubi K, Oduro A, Asoala V, et al. Urogenital schistosomiasis transmission, malaria and anemia among school-age children in Northern Ghana. Heliyon. 2022;8: e10440.
Google Scholar
Duah E, Kenu E, Adela EM, Halm HA, Agoni C, Kumi RO. Article Assessment of urogenital schistosomiasis among basic school children in selected communities along major rivers in the central region of Ghana. Pan Afr Med J. 2021;40:96.
Google Scholar
Mensah BA, Myers-Hansen JL, Obeng Amoako E, Opoku M, Abuaku BK, Ghansah A. Prevalence and risk factors associated with asymptomatic malaria among school children: repeated cross-sectional surveys of school children in two ecological zones in Ghana. BMC Public Health. 2021;21:1697.
Google Scholar
Kulinkina AV, Walz Y, Koch M, Biritwum NK, Utzinger J, Naumova EN. Improving spatial prediction of Schistosoma haematobium prevalence in southern Ghana through new remote sensors and local water access profiles. PLoS Negl Trop Dis. 2018;12: e0006517.
Google Scholar
Dassah S, Adu B, Sirima SB, Mordmüller B, Ngoa UA, Atuguba F, et al. Extended follow-up of children in a phase2b trial of the GMZ2 malaria vaccine. Vaccine. 2021;39:4314–9.
Google Scholar
Osarfo J, Ampofo GD, Tagbor H. Trends of malaria infection in pregnancy in Ghana over the past two decades: a review. Malar J. 2022;21:3.
Google Scholar
Lai YS, Biedermann P, Ekpo UF, Garba A, Mathieu E, Midzi N, et al. Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. Lancet Infect Dis. 2015;15:927–40.
Google Scholar
Anto F, Asoala V, Adjuik M, Anyorigiya T, Oduro A, Akazili J, et al. Childhood Activities and Schistosomiasis Infection in the Kassena-Nankana District of Northern Ghana. J Infect Dis Ther. 2014;2:4.
Mazigo HD, Waihenya R, Lwambo NJS, Mnyone LL, Mahande AM, Seni J, et al. Co-infections with Plasmodium falciparum, Schistosoma mansoni and intestinal helminths among schoolchildren in endemic areas of Northwestern Tanzania. Parasit Vectors. 2010;3:44.
Google Scholar
Sumbele IUN, Otia OV, Francis L, Bopda OSM, Ebai CB, Ning TR, et al. Confounding influences of malnutrition and Plasmodium falciparum and Schistosoma haematobium infections on haematological parameters in school children in Muyuka, Cameroon. BMC Infect Dis. 2021;21:477.
Google Scholar
Kinung’hi SM, Mazigo HD, Dunne DW, Kepha S, Kaatano G, Kishamawe C, et al. Coinfection of intestinal schistosomiasis and malaria and association with haemoglobin levels and nutritional status in school children in Mara region, Northwestern Tanzania: a cross-sectional exploratory study. BMC Res Notes. 2017;10:583.
Google Scholar
Matangila JR, Doua JY, Linsuke S, Madinga J, Inocêncio Da Luz R, Van Geertruyden JP, et al. Malaria, schistosomiasis and soil transmitted helminth burden and their correlation with anemia in children attending primary schools in kinshasa, democratic republic of congo. PLoS One. 2014;9: e110789.
Google Scholar
Safiri S, Kolahi AA, Noori M, Nejadghaderi SA, Karamzad N, Bragazzi NL, et al. Burden of anemia and its underlying causes in 204 countries and territories, 1990–2019: results from the Global Burden of Disease Study 2019. J Hematol Oncol. 2021;14:185.
Google Scholar
Gardner W, Kassebaum N. Global, regional, and national prevalence of anemia and its causes in 204 countries and territories, 1990–2019. Curr Dev Nutr. 2020;4(2):830.
Google Scholar
Moschovis PP, Wiens MO, Arlington L, Antsygina O, Hayden D, Dzik W, et al. Individual, maternal and household risk factors for anaemia among young children in sub-Saharan Africa: a cross-sectional study. BMJ Open. 2018;8: e019654.
