• 1.

    Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367: 15211532.

    • Search Google Scholar
    • Export Citation
  • 2.

    Ahmed T, Hossain M, Sanin KI, 2012. Global burden of maternal and child undernutrition and micronutrient deficiencies. Ann Nutr Metab 61 (Suppl 1): 817.

    • Search Google Scholar
    • Export Citation
  • 3.

    Ahmed A, Al-Mekhlafi HM, Al-Adhroey AH, Ithoi I, Abdulsalam AM, Surin J, 2012. The nutritional impacts of soil-transmitted helminths infections among Orang Asli schoolchildren in rural Malaysia. Parasit Vectors 5: 119.

    • Search Google Scholar
    • Export Citation
  • 4.

    Crompton DW, Nesheim MC, 2002. Nutritional impact of intestinal helminthiasis during the human life cycle. Annu Rev Nutr 22: 3559.

  • 5.

    de Gier B, Campos Ponce M, van de Bor M, Doak CM, Polman K, 2014. Helminth infections and micronutrients in school-age children: a systematic review and meta-analysis. Am J Clin Nutr 99: 14991509.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hall A, Hewitt G, Tuffrey V, de Silva N, 2008. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr 4 (Suppl 1): 118236.

    • Search Google Scholar
    • Export Citation
  • 7.

    Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, Wasantwisut E, Furr H, Wieringa FT, 2009. Multi-micronutrient-fortified biscuits decreased prevalence of anemia and improved micronutrient status and effectiveness of deworming in rural Vietnamese school children. J Nutr 139: 10131021.

    • Search Google Scholar
    • Export Citation
  • 8.

    Valentine AR, Tanumihardjo SA, 2004. Adjustments to the modified relative dose response (MRDR) test for assessment of vitamin A status minimize the blood volume used in piglets. J Nutr 134: 11861192.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gnat D, Dunn AD, Chaker S, Delange F, Vertongen F, Dunn JT, 2003. Fast colorimetric method for measuring urinary iodine. Clin Chem 49: 186188.

  • 10.

    de Pee S, Dary O, 2002. Biochemical indicators of vitamin A deficiency: serum retinol and serum retinol binding protein. J Nutr 132: 2895S2901S.

    • Search Google Scholar
    • Export Citation
  • 11.

    World Health Organization, 2001. Iron Deficiency Anaemia: Assessment, Prevention and Control: A Guide for Programme Managers. World Health Organization, ed. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 12.

    International Zinc Nutrition Consultative Group (IZiNCG), 2004. Assessment of the risk of zinc deficiency in populations and options for its control. Hotz C, Brown KH, eds. Food and Nutrition Bulletin. Tokyo, Japan: United Nations University Press.

    • Search Google Scholar
    • Export Citation
  • 13.

    Laurberg P, 2014. Iodine. Ross AC, Caballero B, Cousins RJ, Tucker KL, Ziegler TR, eds. Modern Nutrition in Health and Disease. Baltimore, MD: Lippincott Williams and Wilkins, 217224.

    • Search Google Scholar
    • Export Citation
  • 14.

    Thurnham DI, 2014. Interactions between nutrition and immune function: using inflammation biomarkers to interpret micronutrient status. Proc Nutr Soc 73: 18.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pal R, Sagar V, 2008. Antecedent risk factors of xerophthalmia among Indian rural preschool children. Eye Contact Lens 34: 106108.

  • 16.

    Curtale F, Pokhrel RP, Tilden RL, Higashi G, 1995. Intestinal helminths and xerophthalmia in Nepal. A case-control study. J Trop Pediatr 41: 334337.

    • Search Google Scholar
    • Export Citation
  • 17.

    Muniz-Junqueira MI, Queiroz EF, 2002. Relationship between protein-energy malnutrition, vitamin A, and parasitoses in living in Brasilia. Rev Soc Bras Med Trop 35: 133141.

    • Search Google Scholar
    • Export Citation
  • 18.

    Friis H, Mwaniki D, Omondi B, Muniu E, Magnussen P, Geissler W, Thiong'o F, Michaelsen KF, 1997. Serum retinol concentrations and Schistosoma mansoni, intestinal helminths, and malarial parasitemia: a cross-sectional study in Kenyan preschool and primary school children. Am J Clin Nutr 66: 665671.

    • Search Google Scholar
    • Export Citation
  • 19.

    Persson V, Ahmed F, Gebre-Medhin M, Greiner T, 2000. Relationships between vitamin A, iron status and helminthiasis in Bangladeshi school children. Public Health Nutr 3: 8389.

    • Search Google Scholar
    • Export Citation
  • 20.

