{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T18:03:52Z","timestamp":1792260232122,"version":"4.4.0"},"reference-count":55,"publisher":"American Society of Tropical Medicine and Hygiene","issue":"4","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2016,10,5]]},"abstract":"<jats:p>Soil-transmitted helminth (STH) infection has been associated with lower cognitive performance of schoolchildren. To identify pathways through which STH infection might affect school performance, baseline data from a large rice-fortification trial in Cambodian schoolchildren were used to investigate associations between STH infection, micronutrient status, anemia, and cognitive performance. Complete data on anthropometry, cognitive performance, and micronutrient status were available for 1,760 schoolchildren, 6\u201316 years of age. STH infection was identified using Kato\u2013Katz, whereas cognitive performance was assessed using Raven's Colored Progressive Matrices (RCPM), block design, and picture completion. STH infection was found in 18% of the children; almost exclusively hookwork infection. After adjusting for age and gender, raw cognitive test scores were significantly lower in hookworm-infected children (\u22120.65; \u22120.78; \u22122.03 points for picture completion, RCPM, and block design, respectively; <jats:italic>P<\/jats:italic> &lt; 0.05 for all). Hookworm infection was associated with iron status (total body iron), but not with vitamin A and zinc status, nor with inflammation or anthropometry. Body iron was negatively associated with increased intensity of hookworm infection (<jats:italic>R<\/jats:italic> = 0.22, <jats:italic>P<\/jats:italic> &lt; 0.001). Hookworm infection in Cambodian schoolchildren was associated with lower cognitive performance, an effect most likely mediated through lower body iron. Interventions that are more effective against hookworm infection are needed to contribute to better health and improvement of cognitive performance.<\/jats:p>","DOI":"10.4269\/ajtmh.15-0813","type":"journal-article","created":{"date-parts":[[2016,8,30]],"date-time":"2016-08-30T02:43:08Z","timestamp":1472524988000},"page":"856-863","source":"Crossref","is-referenced-by-count":25,"title":["Cognitive Performance and Iron Status are Negatively Associated with Hookworm Infection in Cambodian Schoolchildren"],"prefix":"10.4269","volume":"95","author":[{"given":"Khov","family":"Kuong","sequence":"first","affiliation":[{"name":"1Department of Fisheries Post-Harvest Technologies and Quality Control, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia."},{"name":"7Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marion","family":"Fiorentino","sequence":"additional","affiliation":[{"name":"2Institut de Recherche pour le D\u00e9veloppement, Montpellier, France."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marlene","family":"Perignon","sequence":"additional","affiliation":[{"name":"2Institut de Recherche pour le D\u00e9veloppement, Montpellier, France."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chhoun","family":"Chamnan","sequence":"additional","affiliation":[{"name":"1Department of Fisheries Post-Harvest Technologies and Quality Control, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacques","family":"Berger","sequence":"additional","affiliation":[{"name":"2Institut de Recherche pour le D\u00e9veloppement, Montpellier, France."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muth","family":"Sinuon","sequence":"additional","affiliation":[{"name":"3National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vann","family":"Molyden","sequence":"additional","affiliation":[{"name":"3National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kurt","family":"Burja","sequence":"additional","affiliation":[{"name":"4United Nations World Food Program, Phnom Penh, Cambodia."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan","family":"Parker","sequence":"additional","affiliation":[{"name":"5PATH, Seattle, Washington."