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Cognitive Performance and Iron Status are Negatively Associated with Hookworm Infection in Cambodian Schoolchildren
Khov Kuong
Khov Kuong
Department of Fisheries Post-Harvest Technologies and Quality Control, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia.
Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark.
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Marion Fiorentino
Marion Fiorentino
Institut de Recherche pour le Développement, Montpellier, France.
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Marlene Perignon
Marlene Perignon
Institut de Recherche pour le Développement, Montpellier, France.
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Chhoun Chamnan
Chhoun Chamnan
Department of Fisheries Post-Harvest Technologies and Quality Control, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia.
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Jacques Berger
Jacques Berger
Institut de Recherche pour le Développement, Montpellier, France.
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Muth Sinuon
Muth Sinuon
National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia.
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Vann Molyden
Vann Molyden
National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia.
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Kurt Burja
Kurt Burja
United Nations World Food Program, Phnom Penh, Cambodia.
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Megan Parker
Megan Parker
PATH, Seattle, Washington.
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Sou Chheng Ly
Sou Chheng Ly
Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands.
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Henrik Friis
Henrik Friis
Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark.
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Nanna Roos
Nanna Roos
Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark.
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Frank T. Wieringa
Frank T. Wieringa
Institut de Recherche pour le Développement, Montpellier, France.
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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, 6–16 years of age. STH infection was identified using Kato–Katz, 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 (−0.65; −0.78; −2.03 points for picture completion, RCPM, and block design, respectively; P < 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 (R = 0.22, P < 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.
Author Notes
Financial support: FORISCA study was funded by the U.S. Department of Agriculture (USDA) in collaboration with the World Food Program (WFP), IRD, and DSM consortium.
Authors' addresses: Khov Kuong and Chhoun Chamnan, Department of Fisheries Post-Harvest Technologies and Quality Control, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia, E-mails: kuong.kh@gmail.com and chhounchamnan@gmail.com. Marion Fiorentino, Marlene Perignon, Jacques Berger, and Frank T. Wieringa, Institut de Recherche pour le Développement, Montpellier, France, E-mails: marionfiorentino@hotmail.com, perignonmarlene@gmail.com, jacques.berger@ird.fr, and franck.wieringa@ird.fr. Muth Sinuon and Vann Molyden, National Center for Parasitology, Entomology and Malaria Control, Phnom Penh, Cambodia, E-mails: sinuonm@gmail.com and vannmolyden@gmail.com. Kurt Burja, United Nations World Food Program, Phnom Penh, Cambodia, E-mail: kurt.burja@wfp.org. Megan Parker, PATH, Seattle, WA, E-mail: mparker@path.org. Sou Chheng Ly, Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands, E-mail: souchheng.ly@gmail.com. Henrik Friis and Nanna Roos, Department of Nutrition, Exercise and Sports, University of Copenhagen, Denmark, E-mail: hfr@nexs.ku.dk and nro@nexs.ku.dk.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, Sachs JD, Savioli L, 2007. Control of neglected tropical diseases. N Engl J Med 357: 1018–1027.
-
2.
Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P, 2006. Disease Control Priorities in Developing Countries. Washington, DC: World Bank Publications.
-
3.
Evans DB, Guyatt HL, 1995. The cost effectiveness of mass drug therapy for intestinal helminths. Pharmacoeconomics 8: 14–22.
-
4.
Nokes C, Bundy D, 1994. Does helminth infection affect mental processing and educational achievement? Parasitol Today 10: 14–18.
-
5.
Savioli L, Bundy D, Tomkins A, 1992. Intestinal parasitic infections: a soluble public health problem. Trans R Soc Trop Med Hyg 86: 353–354.
-
6.
Simeon D, Callender J, Wong M, Grantham-McGregor S, Ramdath DD, 1994. School performance, nutritional status and trichuriasis in Jamaican schoolchildren. Acta Paediatr 83: 1188–1193.
-
7.
Crompton DWT, Nesheim M, 2002. Nutritional impact of intestinal helminthiasis during the human life cycle. Annu Rev Nutr 22: 35–59.
