Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Communication
  • Published:

Vitamin A status and hemoglobin concentrations are improved in Indonesian children with vitamin A and deworming interventions

European Journal of Clinical Nutrition volume 58, pages 1223–1230 (2004)Cite this article

Abstract

Objective: Anemia is a major public health problem caused by multiple factors. Vitamin A (VA) depletion can affect hemoglobin concentration (Hb). This study investigated the improvement in Hb and VA status in preschool Indonesian children following supplementation with 210 μmol VA and deworming with 400 mg albendazole.

Subjects and design: Indonesian children (n=131) infected with Ascaris lumbricoides and/or Trichuris trichiura were enrolled. The children were grouped by length of time since receiving 210 μmol VA through the local health system. Group 1 (VA administered ≥4 month before baseline) included 51 children with Ascaris and 29 children with Trichuris. Group 2 had received VA ≤1 month of baseline from the local health post and included 51 children.

Intervention and methods: Immediately following baseline Hb and VA status assessment (modified relative dose response (MRDR) test), Group 1 children were given 210 μmol VA and 400 mg albendazole. Group 2 were randomized to be dewormed either 1 week before, at the same time or 1 week after baseline MRDR and Hb measures. Follow-up assessment was 3–4 weeks after baseline.

Results: VA status in Group 1 significantly improved in children with either Ascaris (P<0.0001) or Trichuris (P=0.028). Although the prevalence of anemia declined, the improvement in Hb was not significant (P=0.08). In Group 2, improvement in VA status from the VA delivered through the public health system was maintained for more than 1 month. Hb improved (P=0.0037) and this improvement appeared to be associated with the length of time between deworming and follow-up assessments.

Conclusion: Public health supplementation programs to improve VA status may also increase Hb concentrations and decrease anemia prevalence, especially when linked to deworming.

Sponsorship: These studies were supported by the Thrasher Research Fund, SmithKline Beecham and Hatch-Wisconsin Agricultural Experiment Station number WIS04533.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  • Ahmed F, Khan MR & Jackson AA (2001): Concomitant supplemental vitamin A enhances the response to weekly supplemental iron and folic acid in anemic teenagers in urban Bangladesh. Am. J. Clin. Nutr. 74, 108–115.

    Article  CAS  Google Scholar 

  • Ahmed F, Mohiduzzaman M & Jackson AA (1993): Vitamin A absorption in children with ascariasis. Br. J. Nutr. 69, 817–825.

    Article  CAS  Google Scholar 

  • Anderson TJ, Zizza CA, Leche GM, Scott ME & Solomons NW (1993): The distribution of intestinal helminth infections in a rural village in Guatemala. Memorias do Instit. Oswaldo Cruz. 88, 53–65.

    Article  CAS  Google Scholar 

  • Barua AB & Ghosh MC (1972): Preparation and properties of 4-oxo-retinoic acid and its methylester. Tetrahedron Lett. 18, 1823–1825.

    Article  Google Scholar 

  • Chandiwana SK, Bradley M & Chombo F (1989): Hookworm and roundworm infections in farm-worker communities in the large-scale agricultural sector in Zimbabwe. J. Trop. Med. Hyg. 92, 338–344.

    CAS  PubMed  Google Scholar 

  • Curtale F, Tilden R, Muhilal, Vaidya Y, Pokhrel RP & Guerra R (1993): Intestinal helminths and risk of anaemia among Nepalese children. Panminerva Med. 35, 159–166.

    CAS  PubMed  Google Scholar 

  • Filteau SM (1999): Vitamin A and the acute-phase response. Nutrition 15, 326–328.

    Article  CAS  Google Scholar 

  • Harding JE (2001): The nutritional basis of the fetal origins of adult disease. Int. J. Epidemiol. 30, 145–153.

    Article  Google Scholar 

  • Jang JT, Green JB, Beard JL & Green MH (2000): Kinetic analysis shows that iron deficiency decreases liver vitamin A mobilization in rats. J. Nutr. 130, 1291–1296.

    Article  CAS  Google Scholar 

  • Kasuya S, Khamboonruang C, Amano K, Murase T, Araki H, Kato Y, Kumada Y, Koyama A, Higuchi M, Nakamura J, Tomida K & Makino S (1989): Intestinal parasitic infections among schoolchildren in Chiang Mai, northern Thailand: an analysis of the present situation. J. Trop. Med. Hyg. 92, 360–364.

    CAS  PubMed  Google Scholar 

  • Kato K & Miura M (1954): Comparative examinations. Jpn. J. Parasitol. 3, 35.

    Google Scholar 

  • Layrisse M, Aparcedo L, Martinez-Torres C & Roche M (1967): Blood loss due to infection with Trichuris trichiura. Am. J. Trop. Med. Hyg. 16, 613–619.

