Urogenital schistosomiasis transmission, malaria and anemia among school-age children in Northern Ghana
Tóm tắt
Background In sub-Saharan Africa, co-morbidity with malaria, schistosomiasis, and soil transmitted helminths (STH) is common among young children. The current study investigated malaria, urinary schistosomiasis and their co-infection and anemia among school-age children in an endemic community, Nakolo in the Kassena-Nankana East District of northern Ghana. Methods A cross-sectional survey of 336 school-age children, 5–16 years was undertaken. Urine samples were examined for Schistosoma haematobium ova using microscopy. Finger prick blood samples were examined for Plasmodium parasites using microscopy and haemoglobin concentration measured with HemoCue Hb301 photometer. Results The mean age was 10.52 (Standard deviation: ±2.27; range: 5–16 years), of which 50.6% (170/336) were males. The overall prevalence of urinary schistosomiasis and Plasmodium (P.) falciparum was 12.8% (43/336) and 37.8% (127/336), respectively with 6.0% (20/336) coinfection. Participants with only P. falciparum infection had 17.8% (19/107) of moderate anemia whilst 21.7% (5/23) of children infected with only S. haematobium had moderate anemia and 4.3% (1/23) had severe anemia. 5.0 % (1/20) of moderate anemia was observed in concurrent infections of P. falciparum and S. haematobium. Use of open water bodies was associated with increased risk of S. haematobium infection (OR = 1.21; 95% CI = [1.06–1.39]; p = 0.001), with females being at reduced risk (OR = 0.93; 95%CI = [0.87–0.99]; p = 0.005). Absence of self-reported haematuria had 0.81 times reduced odds of S. haematobium infection (OR = 0.81; 95%CI = [0.74–0.87]; p < 0.001). Conclusion This study has revealed that urinary schistosomiasis remains prevalent in Kassena-Nankana East district and suggests that urinary schistosomiasis may contribute to moderate anemia among school-age children as compared to asymptomatic malaria infection. These findings call for an evaluation of the annual mass drug administration of Praziquantel among in-school children to ascertain its impact on urinary schistosomiasis prevalence across the district.
Từ khóa
#Urogenital schistosomiasis #Schistosoma haematobium #Malaria #Anemia #Northern GhanaTài liệu tham khảo
[1] J.C. Sousa-Figueiredo D. Gamboa J.M. Pedro C. Fançony A.J. Langa R.J.S. Magalhães Epidemiology of malaria, schistosomiasis, geohelminths, anemia and malnutrition in the context of a demographic surveillance System in northern Angola PLoS One 7 2012 e33189 Sousa-Figueiredo JC, Gamboa D, Pedro JM, Fancony C, Langa AJ, Magalhaes RJS, et al. Epidemiology of malaria, schistosomiasis, geohelminths, anemia and malnutrition in the context of a demographic surveillance System in northern Angola. PLoS One. 2012;7: e33189.
[2] D.G. Colley A.L. Bustinduy W.E. Secor C.H. King Human schistosomiasis Lancet 383 2014 2253 2264 Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383: 2253-2264.
null
[4] F. Anto Water contact activities and prevalence of schistosomiasis infection among school-age children in communities along an irrigation scheme in rural northern Ghana J. Bacteriol. Parasitol. 4 2013 Anto F. Water contact activities and prevalence of schistosomiasis infection among school-age children in communities along an irrigation scheme in rural northern Ghana. J. Bacteriol. Parasitol.. 2013;4.
[5] C. Shiff R. Veltri J. Naples J. Quartey J. Otchere W. Anyan Ultrasound verification of bladder damage is associated with known biomarkers of bladder cancer in adults chronically infected with Schistosoma haematobium in Ghana Trans. R. Soc. Trop. Med. Hyg. 100 2006 847 854 Shiff C, Veltri R, Naples J, Quartey J, Otchere J, Anyan W, et al. Ultrasound verification of bladder damage is associated with known biomarkers of bladder cancer in adults chronically infected with Schistosoma haematobium in Ghana. Trans. R. Soc. Trop. Med. Hyg.. 2006;100: 847-854.
[6] D.M. Forsyth G. MacDonald Urological Complications of Endemic Schistosomiasis in School-Children: Part 1. Usagara School Transactions of the Royal Society of Tropical Medicine and Hygiene 59 1965 171 178 Forsyth DM, MacDonald G. Urological Complications of Endemic Schistosomiasis in School-Children: Part 1. Usagara School. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1965;59: 171-178.