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sou Chheng","family":"Ly","sequence":"additional","affiliation":[{"name":"6Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henrik","family":"Friis","sequence":"additional","affiliation":[{"name":"7Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nanna","family":"Roos","sequence":"additional","affiliation":[{"name":"7Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank T.","family":"Wieringa","sequence":"additional","affiliation":[{"name":"2Institut de Recherche pour le D\u00e9veloppement, Montpellier, France."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"2795","reference":[{"key":"ref1","series-title":"N Engl J Med","first-page":"1018","article-title":"Control of neglected tropical diseases","volume":"357","author":"Hotez","year":"2007"},{"key":"ref2","series-title":"Disease Control Priorities in Developing Countries","author":"Jamison","year":"2006"},{"key":"ref3","series-title":"Pharmacoeconomics","first-page":"14","article-title":"The cost effectiveness of mass drug therapy for intestinal helminths","volume":"8","author":"Evans","year":"1995"},{"key":"ref4","series-title":"Parasitol Today","first-page":"14","article-title":"Does helminth infection affect mental processing and educational achievement?","volume":"10","author":"Nokes","year":"1994"},{"key":"ref5","series-title":"Trans R Soc Trop Med Hyg","first-page":"353","article-title":"Intestinal parasitic infections: a soluble public health problem","volume":"86","author":"Savioli","year":"1992"},{"key":"ref6","series-title":"Acta Paediatr","first-page":"1188","article-title":"School performance, nutritional status and trichuriasis in Jamaican schoolchildren","volume":"83","author":"Simeon","year":"1994"},{"key":"ref7","series-title":"Annu Rev Nutr","first-page":"35","article-title":"Nutritional impact of intestinal helminthiasis during the human life cycle","volume":"22","author":"Crompton","year":"2002"},{"key":"ref8","series-title":"Semin Pediatr Infect Dis","first-page":"245","article-title":"Geohelminth infections (ascariasis, trichuriasis, and hookworm): cognitive and developmental impacts","volume":"11","author":"Drake","year":"2000"},{"key":"ref9","series-title":"Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level","first-page":"1","author":"Montresor","year":"1998"},{"key":"ref10","series-title":"Cochrane Database Syst Rev","first-page":"CD000371","article-title":"Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin and school performance","volume":"7","author":"Taylor-Robinson","year":"2012"},{"key":"ref11","series-title":"Am J Trop Med Hyg","first-page":"77","article-title":"Species-specific associations between soil-transmitted helminths and micronutrients in Vietnamese schoolchildren","volume":"95","author":"de Gier","year":"2016"},{"key":"ref12","series-title":"Adv Parasitol","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/S0065-308X(10)72002-9","article-title":"Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region","volume":"72","author":"Hotez","year":"2010"},{"key":"ref13","series-title":"Deworming for Health and Development: Report of the Third Global Meeting of the Partners for Parasite Control","author":"World Health Organization (WHO)","year":"2005"},{"key":"ref14","series-title":"Parasitic Infections in Pregnancy and the Newborn","author":"MacLeod","year":"1988"},{"key":"ref15","series-title":"Pediatrics","first-page":"1381","article-title":"Iron deficiency and cognitive achievement among school-aged children and adolescents in the United States","volume":"107","author":"Halterman","year":"2001"},{"key":"ref16","series-title":"Arzneimittel-Forschung-Drug Research","first-page":"426","article-title":"Effects of iron deficiency anemia on cognitive function in children","volume":"57","author":"Agaoglu","year":"2007"},{"key":"ref17","series-title":"J Nutr","first-page":"676S","article-title":"Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship","volume":"131","author":"Haas","year":"2001"},{"key":"ref18","series-title":"CMAJ","first-page":"1477","article-title":"Iron supplementation for children: safety in all settings is not clear","volume":"185","author":"Gray-Donald","year":"2013"},{"key":"ref19","series-title":"PLoS Negl Trop Dis","first-page":"e1550","article-title":"Association between anaemia, iron deficiency anaemia, neglected parasitic infections and socioeconomic factors in rural children of west