-
8.
Drake L, Jukes M, Sternberg R, Bundy D, 2000. Geohelminth infections (ascariasis, trichuriasis, and hookworm): cognitive and developmental impacts. Semin Pediatr Infect Dis 11: 245–251.
-
9.
Montresor A, Crompton D, Hall A, Bundy D, Savioli L, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva, Switzerland: World Health Organization, 1–48.
-
10.
Taylor-Robinson DC, Maayan N, Soares-Weiser K, Donegan S, Garner P, 2012. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin and school performance. Cochrane Database Syst Rev 7: CD000371.
-
11.
de Gier B, Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, van de Bor M, Ponce MC, Polman K, Wieringa FT, 2016. Species-specific associations between soil-transmitted helminths and micronutrients in Vietnamese schoolchildren. Am J Trop Med Hyg 95: 77–82.
-
12.
Hotez PJ, Ehrenberg JP, 2010. Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol 72: 31–53.
-
13.
World Health Organization (WHO), 2005. Deworming for Health and Development: Report of the Third Global Meeting of the Partners for Parasite Control. Geneva, Switzerland: WHO.
-
14.
MacLeod CL, 1988. Parasitic Infections in Pregnancy and the Newborn. New York, NY: Oxford University Press.
-
15.
Halterman JS, Kaczorowski JM, Aligne CA, Auinger P, Szilagyi PG, 2001. Iron deficiency and cognitive achievement among school-aged children and adolescents in the United States. Pediatrics 107: 1381–1386.
-
16.
Agaoglu L, Torun O, Unuvar E, Sefil Y, Demir D, 2007. Effects of iron deficiency anemia on cognitive function in children. Arzneimittel-Forschung-Drug Research 57: 426–430.
-
17.
Haas JD, Brownlie T, 2001. Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr 131: 676S–690S.
-
18.
Gray-Donald K, 2013. Iron supplementation for children: safety in all settings is not clear. CMAJ 185: 1477–1478.
-
19.
Ngui R, Lim YAL, Kin LC, Chuen CS, Jaffar S, 2012. Association between anaemia, iron deficiency anaemia, neglected parasitic infections and socioeconomic factors in rural children of west Malaysia. PLoS Negl Trop Dis 6: e1550.
-
20.
National Institute of Statistics, Directorate General for Health, ICF Macro, 2011. Cambodia Demographic and Health Survey 2010. Phnom Penh, Cambodia: National Institute of Statistics, Directorate General for Health, ICF Macro.
-
21.
Montresor A, Sinuon M, Tsuyuoka R, Chanthavisouk C, Strandgaard H, Velayudhan R, Capuano CM, Le Anh T, Dato AST, 2008. Large-scale preventive chemotherapy for the control of helminth infection in western Pacific countries: six years later. PLoS Negl Trop Dis 2: e278.
-
22.
CNM, 2004. Cambodia National Helminth Task-Force, Policy and Guideline. Phnom Penh, Cambodia: National Centre for Parasitology Entomology and Malaria Control.
-
23.
Cogill B, 2003. Anthropometric Indicators Measurement Guide. Washington, DC: Food and Nutrition Technical Assistance (FANTA) Project.
-
24.
World Health Organization (WHO), 1995. Physical Status: The Use and Interpretation of Anthropometry. Report of a WHO Expert Committee. Geneva, Switzerland: WHO.
-
25.
Kaplan R, Saccuzzo D, 2012. Psychological Testing: Principles, Applications, and Issues. Cengage Learning.
-
26.
Isaacs E, Oates J, 2008. Nutrition and cognition: assessing cognitive abilities in children and young people. Eur J Nutr 47: 4–24.
-
27.
Hughes D, Bryan J, 2003. The assessment of cognitive performance in children: considerations for detecting nutritional influences. Nutr Rev 61: 413–422.
-
28.
World Health Organization (WHO), 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control: A Guide for Programme Managers. Geneva, Switzerland: WHO.
-
29.