[7] C.H. King M. Dangerfield-Cha The unacknowledged impact of chronic schistosomiasis Chron. Illness 4 2008 65 79 King CH, Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chron. Illness. 2008;4: 65-79.
[8] K. Deribew Z. Tekeste B. Petros Urinary schistosomiasis and malaria associated anemia in Ethiopia Asian Pac. J. Trop. Biomed. 3 2013 307 310 Deribew K, Tekeste Z, Petros B. Urinary schistosomiasis and malaria associated anemia in Ethiopia. Asian Pac. J. Trop. Biomed.. 2013;3: 307-310.
[9] V. Briand L. Watier J.-Y.L. Hesran A. Garcia M. Cot Coinfection with plasmodium falciparum and schistosoma haematobium: protective effect of schistosomiasis on malaria in SENEGALESE children? Am. J. Trop. Med. Hyg. 72 2005 702 707 Briand V, Watier L, Hesran J-YL, Garcia A, Cot M. Coinfection with plasmodium falciparum and schistosoma haematobium: protective effect of schistosomiasis on malaria in SENEGALESE children? Am. J. Trop. Med. Hyg.. 2005;72: 702-707.
[10] S.M. Kinung’hi P. Magnussen G.M. Kaatano C. Kishamawe B.J. Vennervald Malaria and helminth Co-infections in school and preschool children: a cross-sectional study in magu district, north-western Tanzania PLoS One 9 2014 e86510 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: e86510.
[11] L.E.G. Mboera K.P. Senkoro S.F. Rumisha B.K. Mayala E.H. Shayo M.R.S. Mlozi Plasmodium falciparum and helminth coinfections among schoolchildren in relation to agro-ecosystems in Mvomero District, Tanzania Acta Trop. 120 2011 95 102 Mboera LEG, Senkoro KP, Rumisha SF, Mayala BK, Shayo EH, Mlozi MRS. Plasmodium falciparum and helminth coinfections among schoolchildren in relation to agro-ecosystems in Mvomero District, Tanzania. Acta Trop.. 2011;120: 95-102.
[12] S.J. Brooker R.L. Pullan C.W. Gitonga R.A. Ashton J.H. Kolaczinski N.B. Kabatereine Plasmodium–helminth coinfection and its sources of heterogeneity across East Africa J. Infect. Dis. 205 2012 841 852 Brooker SJ, Pullan RL, Gitonga CW, Ashton RA, Kolaczinski JH, Kabatereine NB, et al. Plasmodium-helminth coinfection and its sources of heterogeneity across East Africa. J. Infect. Dis.. 2012;205: 841-852.
[13] T.O. Diallo F. Remoue L. Gaayeb A.-M. Schacht N. Charrier D.D. Clerck Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens PLoS One 5 2010 e12764 Diallo TO, Remoue F, Gaayeb L, Schacht A-M, Charrier N, Clerck DD, et al. Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS One. 2010;5: e12764.
[14] J.F. Friedman H.K. Kanzaria S.T. McGarvey Human schistosomiasis and anemia: the relationship and potential mechanisms Trends Parasitol. 21 2005 386 392 Friedman JF, Kanzaria HK, McGarvey ST. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol.. 2005;21: 386-392.
[15] L.J. Cunningham S.J. Campbell S. Armoo A. Koukounari V. Watson P. Selormey 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 Neglected Trop. Dis. 14 2020 e0007973 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 Neglected Trop. Dis.. 2020;14: e0007973.
[16] Q. Abass J.Y. Bedzo S. Manortey Impact of mass drug administration on prevalence of schistosomiasis in eight riverine communities in the asuogyaman district of the eastern region, Ghana Int. J. Trop. Dis. Health 2020 18 32 Abass Q, Bedzo JY, Manortey S. Impact of mass drug administration on prevalence of schistosomiasis in eight riverine communities in the asuogyaman district of the eastern region, Ghana. Int. J. Trop. Dis. Health. 2020; 18-32.
[17] I.F. Aboagye D. Edoh Investigation of the risk of infection of urinary schistosomiasis at mahem and galilea communities in the greater Accra region of Ghana West Afr. J. Appl. Ecol. 15 2009 Aboagye IF, Edoh D. Investigation of the risk of infection of urinary schistosomiasis at mahem and galilea communities in the greater Accra region of Ghana. West Afr. J. Appl. Ecol.. 2009;15.