    Kongsbak K, Wahed MA, Friis H, Thilsted SH, 2006. Acute-phase protein levels, diarrhoea, Trichuris trichiura and maternal education are predictors of serum retinol: a cross-sectional study of children in a Dhaka slum, Bangladesh. Br J Nutr 96: 725734.

    • Search Google Scholar
    • Export Citation
  • 21.

    Rai SK, Nakanishi M, Upadhyay MP, Hirai K, Ohno Y, Ono K, Uga S, Shrestha HG, Matsumura T, 2000. Effect of intestinal helminth infection on retinol and beta-carotene status among rural Nepalese. Nutr Res 20: 1523.

    • Search Google Scholar
    • Export Citation
  • 22.

    Taren DL, Nesheim MC, Crompton DWT, Holland CV, Barbeau I, Rivera G, Sanjur D, Tiffany J, Tucker K, 1987. Contributions of ascariasis to poor nutritional-status in children from Chiriqui Province, Republic of Panama. Parasitology 95: 603613.

    • Search Google Scholar
    • Export Citation
  • 23.

    Suchdev PS, Davis SM, Bartoces M, Ruth LJ, Worrell CM, Kanyi H, Odero K, Wiegand RE, Njenga SM, Montgomery JM, Fox LM, 2014. Soil-transmitted helminth infection and nutritional status among urban slum children in Kenya. Am J Trop Med Hyg 90: 299305.

    • Search Google Scholar
    • Export Citation
  • 24.

    Ross AC, 2014. Vitamin A. Ross AC, Caballero B, Cousins RJ, Tucker KL, Ziegler TR, eds. Modern Nutrition in Health and Disease. Baltimore, MD: Lippincott Williams and Wilkins.

    • Search Google Scholar
    • Export Citation
  • 25.

    Mahalanabis D, Simpson TW, Chakraborty ML, Ganguli C, Bhattacharjee AK, Mukherjee KL, 1979. Malabsorption of water miscible vitamin A in children with giardiasis and ascariasis. Am J Clin Nutr 32: 313318.

    • Search Google Scholar
    • Export Citation
  • 26.

    Tripathy K, Duque E, Bolanos O, Lotero H, Mayoral LG, 1972. Malabsorption syndrome in ascariasis. Am J Clin Nutr 25: 12761281.

  • 27.

    Ahmed F, Mohiduzzaman M, Jackson AA, 1993. Vitamin A absorption in children with ascariasis. Br J Nutr 69: 817825.

  • 28.

    McCullough FS, Northrop-Clewes CA, Thurnham DI, 1999. The effect of vitamin A on epithelial integrity. Proc Nutr Soc 58: 289293.

  • 29.

    Mora JR, Iwata M, von Andrian UH, 2008. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8: 685698.

  • 30.

    Payne LG, Koski KG, Ortega-Barria E, Scott ME, 2007. Benefit of vitamin A supplementation on Ascaris reinfection is less evident in stunted children. J Nutr 137: 14551459.

    • Search Google Scholar
    • Export Citation
  • 31.

    Al-Mekhlafi HM, Anuar TS, Al-Zabedi EM, Al-Maktari MT, Mahdy MA, Ahmed A, Sallam AA, Abdullah WA, Moktar N, Surin J, 2014. Does vitamin A supplementation protect schoolchildren from acquiring soil-transmitted helminthiasis? A randomized controlled trial. Parasit Vectors 7: 367.

    • Search Google Scholar
    • Export Citation
  • 32.

    Long KZ, Rosado JL, Montoya Y, de Lourdes Solano M, Hertzmark E, DuPont HL, Santos JI, 2007. Effect of vitamin A and zinc supplementation on gastrointestinal parasitic infections among Mexican children. Pediatrics 120: e846e855.

    • Search Google Scholar
    • Export Citation
  • 33.

    Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, Wasantwisut E, Wieringa FT, 2011. Decreased parasite load and improved cognitive outcomes caused by deworming and consumption of multi-micronutrient fortified biscuits in rural Vietnamese schoolchildren. Am J Trop Med Hyg 85: 333340.

    • Search Google Scholar
    • Export Citation
  • 34.

    Weinberg ED, 1975. Nutritional immunity. Host's attempt to withhold iron from microbial invaders. JAMA 231: 3941.

  • 35.

    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: 546555.

    • Search Google Scholar
    • Export Citation
  • 36.

    Balarajan Y, Ramakrishnan U, Ozaltin E, Shankar AH, Subramanian SV, 2011. Anaemia in low-income and middle-income countries. Lancet 378: 21232135.

  • 37.

    Finlay CM, Walsh KP, Mills KH, 2014. Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases. Immunol Rev 259: 206230.

    • Search Google Scholar
    • Export Citation
  • 38.

