{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T11:35:10Z","timestamp":1774265710746,"version":"3.50.1"},"reference-count":53,"publisher":"BMJ","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["BMJ Open"],"accepted":{"date-parts":[[2013,1,24]]},"published-print":{"date-parts":[[2013]]},"abstract":"<jats:sec>\n                    <jats:title>Objectives<\/jats:title>\n                    <jats:p>To quantify geographical variation in the relative contribution of parasitic infections, socioeconomic factors and malnutrition in the aetiology of anaemia among schoolchildren across Kenya, thereby providing a rational basis for the targeting of an integrated school health package.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Design<\/jats:title>\n                    <jats:p>\n                      Nationally representative cross-sectional survey data were collected using standard protocols. For all included children, data were recorded on haemoglobin (Hb) concentration and common parasitic infections (\n                      <jats:italic>Plasmodium falciparum<\/jats:italic>\n                      , hookworm and schistosomes) and socioeconomic indicators. Ecological proxies of malnutrition and food security were generated using Demographic and Health Survey and UN Food and Agriculture Organization food security data, respectively. Spatially explicit, multilevel models were used to quantify impact upon child Hb concentration.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Setting<\/jats:title>\n                    <jats:p>Randomly selected schools in ecologically diverse settings across Kenya.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Main outcome measures<\/jats:title>\n                    <jats:p>Mean Hb concentration adjusted for infection, nutritional and socioeconomic risk factors; associated risk ratios and adjusted Population Attributable Fractions (PAFs) for anaemia, by region.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Data were available for 16\u2005941 children in 167 schools; mean Hb was 122.1\u2005g\/l and 35.3% of children were anaemic. In multivariate analysis, mean Hb was significantly lower in boys and younger children. Severe malnutrition and interactions between\n                      <jats:italic>P falciparum<\/jats:italic>\n                      and hookworm infections were significantly associated with lower Hb, with greater impacts seen for coinfected children. The contribution of risk factors to anaemia risk varied by province: in 14-year-old girls, PAFs ranged between 0% and 27.6% for\n                      <jats:italic>P falciparum,<\/jats:italic>\n                      0% and 29% for hookworm and 0% and 18.4% for severe malnutrition.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>The observed geographical heterogeneity in the burden of anaemia attributable to different aetiological factors has important implications for the rational targeting of antianaemia interventions that can be included in an integrated school health programme.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1136\/bmjopen-2012-001936","type":"journal-article","created":{"date-parts":[[2013,2,23]],"date-time":"2013-02-23T20:09:04Z","timestamp":1361650144000},"page":"e001936","source":"Crossref","is-referenced-by-count":24,"title":["Estimating the relative contribution of parasitic infections and nutrition for anaemia among school-aged children in Kenya: a subnational geostatistical analysis"],"prefix":"10.1136","volume":"3","author":[{"given":"Rachel L","family":"Pullan","sequence":"first","affiliation":[{"name":"Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carol","family":"Gitonga","sequence":"additional","affiliation":[{"name":"Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK"},{"name":"Kenya Medical Research Institute-Wellcome Trust Research Programme, Nairobi, Kenya"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Charles","family":"Mwandawiro","sequence":"additional","affiliation":[{"name":"Eastern