Malaysia","volume":"6","author":"Ngui","year":"2012"},{"key":"ref20","series-title":"Cambodia Demographic and Health Survey 2010","author":"National Institute of Statistics, Directorate General for Health, ICF Macro","year":"2011"},{"key":"ref21","series-title":"PLoS Negl Trop Dis","first-page":"e278","article-title":"Large-scale preventive chemotherapy for the control of helminth infection in western Pacific countries: six years later","volume":"2","author":"Montresor","year":"2008"},{"key":"ref22","series-title":"Cambodia National Helminth Task-Force, Policy and Guideline","author":"CNM","year":"2004"},{"key":"ref23","series-title":"Anthropometric Indicators Measurement Guide","author":"Cogill","year":"2003"},{"key":"ref24","series-title":"Physical Status: The Use and Interpretation of Anthropometry","author":"World Health Organization (WHO)","year":"1995"},{"key":"ref25","series-title":"Psychological Testing: Principles, Applications, and Issues","author":"Kaplan","year":"2012"},{"key":"ref26","series-title":"Eur J Nutr","first-page":"4","article-title":"Nutrition and cognition: assessing cognitive abilities in children and young people","volume":"47","author":"Isaacs","year":"2008"},{"key":"ref27","series-title":"Nutr Rev","first-page":"413","article-title":"The assessment of cognitive performance in children: considerations for detecting nutritional influences","volume":"61","author":"Hughes","year":"2003"},{"key":"ref28","series-title":"Iron Deficiency Anaemia: Assessment, Prevention and Control: A Guide for Programme Managers","author":"World Health Organization (WHO)","year":"2001"},{"key":"ref29","series-title":"J Nutr","first-page":"1974","article-title":"Hemoglobin and ferritin are currently the most efficient indicators of population response to iron interventions: an analysis of nine randomized controlled trials","volume":"135","author":"Mei","year":"2005"},{"key":"ref30","series-title":"Am J Clin Nutr","first-page":"615","article-title":"Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children","volume":"81","author":"Zimmermann","year":"2005"},{"key":"ref31","series-title":"J Nutr","first-page":"781","article-title":"Genetic hemoglobin disorders, infection, and deficiencies of iron and vitamin A determine anemia in young Cambodian children","volume":"142","author":"George","year":"2012"},{"key":"ref32","series-title":"Blood","first-page":"3359","article-title":"The quantitative assessment of body iron","volume":"101","author":"Cook","year":"2003"},{"key":"ref33","series-title":"J Nutr","first-page":"3127","article-title":"Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique","volume":"134","author":"Erhardt","year":"2004"},{"key":"ref34","series-title":"Am J Clin Nutr","first-page":"546","article-title":"Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: a meta-analysis","volume":"92","author":"Thurnham","year":"2010"},{"key":"ref35","series-title":"Am J Clin Nutr","first-page":"615","article-title":"Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children","volume":"81","author":"Zimmermann","year":"2005"},{"key":"ref36","series-title":"Blood","first-page":"1870","article-title":"Serum transferrin receptor: a quantitative measure of tissue iron deficiency","volume":"75","author":"Skikne","year":"1990"},{"key":"ref37","series-title":"Am J Clin Nutr","first-page":"615","article-title":"Serum transferrin receptor and zinc protoporphyrin as indicators of iron status","volume":"81","author":"Zimmermann","year":"2005"},{"key":"ref38","series-title":"Blood","first-page":"1870","article-title":"Serum transferrin receptor: a quantitative measure of tissue iron deficiency","volume":"75","author":"Skikne","year":"1990"},{"key":"ref39","series-title":"Blood","first-page":"3359","article-title":"The quantitative assessment of body iron","volume":"101","author":"Cook","year":"2003"},{"key":"ref40","series-title":"J Nutr","first-page":"2895S","article-title":"Biochemical indicators of vitamin A deficiency: serum retinol and serum retinol binding protein","volume":"132","author":"De Pee","year":"2002"},{"key":"ref41","series-title":"Lancet","first-page":"2052","article-title":"Effects of subclinical infection on plasma retinol concentrations and assessment of prevalence of