[18] M.E. Aryeetey Y. Wagatsuma G. Yeboah M. Asante G. Mensah F.K. Nkrumah Urinary schistosomiasis in southern Ghana: 1. Prevalence and morbidity assessment in three (defined) rural areas drained by the Densu river Parasitol. Int. 49 2000 155 163 Aryeetey ME, Wagatsuma Y, Yeboah G, Asante M, Mensah G, Nkrumah FK, et al. Urinary schistosomiasis in southern Ghana: 1. Prevalence and morbidity assessment in three (defined) rural areas drained by the Densu river. Parasitol. Int.. 2000;49: 155-163.
[19] M.F. Lima e Costa M.H. Magalhães R.S. Rocha C.M. Antunes N. Katz Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil Bull. World Health Organ. 65 1987 57 66 Lima e Costa MF, Magalhaes MH, Rocha RS, Antunes CM, Katz N. Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull. World Health Organ.. 1987;65: 57-66.
[20] N.C. Lo D.G. Addiss P.J. Hotez C.H. King J.R. Stothard D.S. Evans A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now Lancet Infect. Dis. 17 2017 e64 e69 Lo NC, Addiss DG, Hotez PJ, King CH, Stothard JR, Evans DS, et al. A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now. Lancet Infect. Dis.. 2017;17: e64-e69.
[21] B.E. Barber G.S. Rajahram M.J. Grigg T. William N.M. Anstey World Malaria Report: time to acknowledge Plasmodium knowlesi malaria Malar. J. 16 2017 135 Barber BE, Rajahram GS, Grigg MJ, William T, Anstey NM. World Malaria Report: time to acknowledge Plasmodium knowlesi malaria. Malar. J.. 2017;16: 135.
[22] E.C. Opoku A. Olsen E. Browne A. Hodgson J.K. Awoonor-Williams L. Yelifari Impact of combined intermittent preventive treatment of malaria and helminths on anaemia, sustained attention, and recall in Northern Ghanaian schoolchildren Glob. Health Action 9 2016 32197 Opoku EC, Olsen A, Browne E, Hodgson A, Awoonor-Williams JK, Yelifari L, et al. Impact of combined intermittent preventive treatment of malaria and helminths on anaemia, sustained attention, and recall in Northern Ghanaian schoolchildren. Glob. Health Action. 2016;9: 32197.
[23] A.R. Oduro G. Wak D. Azongo C. Debpuur P. Wontuo F. Kondayire Profile of the Navrongo health and demographic surveillance System Int. J. Epidemiol. 41 2012 968 976 Oduro AR, Wak G, Azongo D, Debpuur C, Wontuo P, Kondayire F, et al. Profile of the Navrongo health and demographic surveillance System. Int. J. Epidemiol.. 2012;41: 968-976.
[24] K.A. Koram S. Owusu-Agyei D.J. Fryauff F. Anto F. Atuguba A. Hodgson Seasonal profiles of malaria infection, anaemia, and bednet use among age groups and communities in northern Ghana Trop. Med. Int. Health 8 2003 793 802 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.
[25] E.O. Okanla B.N. Agba J.O. Awotunde Schistosoma haematobium: prevalence and socio-economic factors among students in Cape Coast Ghana Afr. J. Biomed. Res. 6 2003 Okanla EO, Agba BN, Awotunde JO. Schistosoma haematobium: prevalence and socio-economic factors among students in Cape Coast Ghana. Afr. J. Biomed. Res.. 2003;6.
[26] R Core T. R A Language and Environment for Statistical Computing 2017 R Foundation for Statistical Computing Vienna, Austria Available: https://www.R-project.org/ R Core T. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2017;Vienna, Austria. Available: https://www.R-project.org/.
null
[28] V.A. Francis Anto Childhood activities and schistosomiasis infection in the kassena-nankana district of northern Ghana J. Infect. Dis. 2 2014 Francis Anto VA. Childhood activities and schistosomiasis infection in the kassena-nankana district of northern Ghana. J. Infect. Dis.. 2014;2.
null
[30] S.J. Campbell G.B. Savage D.J. Gray J.-A.M. Atkinson R.J.S. Magalhães S.V. Nery Water, sanitation, and hygiene (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control PLoS Neglected Trop. Dis. 8 2014 e2651 Campbell SJ, Savage GB, Gray DJ, Atkinson J-AM, Magalhaes RJS, Nery SV, et al. Water, sanitation, and hygiene (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control. PLoS Neglected Trop. Dis.. 2014;8: e2651.