and Southern Africa Centre of International Parasite Control, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert William","family":"Snow","sequence":"additional","affiliation":[{"name":"Kenya Medical Research Institute-Wellcome Trust Research Programme, Nairobi, Kenya"},{"name":"Nuffield Department of Clinical Medicine, Centre for Tropical Medicine University of Oxford, Oxford, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simon J","family":"Brooker","sequence":"additional","affiliation":[{"name":"Department of Disease Control, London School of Hygiene and Tropical Medicine, London, UK"},{"name":"Kenya Medical Research Institute-Wellcome Trust Research Programme, Nairobi, Kenya"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"239","published-online":{"date-parts":[[2013,2,22]]},"reference":[{"key":"2025120521393215000_3.2.e001936.1","unstructured":"United Nations Department of Economic and Social Affairs. World population prospects, 2010 revision. http:\/\/esa.Un.Org\/unpd\/wpp\/ (accessed June 2012)."},{"key":"2025120521393215000_3.2.e001936.2","unstructured":"Global Partnership for Education. All children learning: Report 2011. Global Partnership for Education. http:\/\/allchildrenlearningreport.globalpartnership.org (accessed June 2012)."},{"key":"2025120521393215000_3.2.e001936.3","unstructured":"World Bank. Fresh: Focusing resources on education and school health. A fresh start to improving the quality and equity of education. Washington: UNESCO, UNICEF, WHO & World Bank, 2000."},{"key":"2025120521393215000_3.2.e001936.4","doi-asserted-by":"publisher","DOI":"10.1017\/S1368980008002401"},{"key":"2025120521393215000_3.2.e001936.5","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1177\/156482651003100303","article-title":"The nutritional status of school-aged children: why should we care?","volume":"31","author":"Best","year":"2010","journal-title":"Food Nutr Bull"},{"issue":"2Suppl 2","key":"2025120521393215000_3.2.e001936.6","doi-asserted-by":"crossref","first-page":"649S","DOI":"10.1093\/jn\/131.2.649S","article-title":"A review of studies on the effect of iron deficiency on cognitive development in children","volume":"131","author":"Grantham-McGregor","year":"2001","journal-title":"J Nutr"},{"key":"2025120521393215000_3.2.e001936.7","doi-asserted-by":"publisher","DOI":"10.3945\/an.110.000190"},{"key":"2025120521393215000_3.2.e001936.8","doi-asserted-by":"crossref","first-page":"1218S","DOI":"10.1093\/ajcn\/81.5.1218","article-title":"Iron status during pregnancy: setting the stage for mother and infant","volume":"81","author":"Scholl","year":"2005","journal-title":"Am J Clin Nutr"},{"key":"2025120521393215000_3.2.e001936.9","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1007\/s10995-009-0451-8","article-title":"Nutritional status of mothers and low birth weight in India","volume":"14","author":"Dharmalingam","year":"2010","journal-title":"Matern Child Health J"},{"key":"2025120521393215000_3.2.e001936.10","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(08)61034-X"},{"key":"2025120521393215000_3.2.e001936.11","doi-asserted-by":"crossref","unstructured":"Leenstra T Phillips-Howard PA Kariuki SK . Permethrin-treated bed nets in the prevention of malaria and anemia in adolescent schoolgirls in western Kenya. Am J Trop Med Hyg 2003;68:S86\u2013S93.","DOI":"10.4269\/ajtmh.2003.68.86"},{"key":"2025120521393215000_3.2.e001936.12","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3156.2010.02542.x"},{"key":"2025120521393215000_3.2.e001936.13","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/sj.ejcn.1602919","article-title":"The effect of weekly iron and vitamin a supplementation on hemoglobin levels and iron status in adolescent schoolgirls in western Kenya","volume":"63","author":"Leenstra","year":"2009","journal-title":"Eur J Clin Nutr"},{"key":"2025120521393215000_3.2.e001936.14","first-page":"15","article-title":"Effects of iron supplementation on physical performance