Mei Z, Cogswell ME, Parvanta I, Lynch S, Beard JL, Stoltzfus RJ, Grummer-Strawn LM, 2005. Hemoglobin and ferritin are currently the most efficient indicators of population response to iron interventions: an analysis of nine randomized controlled trials. J Nutr 135: 1974–1980.
-
30.
Zimmermann MB, Molinari L, Staubli-Asobayire F, Hess SY, Chaouki N, Adou P, Hurrell RF, 2005. Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children. Am J Clin Nutr 81: 615–623.
-
31.
George J, Yiannakis M, Main B, Devenish R, Anderson C, An US, Williams SM, Gibson RS, 2012. Genetic hemoglobin disorders, infection, and deficiencies of iron and vitamin A determine anemia in young Cambodian children. J Nutr 142: 781–787.
-
32.
Cook JD, Flowers CH, Skikne BS, 2003. The quantitative assessment of body iron. Blood 101: 3359–3364.
-
33.
Erhardt JG, Estes JE, Pfeiffer CM, Biesalski HK, Craft NE, 2004. 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. J Nutr 134: 3127–3132.
-
34.
Thurnham DI, McCabe LD, Haldar S, Wieringa FT, Northrop-Clewes CA, McCabe GP, 2010. Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: a meta-analysis. Am J Clin Nutr 92: 546–555.
-
35.
Zimmermann MB, Molinari L, Staubli-Asobayire F, Hess SY, Chaouki N, Adou P, Hurrell RF, 2005. Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children. Am J Clin Nutr 81: 615–623.
-
36.
Skikne BS, Flowers CH, Cook J, 1990. Serum transferrin receptor: a quantitative measure of tissue iron deficiency. Blood 75: 1870–1876.
-
37.
Zimmermann MB, Molinari L, Staubli-Asobayire F, Hess SY, Chaouki N, Adou P, Hurrell RF, 2005. Serum transferrin receptor and zinc protoporphyrin as indicators of iron status. Am J Clin Nutr 81: 615–623.
-
38.
Skikne BS, Flowers CH, Cook JD, 1990. Serum transferrin receptor: a quantitative measure of tissue iron deficiency. Blood 75: 1870–1876.
-
39.
Cook JD, Flowers CH, Skikne BS, 2003. The quantitative assessment of body iron. Blood 101: 3359–3363.
-
40.
De Pee S, Dary O, 2002. Biochemical indicators of vitamin A deficiency: serum retinol and serum retinol binding protein. J Nutr 132: 2895S–2901S.
-
41.
Thurnham DI, McCabe G, Northrop-Clewes C, Nestel P, 2003. Effects of subclinical infection on plasma retinol concentrations and assessment of prevalence of vitamin A deficiency: meta-analysis. Lancet 362: 2052–2058.
-
42.
Gibson RS, 2005. Principles of Nutritional Assessment. New York, NY: Oxford University Press.
-
43.
Brown KH, Rivera J, Bhutta Z, Gibson R, King J, Lönnerdal B, Ruel M, Sandtröm B, Wasantwisut E, Hotz C, 2004. International Zinc Nutrition Consultative Group (IZiNCG) technical document #1. Assessment of the risk of zinc deficiency in populations and options for its control. Food Nutr Bull 25: S99–S203.
-
44.
Srivorakun H, Fucharoen G, Sae-Ung N, Sanchaisuriya K, Ratanasiri T, Fucharoen S, 2009. Analysis of fetal blood using capillary electrophoresis system: a simple method for prenatal diagnosis of severe thalassemia diseases. Eur J Haematol 83: 57–65.
-
45.
World Health Organization (WHO), 1994. Bench Aids for the Diagnosis of Intestinal Parasites. Geneva, Switzerland: WHO.
-
46.
Soukhathammavong PA, Sayasone S, Phongluxa K, Xayaseng V, Utzinger J, Vounatsou P, Hatz C, Akkhavong K, Keiser J, Odermatt P, 2012. Low efficacy of single-dose albendazole and mebendazole against hookworm and effect on concomitant helminth infection in Lao PDR. PLoS Negl Trop Dis 6: e1417.
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