    Article  CAS  Google Scholar 

  • Mahalanabis D, Halan KN, Maitra TK & Agarawal SK (1976): Vitamin A absorption in ascariasis. Am. J. Clin. Nutr. 29, 1372–1375.

    Article  CAS  Google Scholar 

  • Martin LK & Beaver PC (1968): Evaluation of Kato thick smear technique for quantitative diagnosis of helminth infections. Am. J. Trop. Med. Hyg. 17, 382–391.

    Article  CAS  Google Scholar 

  • Molla A, Khurshid M, Molla AM, Badruddin SH, Hendricks K & Snyder JD (1993): Is anemia an accurate predictor of vitamin A status in Pakistani children? Am. J. Trop. Med. Hyg. 49, 276–279.

    Article  CAS  Google Scholar 

  • Muslimatun S, Schmidt MK, Schultink W, West CE, Hautvast JGAJ, Gross R & Muhilal (2001): Weekly supplementation with iron and vitamin A during pregnancy increases hemoglobin concentration but decreases serum ferritin concentration in Indonesian pregnant women. J. Nutr. 131, 85–90.

    Article  CAS  Google Scholar 

  • Nesheim MC (1993): Human nutrition needs and parasitic infections. Parasitology 107, S7–S18.

    Article  Google Scholar 

  • 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, 83–89.

    Article  CAS  Google Scholar 

  • Rosales FJ, Jang JT, Pinero DJ, Erikson KM, Beard JL & Ross AC (1999): Iron deficiency in young rats alters the distribution of vitamin A between plasma and liver and between hepatic retinol and retinyl esters. J. Nutr. 129, 1223–1228.

    Article  CAS  Google Scholar 

  • Schultz MG (1981): Ascariasis: nutritional implications. Rev. Infect. Diseases 4, 815–819.

    Article  Google Scholar 

  • Sebastian VJ, Bhattacharya S & Ray S (1989): Mebendazole retention enema for severe Trichuris trichiura (whipworm) infection: a case report. J. Trop. Med. Hyg. 92, 39–40.

    CAS  PubMed  Google Scholar 

  • Semba RD & Bloem MW (2002): The anemia of vitamin A deficiency: epidemiology and pathogenesis. Eur. J. Clin. Nutr. 56, 271–281.

    Article  CAS  Google Scholar 

  • Semba RD, Kumwenda N, Taha TE, Mtimavalye L, Broadhead R, Garrett E, Miotti PG & Chiphangwi JD (2001): Impact of vitamin A supplementation on anaemia and plasma erythropoietin concentrations in pregnant women: a controlled clinical trial. Eur. J. Haematol. 66, 389–395.

    Article  CAS  Google Scholar 

  • Sivakumar B & Reddy V (1975): Absorption of vitamin A in children with ascariasis. Am. J. Trop. Med. Hyg. 78, 114–115.

    CAS  Google Scholar 

  • Solomons NW & Keusch GT (1981): Nutritional implications of parasitic infections. Nutr. Rev. 39, 149–161.

    Article  CAS  Google Scholar 

  • Stanton B, Silimperi DR, Khatun K, Kay B, Ahmed S, Khatun J & Alam K (1989): Parasitic, bacterial and viral pathogens isolated from diarrhoeal and routine stool specimens of urban Bangladeshi children. J. Trop. Med. Hyg. 92, 46–55.

    CAS  PubMed  Google Scholar 

  • Stephensen CB (2001): Vitamin A, infection, and immune function. Ann. Rev. Nutr. 21, 167–192.

    Article  CAS  Google Scholar 

  • Stephensen CB, Franchi LM, Hernandez H, Campos M, Colarossi A, Gilman RH & Alvarez JO (2002): Assessment of vitamin A status with the relative-dose–response test in Peruvian children recovering from pneumonia. Am. J. Clin. Nutr. 76, 1351–1357.

    Article  CAS  Google Scholar 

  • Stephenson LS, Holland CV & Cooper ES (2000): The public health significance of Trichuris trichiura. Parasitology 121, S73–95.

    Article  Google Scholar 

  • Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ & Savioli L (1998): Effects of the Zanzibar school-based deworming program on iron status of children. Am. J. Clin. Nutr. 68, 179–186.

    Article  CAS  Google Scholar 

  • Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M & Savioli L (1997): Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. Am. J. Clin. Nutr. 65, 153–159.

    Article  CAS  Google Scholar 

  • Suharno D, West CE, Muhilal Karyadi D & Hautvast JGAJ (1993): Supplementation with vitamin A and iron for nutritional anaemia in pregnant women in West Java, Indonesia. Lancet 342, 1325–1328.