in chidlren and adolescents: systematic review of randomized controlled trials","volume":"44","author":"Gera","year":"2007","journal-title":"Indian Pediatr"},{"key":"2025120521393215000_3.2.e001936.15","doi-asserted-by":"crossref","unstructured":"Bundy DAP Burbano C Grosh M . Rethinking school feeding: social safety nets, child development and the education sector. New York: The World Bank, 2009.","DOI":"10.1596\/978-0-8213-7974-5"},{"key":"2025120521393215000_3.2.e001936.16","doi-asserted-by":"crossref","unstructured":"Bundy DAP . Rethinking school health: a key component of education for all. Washington: The World Bank, 2012.","DOI":"10.1596\/978-0-8213-7907-3"},{"key":"2025120521393215000_3.2.e001936.17","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1000438"},{"key":"2025120521393215000_3.2.e001936.18","doi-asserted-by":"publisher","DOI":"10.1186\/1475-2875-9-306"},{"key":"2025120521393215000_3.2.e001936.19","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3156.2012.03001.x"},{"key":"2025120521393215000_3.2.e001936.20","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jir844"},{"key":"2025120521393215000_3.2.e001936.21","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-308X(05)62004-0"},{"key":"2025120521393215000_3.2.e001936.22","unstructured":"Balk D Pozzi F Yetman G . The distribution of people and the dimension of place: methodologies to improve the global estimation of urban extents. Urban Remote Sensing Conference ; 2004. http:\/\/www.iussp.org\/Activities\/wgc-urb\/balk.pdf"},{"key":"2025120521393215000_3.2.e001936.23","unstructured":"Kenya National Bureau of Statistics, Measure DHS. Kenya: Dsh, 2008-09-final report. Calverton, MD: Measure DHS, ICF Macro, 2010."},{"key":"2025120521393215000_3.2.e001936.24","unstructured":"Measure DHS. Kenya 2008-09 DHS data. http:\/\/www.measuredhs.com (accessed June 2012)."},{"key":"2025120521393215000_3.2.e001936.25","first-page":"299","article-title":"Model-based geostatistics (with discussion)","volume":"47","author":"Diggle","year":"1998","journal-title":"Appl Statistics"},{"key":"2025120521393215000_3.2.e001936.26","unstructured":"FEWSNET. Famine early warning system network (FEWSNET) livelihood zone map for Kenya. FEWSNET and USAID, 2011."},{"key":"2025120521393215000_3.2.e001936.27","unstructured":"Grillo J Holt J . Application of the livelihood zone maps and profiles for food security analysis and early warning. USAID FEWSNET, 2009."},{"key":"2025120521393215000_3.2.e001936.28","unstructured":"FEWSNET. Famine early warning system network (FEWSNET) Kenya archive: food security update. FEWSNET and USAID, 2011. (accessed June 2012)."},{"key":"2025120521393215000_3.2.e001936.29","unstructured":"WHO. Iron deficiency anaemia: Assessment, prevention and control. A guide for programme managers. Geneva: World Health Organisation, 2001."},{"key":"2025120521393215000_3.2.e001936.30","first-page":"115","article-title":"Estimating wealth effects without expenditure data\u2014or tears: an application to educational enrollments in states of India","volume":"38","author":"Filmer","year":"2001","journal-title":"Demography"},{"key":"2025120521393215000_3.2.e001936.31","doi-asserted-by":"publisher","DOI":"10.1111\/j.0006-341X.2000.00645.x"},{"key":"2025120521393215000_3.2.e001936.32","doi-asserted-by":"publisher","DOI":"10.2105\/AJPH.88.1.15"},{"key":"2025120521393215000_3.2.e001936.33","doi-asserted-by":"crossref","first-page":"88","DOI":"10.4269\/ajtmh.2007.77.88","article-title":"Epidemiology of Plasmodium-helminth coinfeciton in Africa: potential impact on anaemia and prospects for combining control","volume":"77","author":"Brooker","year":"2007","journal-title":"Am J Trop Med Hyg"},{"key":"2025120521393215000_3.2.e001936.34","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182008000346"},{"key":"2025120521393215000_3.2.e001936.35","doi-asserted-by":"publisher","DOI":"10.1645\/GE-895R.1"},{"key":"2025120521393215000_3.2.e001936.36","doi-asserted-by":"publisher","DOI":"10.1016\/j.actatropica.2010.02.010"},{"key":"2025120521393215000_3.2.e001936.37","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0000245"},{"key":"2025120521393215000_3.2.e001936.38","unstructured":"Bundy DAP Shaeffer S Jukes M . School based health and nutrition programs. Chapter 58. In: Jamison DT Breman JG Measham AR ., editors. Disease control priorities for developing countries Washington DC: World Bank; 2006."