    Quihui-Cota L, Astiazaran-Garcia H, Valencia ME, Morales-Figueroa GG, Lopez-Mata MA, Vazquez Ortiz F, 2008. Impact of Giardia intestinalis on vitamin A status in schoolchildren from northwest Mexico. Int J Vitam Nutr Res 78: 5156.

    • Search Google Scholar
    • Export Citation
  • 39.

    Verhagen LM, Incani RN, Franco CR, Ugarte A, Cadenas Y, Sierra Ruiz CI, Hermans PW, Hoek D, Campos Ponce M, de Waard JH, Pinelli E, 2013. High malnutrition rate in Venezuelan Yanomami compared to Warao Amerindians and Creoles: significant associations with intestinal parasites and anemia. PLoS One 8: e77581.

    • Search Google Scholar
    • Export Citation
  • 40.

    Nikolay B, Brooker SJ, Pullan RL, 2014. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol 44: 765774.

    • Search Google Scholar
    • Export Citation
  • 41.

    Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J, 2008. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2: e331.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Species-Specific Associations Between Soil-Transmitted Helminths and Micronutrients in Vietnamese Schoolchildren

View More View Less
  • 1 Section Health and Life Sciences, Athena Institute, Vrije Universiteit (VU University), Amsterdam, The Netherlands.
  • | 2 National Institute of Nutrition, Hanoi, Vietnam.
  • | 3 Institute of Nutrition, Mahidol University, Salaya, Thailand.
  • | 4 Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark.
  • | 5 Ministry of Health, Hanoi, Vietnam.
  • | 6 Section Infectious Diseases, Department of Health Sciences, Vrije Universiteit (VU University), Amsterdam, The Netherlands.
  • | 7 Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.
  • | 8 UMR-204 NutriPass IRD-UM-SupAgro, Institut de Recherche pour le Développement, Montpellier, France.
Restricted access

Soil-transmitted helminth (STH) infections and micronutrient deficiencies are closely related and often coexist among low-income populations. We studied the association between infections with specific STH species and micronutrient status in rural Vietnamese schoolchildren. Children (N = 510) aged 6–9 years were recruited from two primary schools. STH infections were determined in stool samples. Hemoglobin, ferritin, retinol, and zinc were measured in blood samples, as well as C-reactive protein to control for inflammation. Iodine excretion was measured in urine. Associations of single and multiple infections with Ascaris lumbricoides, Trichuris trichiura, and hookworm with micronutrient status (hemoglobin, plasma ferritin, retinol, zinc, and urinary iodine) were estimated by multiple regression analysis. Ascaris infections showed a specific and intensity-dependent negative association with vitamin A. Trichuris and hookworm infections were associated with lower hemoglobin concentration, but not with plasma ferritin. Trichuris-infected children had zinc deficiency less often than uninfected children. In conclusion, our study shows species-specific associations between STH infections and micronutrient status in children. The different life cycles of STH species might have specific effects on the absorption or loss of specific micronutrients. Tailor-made combinations of deworming and nutritional interventions may be needed to improve child health and nutrition.

Author Notes

* Address correspondence to Frank T. Wieringa, UMR-204 Nutripass, IRD, 911 Avenue d'Agropolis, 34394 Montpellier, France. E-mail: franck.wieringa@ird.fr

Financial support: This study was supported by the Neys-van Hoogstraten Foundation, The Netherlands, and the Ellison Medical Foundation.

Authors' addresses: Brechje de Gier and Margot van de Bor, Department of Health and Life Sciences, Athena Institute, Vrije Universiteit (VU University) Amsterdam, The Netherlands, E-mails: b.de.gier@vu.nl and margot.vande.bor@vu.nl. Tran Thuy Nga, National Institute of Nutrition, Hanoi, Vietnam, E-mail: thuynga1997@gmail.com. Pattanee Winichagoon, Institute of Nutrition, Mahidol University, Salaya, Thailand, E-mail: pattanee.win@mahidol.ac.th. Marjoleine A. Dijkhuizen, Department of Nutrition, Exercise and Sports, University of Copenhagen, Copenhagen, Denmark, E-mail: madijkhuizen@gmail.com. Nguyen Cong Khan, Ministry of Health, Hanoi, Vietnam, E-mail: dr_nguyen_cong_khan@yahoo.com. Maiza Campos Ponce, Section Infectious Diseases, Department of Health Sciences, Vrije Universiteit (VU University) Amsterdam, The Netherlands, E-mail: m.camposponce@vu.nl. Katja Polman, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium and Department of Health Sciences, Vrije Universiteit (VU University) Amsterdam, The Netherlands, E-mail: kpolman@itg.be. Frank T. Wieringa, UMR-204 NutriPass IRD-UM-SupAgro, Institut de Recherche pour le Développement, Montpellier, France, E-mail: franck.wieringa@ird.fr.

Save