vitamin A deficiency: meta-analysis","volume":"362","author":"Thurnham","year":"2003"},{"key":"ref42","series-title":"Principles of Nutritional Assessment","author":"Gibson","year":"2005"},{"key":"ref43","series-title":"Food Nutr Bull","first-page":"S99","article-title":"International Zinc Nutrition Consultative Group (IZiNCG) technical document #1. Assessment of the risk of zinc deficiency in populations and options for its control","volume":"25","author":"Brown","year":"2004"},{"key":"ref44","series-title":"Eur J Haematol","first-page":"57","article-title":"Analysis of fetal blood using capillary electrophoresis system: a simple method for prenatal diagnosis of severe thalassemia diseases","volume":"83","author":"Srivorakun","year":"2009"},{"key":"ref45","series-title":"Bench Aids for the Diagnosis of Intestinal Parasites","author":"World Health Organization (WHO)","year":"1994"},{"key":"ref46","series-title":"PLoS Negl Trop Dis","first-page":"e1417","article-title":"Low efficacy of single-dose albendazole and mebendazole against hookworm and effect on concomitant helminth infection in Lao PDR","volume":"6","author":"Soukhathammavong","year":"2012"},{"key":"ref47","series-title":"Am J Clin Nutr","first-page":"462","article-title":"In Ivorian school-age children, infection with hookworm does not reduce dietary iron absorption or systemic iron utilization, whereas afebrile Plasmodium falciparum infection reduces iron absorption by half","volume":"101","author":"Glinz","year":"2015"},{"key":"ref48","series-title":"J Trop Med Hyg","first-page":"114","article-title":"Absorption of vitamin A in children with ascariasis","volume":"78","author":"Sivakumar","year":"1975"},{"key":"ref49","series-title":"Am J Clin Nutr","first-page":"1276","article-title":"Malabsorption syndrome in ascariasis","volume":"25","author":"Tripathy","year":"1972"},{"key":"ref50","series-title":"Am J Trop Med Hyg","first-page":"299","article-title":"Soil-transmitted helminth infection and nutritional status among urban slum children in Kenya","volume":"90","author":"Suchdev","year":"2014"},{"key":"ref51","series-title":"J Nutr","first-page":"2262","article-title":"Acute phase protein levels, T. trichiura, and maternal education are predictors of serum zinc in a cross-sectional study in Bangladeshi children","volume":"136","author":"Kongsbak","year":"2006"},{"key":"ref52","series-title":"Trans R Soc Trop Med Hyg","first-page":"240","article-title":"The epidemiology of hookworm infection and its contribution to anaemia among pre-school children on the Kenyan coast","volume":"93","author":"Brooker","year":"1999"},{"key":"ref53","series-title":"J Nutr","first-page":"1724","article-title":"Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0-to 5-y old Zanzibari children and these relationships change with age","volume":"130","author":"Stoltzfus","year":"2000"},{"key":"ref54","series-title":"J Nutr","first-page":"1099","article-title":"Linear growth retardation in Zanzibari school children","volume":"127","author":"Stoltzfus","year":"1997"},{"key":"ref55","series-title":"Trans R Soc Trop Med Hyg","first-page":"643","article-title":"The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in western Kenya","volume":"92","author":"Olsen","year":"1998"}],"container-title":["The American Society of Tropical Medicine and Hygiene"],"original-title":[],"link":[{"URL":"https:\/\/www.ajtmh.org\/view\/journals\/tpmd\/95\/4\/article-p856.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.ajtmh.org\/downloadpdf\/journals\/tpmd\/95\/4\/article-p856.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/www.ajtmh.org\/downloadpdf\/journals\/tpmd\/95\/4\/article-p856.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,7]],"date-time":"2024-08-07T21:55:46Z","timestamp":1723067746000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.ajtmh.org\/view\/journals\/tpmd\/95\/4\/article-p856.xml"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,5]]},"references-count":55,"journal-issue":{"issue":"4"},"URL":"https:\/\/doi.org\/10.4269\/ajtmh.15-0813","relation":{},"ISSN":["0002-9637","1476-1645"],"issn-type":[{"value":"0002-9637","type":"print"},{"value":"1476-1645","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,5]]}}}