},{"key":"2025120521393215000_3.2.e001936.39","doi-asserted-by":"publisher","DOI":"10.1016\/j.trstmh.2008.01.010"},{"key":"2025120521393215000_3.2.e001936.40","doi-asserted-by":"publisher","DOI":"10.1016\/j.amepre.2003.12.007"},{"key":"2025120521393215000_3.2.e001936.41","doi-asserted-by":"crossref","unstructured":"Anumudu C Adolami M Igwe C . Nutritional anaemia and malaria in pre-school and school-aged children. Ann Afr Med 2008;1:11\u201317.","DOI":"10.4103\/1596-3519.55690"},{"key":"2025120521393215000_3.2.e001936.42","doi-asserted-by":"publisher","DOI":"10.1186\/1475-2891-10-34"},{"key":"2025120521393215000_3.2.e001936.43","doi-asserted-by":"publisher","DOI":"10.1097\/QAD.0b013e3282fa759f"},{"key":"2025120521393215000_3.2.e001936.44","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1097\/00042560-200101010-00004","article-title":"Prevalence and correlates of anemia in a large cohort of HIV-infected women: women's interagency HIV study","volume":"26","author":"Levine","year":"2001","journal-title":"J Acquir Immune Defic Syndr"},{"key":"2025120521393215000_3.2.e001936.45","doi-asserted-by":"crossref","first-page":"44","DOI":"10.4269\/ajtmh.2007.77.44","article-title":"An update on anaemia in less developed countries","volume":"77","author":"Tolentino","year":"2007","journal-title":"Am J Trop Med Hyg"},{"key":"2025120521393215000_3.2.e001936.46","doi-asserted-by":"publisher","DOI":"10.1038\/sj.ejcn.1601865"},{"key":"2025120521393215000_3.2.e001936.47","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182003004128"},{"key":"2025120521393215000_3.2.e001936.48","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1086\/644781","article-title":"Submicroscopic infection in Plasmodium falciparum endemic populations: a systematic review and meta-analysis","volume":"15","author":"Okell","year":"2009","journal-title":"J Infect Dis"},{"key":"2025120521393215000_3.2.e001936.49","unstructured":"World Bank. World development report 2007: development and the next generation. Washington: The World Bank, 2007."},{"key":"2025120521393215000_3.2.e001936.50","unstructured":"Education and Policy Data Center. Kenya 2005 District Primary Education Profiles. http:\/\/www.epdc.org\/country\/kenya"},{"key":"2025120521393215000_3.2.e001936.51","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.ijedudev.2008.09.011","article-title":"Successful globilisation, education and sustainable development","volume":"29","author":"Little","year":"2009","journal-title":"Int J Educ Dev"},{"key":"2025120521393215000_3.2.e001936.52","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(12)60072-5"},{"key":"2025120521393215000_3.2.e001936.53","unstructured":"Kleinbaum DG Kupper LL Morgenstern H . Epidemiological research. Belmont, CA: Lifetime Learning Publications, 1982:163."}],"container-title":["BMJ Open"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1136\/bmjopen-2012-001936","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T05:39:45Z","timestamp":1764999585000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmjopen.bmj.com\/lookup\/doi\/10.1136\/bmjopen-2012-001936"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013]]},"references-count":53,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2013,2,22]]},"published-print":{"date-parts":[[2013]]}},"alternative-id":["10.1136\/bmjopen-2012-001936"],"URL":"https:\/\/doi.org\/10.1136\/bmjopen-2012-001936","relation":{},"ISSN":["2044-6055","2044-6055"],"issn-type":[{"value":"2044-6055","type":"print"},{"value":"2044-6055","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013]]}}}