Google Scholar
Scott SP, Chen-Edinboro LP, Caulfield LE, Murray-Kolb LE. The impact of anemia on child mortality: an updated review. Nutrients. 2014;6:5915–32.
Google Scholar
Hurtado EK, Claussen AH, Scott KG. Early childhood anemia and mild or moderate mental retardation. Am J Clin Nutr. 1999;69:115–9.
Google Scholar
Ai Y, Zhao SR, Zhou G, Ma X, Liu J. Hemoglobin status associated with performance IQ but not verbal IQ in Chinese preschool children. Pediatr Int. 2012;54:669–75.
Google Scholar
Tsai KZ, Lai SW, Hsieh CJ, Lin CS, Lin YP, Tsai SC, et al. Association between mild anemia and physical fitness in a military male cohort: the CHIEF study. Sci Rep. 2019;9:11165.
Google Scholar
Adekanmbi AF, Ogunlesi TA, Olowu AO, Fetuga MB. Current trends in the prevalence and aetiology of childhood congestive cardiac failure in Sagamu. J Trop Pediatr. 2007;53:103–6.
Google Scholar
Gasim GI, Adam I. Malaria, schistosomiasis, and related anemia. In: Erkekoglu P, Kocer-Gumusel B, editors. Nutritional deficiency. London: IntechOpen; 2016.
Perkins DJ, Were T, Davenport GC, Kempaiah P, Hittner JB, Ong’echa JM. Severe malarial anemia: innate immunity and pathogenesis. Int J Biol Sci. 2011;7:1427–42.
Google Scholar
Haldar K, Mohandas N. Malaria, erythrocytic infection, and anemia. Hematology. 2009;2009:87–93.
White NJ. Anaemia and malaria. Malar J. 2018;17:371.
Google Scholar
Friedman JF, Kanzaria HK, McGarvey ST. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol. 2005;21:386–92.
Google Scholar
Malaria in Ghana: statistics and facts. Severe malaria observatory. https://www.severemalaria.org/countries/ghana. Accessed Mar 25 2023
Ghana Malaria indicator trends: outputs from a DHS program workshop. Ghana National Malaria Control Programme. 2018. https://dhsprogram.com/publications/publication-od72-other-documents.cfm. Accessed Mar 25 2023
Cunningham LJ, Campbell SJ, Armoo S, Koukounari A, Watson V, Selormey P, et al. Assessing expanded community wide treatment for schistosomiasis: Baseline infection status and self-reported risk factors in three communities from the Greater Accra region, Ghana. PLoS Negl Trop Dis. 2020;14: e0007973.
Google Scholar
Koram KA, Owusu-Agyei S, Fryauff DJ, Anto F, Atuguba F, Hodgson A, et al. Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana. Trop Med Int Health. 2003;8:793–802.
Google Scholar
WHO and UNICEF/UNDP/World Bank Special Programme for Research and Training in Tropical Diseases. Microscopy for the detection, identification and quantification of malaria parasites on stained thick and thin blood films in research settings. Geneva: World Health Organization; 2015. Accessed Apr 08 2023
Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972;14:397–400.
Google Scholar
Montresor A, David WT, Hall A, Bundy DAP, Savioli L, et al. Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level: a guide for managers of control programmes. Geneva: World Health Organization; 1998.
WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva: World Health Organization; 2011.
Dakorah MP, Aninagyei E, Attoh J, Adedia D, Tettey CO, Kyei-Barffour I, et al. Ecological and seasonal variations and other factors associated with clinical malaria in the Central Region of Ghana: a cross-sectional study. J Infect Public Health. 2022;15:631–7.
Google Scholar
Klein SL. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 2004;26:247–64.
Google Scholar
van Eijk AM, Sutton PL, Ramanathapuram L, Sullivan SA, Kanagaraj D, Priya GSL, et al. The burden of submicroscopic and asymptomatic malaria in India revealed from epidemiology studies at three varied transmission sites in India. Sci Rep. 2019;9:17095.
Google Scholar
Pathak S, Rege M, Gogtay NJ, Aigal U, Sharma SK, Valecha N, et al. Age-dependent sex bias in clinical malarial disease in hypoendemic regions. PLoS ONE. 2012;7: e35592.
