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:

Change in body water distribution index in infants who become stunted between 4 and 18 months of age

European Journal of Clinical Nutrition volume 57, pages 1097–1106 (2003)Cite this article

Abstract

Objective: To evaluate body composition changes using bioelectrical impedance analysis and skinfold thickness measurements in infants from tropical areas who become stunted between 4–18 months of age.

Design and measurements: Follow-up study. Extracellular water to total body water ratio index (length2/resistance at low to high frequency), peripheral fat (tricipital and subscapular skinfold thickness), and length-for-age index were studied at 4 and 18 months of age.

Setting: Low-income areas in four tropical regions (Congo, Senegal, Bolivia and New Caledonia).

Subjects: Infants were included in the analysis provided they were neither stunted nor wasted at 4 months. Two groups of infants were compared, those that were stunted at 18 months (n=61) or not (n=170).

Results: The extracellular water to total body water ratio index and the sum of skinfold thickness measurements were similar in the two groups at 4 months, and only the extracellular water to total body water ratio index was significantly different at 18 months. When no stunting appeared between 4 and 18 months, the change in the extracellular water to total body water ratio index was not linked with variations in length-for-age, and presented the expected pattern of variation in body water compartments. When stunting occurred, variation in length-for-age was related to significant changes in the extracellular water to total body water ratio index, the biggest increase in the proportion of extracellular water being found in the most stunted infants. Variations in the sum of the two skinfold thickness measurements presented the expected pattern for the 4–18 months growth and did not differ between the two groups.

Conclusions: Multifrequency resistances suggested that stunting was associated with a lack of the expansion of the intracellular compartment that is expected during normal growth of cell mass, together with preserved fat mass.

Sponsorship: Supported by grant 92L0623 from the French Ministry of Research, and by Institut de Recherche pour le Développement (IRD).

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

Similar content being viewed by others

References

  • Allen LH (1994): Nutritional influences on linear growth: a general review. Eur. J. Clin. Nutr. 48(Suppl 1), S75–S89.

    PubMed  Google Scholar 

  • Barker DJP (1998): Mothers, Babies and Health in Later Life, 2nd edition, Edinburgh: Churchill Livingstone.

    Google Scholar 

  • Benefice E (1992): Physical activity and anthropometric and functional characteristics of mildly malnourished Senegalese children. Ann. Trop. Paediatr. 12, 55–66.

    Article  CAS  Google Scholar 

  • Berkman DS, Lescano AG, Gilman RH, Lopez SL & Black MM (2002): Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet 359, 564–571.

    Article  Google Scholar 

  • Bioelectrical Impedance Analysis in Body Composition Measurement (2000): NIH Technol Assess Statement Online 1994 December 12–14; 2000 May 19; http://text.nlm.nih.gov/nih/ta/www/15.html.

  • Bouhaddioui L, Brun JF, Jacquemin JL, Bailly A, Bouhaddioui N, Kabbaj K & Orsetti A (1989): Immunoreactive somatomedine C in children from Morocco: a biological marker of nutritional growth retardation? Biomed. Pharmacother. 43, 59–63.

    Article  CAS  Google Scholar 

  • Boutton TW, Trowbridge FL, Nelson MM, Wills CA, Smith EO, Lopez de Romana G, Madrid S, Marks JS & Klein PD (1987): Body composition of Peruvian children with short stature and high weight-for-height. I. Total body-water measurements and their prediction from anthropometric values. Am. J. Clin. Nutr. 45, 13–25.

    Article  Google Scholar 

  • Butte NF, Hopkinson JM, Wong WW, O'Brian Smith E & Ellis KJ (2000): Body composition during the first 2 years of life: an updated reference. Pediatr. Res. 47, 578–585.

    Article  CAS  Google Scholar 

  • Cheek DB, McIntosh GH, O'Brien V, Ness D & Green RC (1989): Malnutrition in aboriginal children at Yalata, South Australia. Eur. J. Clin. Nutr. 43, 161–168.

    CAS  PubMed  Google Scholar 

  • Cutfield WS, Hofman PL, Vickers M, Breier B, Blum WF & Robinson EM (2002): IGFs and binding proteins in short children with intrauterine growth retardation. J. Clin. Endocrinol. Metab. 87, 235–239.