    Article  CAS  Google Scholar 

  • Tanumihardjo SA (2000): Vitamin A status assessment in rats using 13C4-retinyl acetate and gas chromatography-combustion isotope ratio mass spectrometry (GCCIRMS). J. Nutr. 130, 2844–2849.

    Article  CAS  Google Scholar 

  • Tanumihardjo SA (2001): Can lack of improvement in vitamin A status indicators be explained by little or no overall change in vitamin A status of humans? J. Nutr. 131, 3316–3318.

    Article  CAS  Google Scholar 

  • Tanumihardjo SA (2002): Vitamin A and iron status are improved with vitamin A and iron supplementation in pregnant Indonesian women. J. Nutr. 132, 1909–1912.

    Article  CAS  Google Scholar 

  • Tanumihardjo SA, Barua AB & Olson JA (1987): Use of 3,4-didehydroretinol to assess vitamin A status in rats. Int. J. Vitam. Nutr. Res. 57, 127–132.

    CAS  PubMed  Google Scholar 

  • Tanumihardjo SA, Cheng JC, Permaesih D, Muherdiyantiningsih, Rustan E, Muhilal, Karyadi D & Olson JA (1996a): Refinement of the modified-relative-dose–response test as a method for assessing vitamin A status in a field setting: experience with Indonesian children. Am. J. Clin. Nutr. 64, 966–971.

    Article  CAS  Google Scholar 

  • Tanumihardjo SA, Permaesih D, Muherdiyantiningsih, Rustan E, Rusmil K, Fatah AC, Wilbur S, Muhilal, Karyadi D & Olson JA (1996b): Vitamin A status of Indonesian children infected with Ascaris lumbricoides after dosing with vitamin A supplements and albendazole. J. Nutr. 126, 451–457.

    Article  CAS  Google Scholar 

  • Thein-Hlaing, Thane-Toe, Than-Saw, Myat-Lay-Kyin & Myint-Lwin (1991): A controlled chemotherapeutic intervention trial on the relationship between Ascaris lumbricoides infection and malnutrition in children. Trans. R. Soc. Trop. Med. Hyg. 85, 523–528.

    Article  CAS  Google Scholar 

  • Tripathy K, Duque E, Bolanos O, Lotero H & Mayoral LG (1972): Malabsorption syndrome in ascariasis. Am. J. Clin. Nutr. 25, 1276–1281.

    Article  CAS  Google Scholar 

  • Wieringa FT, Dijkhuizen MA, West CE, Northrop-Clewes CA & Muhilal (2002): Estimation of the effect of the acute phase response on indicators of micronutrient status in Indonesian infants. J. Nutr. 132, 3061–3066.

    Article  CAS  Google Scholar 

  • Willumsen JF, Simmank W, Filteau SM, Wagstaff LA & Tomkins AM (1997): Toxic damage to the respiratory epithelium induces acute phase changes in vitamin A metabolism without depleting retinol stores of South African children. J. Nutr. 127, 1339–1343.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This paper was invited as a poster at the 2003 International Nutritional Anemia Consultative Group (INACG) meeting in Marrakech, Morocco entitled, ‘Hemoglobin concentrations are increased in Indonesian children with vitamin A and deworming interventions,’ Tanumihardjo, SA, Permaesih D, Muhilal. This work was done in conjunction with the dedicated staff of the Nutrition Research and Development Center in Bogor, Indonesia, while SA Tanumihardjo was a visiting scientist. We thank Ashley Valentine, graduate student in Nutritional Sciences, UW-Madison, and Penny Nestel, from the USAID's Micronutrient Global Leadership project, for their helpful comments on the manuscript, and Peter Crump, Senior Information Processing Consultant at University of Wisconsin-Madison, for his help in the statistical analysis of the data.

Author information

Authors and Affiliations

  1. Department of Nutritional Sciences, UW-Madison, Madison, WI, USA

    S A Tanumihardjo

  2. Research and Development Center, Bogor, Indonesia

    D Permaesih &  Muhilal

Authors
  1. S A Tanumihardjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D Permaesih
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhilal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Guarantor: SAT.

Contributors: SAT designed the study, analyzed the samples and wrote the manuscript. DP coordinated all field staff, administered 3, 4-didehydroretinyl acetate to the children and checked accuracy and completeness of clinic charts. Muhilal oversaw the day-to-day operations of the laboratory. Muhilal and SAT worked together in Indonesia with Helen Keller International to secure grant funds.

Corresponding author

Correspondence to S A Tanumihardjo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tanumihardjo, S., Permaesih, D. & Muhilal Vitamin A status and hemoglobin concentrations are improved in Indonesian children with vitamin A and deworming interventions. Eur J Clin Nutr 58, 1223–1230 (2004). https://doi.org/10.1038/sj.ejcn.1601953

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ejcn.1601953

Keywords

This article is cited by

Search

Advanced search

Quick links