[31] K.C. Kosinski M.N. Adjei K.M. Bosompem J.J. Crocker J.L. Durant D. Osabutey Effective control of schistosoma haematobium infection in a Ghanaian community following installation of a water recreation area PLoS Neglected Trop. Dis. 6 2012 e1709 Kosinski KC, Adjei MN, Bosompem KM, Crocker JJ, Durant JL, Osabutey D, et al. Effective control of schistosoma haematobium infection in a Ghanaian community following installation of a water recreation area. PLoS Neglected Trop. Dis.. 2012;6: e1709.
[32] R. Nyarko K. Torpey A. Ankomah Schistosoma haematobium, Plasmodium falciparum infection and anaemia in children in Accra, Ghana. Tropical Diseases Travel Medicine and Vaccines 4 2018 3 Nyarko R, Torpey K, Ankomah A. Schistosoma haematobium, Plasmodium falciparum infection and anaemia in children in Accra, Ghana. Tropical Diseases, Travel Medicine and Vaccines. 2018;4: 3.
[33] T. Awine K. Malm C. Bart-Plange S.P. Silal Towards malaria control and elimination in Ghana: challenges and decision making tools to guide planning Glob. Health Action 10 2017 Awine T, Malm K, Bart-Plange C, Silal SP. Towards malaria control and elimination in Ghana: challenges and decision making tools to guide planning. Glob. Health Action. 2017;10.
[34] H.E. Mensah-Brown J. Abugri K.P. Asante D. Dwomoh D. Dosoo F. Atuguba Assessing the impact of differences in malaria transmission intensity on clinical and haematological indices in children with malaria Malar. J. 16 2017 96 Mensah-Brown HE, Abugri J, Asante KP, Dwomoh D, Dosoo D, Atuguba F, et al. Assessing the impact of differences in malaria transmission intensity on clinical and haematological indices in children with malaria. Malar. J.. 2017;16: 96.
[35] D. Humphries E. Mosites J. Otchere W.A. Twum L. Woo H. Jones-Sanpei Epidemiology of hookworm infection in kintampo North municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure Am. J. Trop. Med. Hyg. 84 2011 792 800 Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, et al. Epidemiology of hookworm infection in kintampo North municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am. J. Trop. Med. Hyg.. 2011;84: 792-800.
[36] D. Humphries S. Nguyen S. Kumar J.E. Quagraine J. Otchere L.M. Harrison Effectiveness of albendazole for hookworm varies widely by community and correlates with nutritional factors: a cross-sectional study of school-age children in Ghana Am. J. Trop. Med. Hyg. 96 2017 347 354 Humphries D, Nguyen S, Kumar S, Quagraine JE, Otchere J, Harrison LM, et al. Effectiveness of albendazole for hookworm varies widely by community and correlates with nutritional factors: a cross-sectional study of school-age children in Ghana. Am. J. Trop. Med. Hyg.. 2017;96: 347-354.
[37] D. Adu-Gyasi K.P. Asante M.T. Frempong D.K. Gyasi L.F. Iddrisu L. Ankrah Epidemiology of soil transmitted Helminth infections in the middle-belt of Ghana, Africa Parasite Epidemiology and Control 3 2018 e00071 Adu-Gyasi D, Asante KP, Frempong MT, Gyasi DK, Iddrisu LF, Ankrah L, et al. Epidemiology of soil transmitted Helminth infections in the middle-belt of Ghana, Africa. Parasite Epidemiology and Control. 2018;3: e00071.
[38] E.M. Tukahebwa P. Magnussen H. Madsen N.B. Kabatereine F. Nuwaha S. Wilson A very high infection intensity of schistosoma mansoni in a Ugandan lake victoria fishing community is required for association with highly prevalent organ related morbidity PLoS Neglected Trop. Dis. 7 2013 e2268 Tukahebwa EM, Magnussen P, Madsen H, Kabatereine NB, Nuwaha F, Wilson S, et al. A very high infection intensity of schistosoma mansoni in a Ugandan lake victoria fishing community is required for association with highly prevalent organ related morbidity. PLoS Neglected Trop. Dis.. 2013;7: e2268.