Google Scholar
Danquah I, Ziniel P, Eggelte T, Ehrhardt S, Mockenhaupt FP. Influence of haemoglobins S and C on predominantly asymptomatic Plasmodium infections in northern Ghana. Trans R Soc Trop Med Hyg. 2010;104:713–9.
Google Scholar
Owusu EDA, Buabeng V, Dadzie S, Brown CA, Grobusch MP, Mens P. Characteristics of asymptomatic Plasmodium spp. parasitaemia in Kwahu-Mpraeso, a malaria endemic mountainous district in Ghana, West Africa. Malar J. 2016;15:38.
Google Scholar
Kanwugu ON, Helegbe GK, Aryee PA, Abdul-Karim A, Anaba F, Ziblim Z, et al. Prevalence of Asymptomatic Malaria among Children in the Tamale metropolis: How Does the PfHRP2 CareStart™ RDT perform against microscopy? J Trop Med. 2019;2019:6457628.
Google Scholar
WHO. Guideline on control and elimination of human schistosomiasis. Geneva: World Health Organization; 2022. p. 142.
WHO/UNICEF Joint Monitoring Program for Water Supply, Sanitation and Hygiene (JMP)—Progress on household drinking water, sanitation and hygiene 2000–2020. https://www.unwater.org/publications/who-unicef-joint-monitoring-program-for-water-supply-sanitation-and-hygiene-jmp-progress-on-household-drinking-water-sanitation-and-hygiene-2000-2020/. Accessed Jun 13 2022
Abanyie FA, McCracken C, Kirwan P, Molloy SF, Asaolu SO, Holland CV, et al. Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children. Malar J. 2013;12:1.
Google Scholar
Chaparro CM, Suchdev PS. Anemia epidemiology, pathophysiology, and etiology in low- and middle-income countries. Ann NY Acad Sci. 2019;1450:15.
Google Scholar
McLean E, Cogswell M, Egli I, Wojdyla D, De Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr. 2009;12:444–54.
Google Scholar
Martín-Masot R, Nestares MT, Diaz-Castro J, López-Aliaga I, Alférez MJM, Moreno-Fernandez J, et al. Multifactorial etiology of anemia in celiac disease and effect of gluten-free diet: a comprehensive review. Nutrients. 2019;11:2557.
Google Scholar
El Hassan AMA, Saeed AM, Fandrey J, Jelkmann W. Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol. 1997;59:299–304.
Google Scholar
Proinflammatory JW, Production CLE. Proinflammatory cytokines lowering erythropoietin production. J Interferon Cytokine Res. 1998;18:555–9.
DufI C, Corcione A, Svahn J, Haupt R, Poggi V, Béka’ssy AN, et al. TNF-α and IFN-γ are overexpressed in the bone marrow of Fanconi anemia patients and TNF-α suppresses erythropoiesis in vitro. Blood. 2003;102:2053–9.
Malaguarnera L, Imbesi RM, Pignatelli S, Simporè J, Malaguarnera M, Musumeci S. Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 2002;24:387–9.
Google Scholar
McDevitt MA, Xie J, Shanmugasundaram G, Griffith J, Liu A, McDonald C, et al. A critical role for the host mediator macrophage migration inhibitory factor in the pathogenesis of malarial anemia. J Exp Med. 2006;203:1185.
Google Scholar
Castro VN, Rodrigues JL, Cardoso DT, Resende SD, Magalhães FC, Souza DC, et al. Systemic cytokine and chemokine profiles in individuals with Schistosoma mansoni Infection and low parasite burden. Front Immunol. 2018;9:2975.
Google Scholar
Zhukovskaya E, Karelin A, Rumyantsev A. Neurocognitive Dysfunctions in Iron Deficiency Patients. In: Rodrigo L, editor. Iron Deficiency Anemia. London: IntechOpen; 2019.
WHO. Anaemia in women and children. Geneva: World Health Organization. https://www.who.int/data/gho/data/themes/topics/anaemia_in_women_and_children. Accessed Apr 24 2023