[39] G. Alebie B. Erko M. Aemero B. Petros Epidemiological Study on Schistosoma Mansoni Infection in Sanja Area, Amhara Region, Ethiopia 7 2014 Parasites & Vectors 15 Alebie G, Erko B, Aemero M, Petros B. Epidemiological Study on Schistosoma Mansoni Infection in Sanja Area, Amhara Region, Ethiopia. Parasites & Vectors. 2014;7: 15.
[40] E. Amuta R. Houmsou Prevalence, intensity of infection and risk factors of urinary schistosomiasis in pre-school and school aged children in Guma Local Government Area, Nigeria Asian Pacific Journal of Tropical Medicine 7 2014 34 39 Amuta E, Houmsou R. Prevalence, intensity of infection and risk factors of urinary schistosomiasis in pre-school and school aged children in Guma Local Government Area, Nigeria. Asian Pacific Journal of Tropical Medicine. 2014;7: 34-39.
[41] O.A. Morenikeji B.A. Idowu Studies on the prevalence of urinary schistosomiasis in ogun state, south-western Nigeria W. Afr. J. Med. 30 2011 62 65–65 Morenikeji OA, Idowu BA. Studies on the prevalence of urinary schistosomiasis in ogun state, south-western Nigeria. W. Afr. J. Med.. 2011;30: 62-65-65.
[42] M.G. Chipeta B. Ngwira L.N. Kazembe Analysis of schistosomiasis haematobium infection prevalence and intensity in chikhwawa, Malawi: an application of a two Part Model PLoS Neglected Trop. Dis. 7 2013 e2131 Chipeta MG, Ngwira B, Kazembe LN. Analysis of schistosomiasis haematobium infection prevalence and intensity in chikhwawa, Malawi: an application of a two Part Model. PLoS Neglected Trop. Dis.. 2013;7: e2131.
[43] A.A. Al-Waleedi N.A. El-Nimr A.A. Hasab H.K. Bassiouny L.A. Al-Shibani Urinary schistosomiasis among schoolchildren in Yemen: prevalence, risk factors, and the effect of a chemotherapeutic intervention J. Egypt. Publ. Health Assoc. 88 2013 130 Al-Waleedi AA, El-Nimr NA, Hasab AA, Bassiouny HK, Al-Shibani LA. Urinary schistosomiasis among schoolchildren in Yemen: prevalence, risk factors, and the effect of a chemotherapeutic intervention. J. Egypt. Publ. Health Assoc.. 2013;88: 130.
[44] F. Anto Water contact activities and prevalence of schistosomiasis infection among school-age children in communities along an irrigation scheme in rural northern Ghana J. Bacteriol. Parasitol. 4 2013 Anto F. Water contact activities and prevalence of schistosomiasis infection among school-age children in communities along an irrigation scheme in rural northern Ghana. J. Bacteriol. Parasitol.. 2013;4.
[45] H. Sady H.M. Al-Mekhlafi M.A.K. Mahdy Y.A.L. Lim R. Mahmud J. Surin Prevalence and associated factors of schistosomiasis among children in Yemen: implications for an effective control programme PLoS Neglected Trop. Dis. 7 2013 e2377 Sady H, Al-Mekhlafi HM, Mahdy MAK, Lim YAL, Mahmud R, Surin J. Prevalence and associated factors of schistosomiasis among children in Yemen: implications for an effective control programme. PLoS Neglected Trop. Dis.. 2013;7: e2377.
[46] B. Senghor A. Diallo S.N. Sylla S. Doucouré M.O. Ndiath L. Gaayeb Prevalence and Intensity of Urinary Schistosomiasis Among School Children in the District of Niakhar, Region of Fatick, Senegal 7 2014 Parasites & Vectors 5 Senghor B, Diallo A, Sylla SN, Doucoure S, Ndiath MO, Gaayeb L, et al. Prevalence and Intensity of Urinary Schistosomiasis Among School Children in the District of Niakhar, Region of Fatick, Senegal. Parasites & Vectors. 2014;7: 5.
[47] Bogoch II J.R. Andrews R.K.D. Ephraim J. Utzinger Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana Trop. Med. Int. Health 17 2012 1217 1221 Bogoch II, Andrews JR, Ephraim RKD, Utzinger J. Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana. Trop. Med. Int. Health. 2012;17: 1217-1221.