    Article  CAS  Google Scholar 

  • Deurenberg P, Tagliabue A & Schouten FJM (1995): Multi-frequency impedance for the prediction of extracellular water and total body water. Br. J. Nutr. 73, 349–358.

    Article  CAS  Google Scholar 

  • Fjeld C, Freundt-Thurne J & Schoeller DA (1990): Total body water measured by 18O dilution and bioelectrical impedance in well and malnourished children. Pediatr. Res. 27, 98–102.

    Article  CAS  Google Scholar 

  • Flyvbjerg A, Dorup I, Everts ME & Orskov H (1991): Evidence that potassium deficiency induces growth retardation through reduced circulating levels of growth hormone and insuline-like growth factor I. Metabolism 40, 769–775.

    Article  CAS  Google Scholar 

  • Forbes GB (1988): Body composition: influence of nutrition, disease, growth and aging. In Modern Nutrition in Health and Disease, ME Shils & VR Young (eds), Philidelphia: Lea & Febiger, pp 533–556.

    Google Scholar 

  • Gartner A, Maire B, Delpeuch F, Sarda P, Dupuy RP & Rieu D (1992): Importance of electrode position in bioelectrical impedance analysis. Am. J. Clin. Nutr. 56, 1067–1068.

    Article  CAS  Google Scholar 

  • Gartner A, Sarda P, Dupuy RP, Maire B, Delpeuch F & Rieu D (1994): Bioelectrical impedance analysis in small- and appropriate-for-gestational-age newborn infants. Eur. J. Clin. Nutr. 48, 425–432.

    CAS  PubMed  Google Scholar 

  • Gaskin PS, Walker SP, Forrester TE & Grantham-McGregor S (2000). Early linear growth retardation and later blood pressure. Eur. J. Clin. Nutr. 54, 563–567.

    Article  CAS  Google Scholar 

  • Golden MH (1991): The nature of nutritional deficiency in relation to growth failure and poverty. Acta Paediatr. Scand. 374(Suppl), 95–110.

    Article  CAS  Google Scholar 

  • Grazioso C, Molina S, Santizo MC, Mazariegos M, Siu ML, Vettorazzi C & Solomons NW (1990): Anthropometry and bioelectrical impedance analysis in newborns with intrauterine retardation. In Advances in in vivo Body Composition Studies, S Yasumura, JE Harrison, KG McNeil, AD Woodhead & FA Dilmanian (eds) New York: Plenum Press. pp 51–54.

    Chapter  Google Scholar 

  • Hansen JDL, Brinkman GL & Bowie MD (1965): Body composition in protein-calorie malnutrition. S. Afr. Med. J. 39, 491–495.

    CAS  PubMed  Google Scholar 

  • Hoffman DJ, Sawaya AL, Verreschi I, Tucker KL & Roberts SB (2000): Why are nutritionally stunted children at increased risk of obesity? Studies of metabolic rate and fat oxidation in shantytown children from Sao Paulo, Brazil. Am. J. Clin. Nutr. 72, 702–707.

    Article  CAS  Google Scholar 

  • Houtkooper LB, Lohman TG, Going SB & Hall MC (1989): Validity of bioelectrical impedance for body composition assessment in children. J. Appl. Physiol. 66, 814–822.

    Article  CAS  Google Scholar 

  • Kabir I, Malek MA, Rahman MM, Khaled MA & Mahalanabis D (1994): Changes in body composition of malnourished children after dietary supplementation as measured by bioelectrical impedance. Am. J. Clin. Nutr. 59, 5–9.

    Article  CAS  Google Scholar 

  • Karlberg J, Jalil F, lam B, Low L & Yeung CY (1994): Linear growth retardation in relation to the three phases of growth. Eur. J. Clin. Nutr. 48(Suppl 1), S25–S44.

    PubMed  Google Scholar 

  • Kossmann J, Nestel P, Herrera MG, El-Amin A & Fawzi WW (2000): Undernutrition and childhood infections: a prospective study of childhood infections in relation to growth in the Sudan. Acta Paediatr. 89, 1122–1128.

    Article  CAS  Google Scholar 

  • Kushner RF & Schoeller DA (1986): Estimation of total body water by bioelectrical impedance analysis. Am. J. Clin. Nutr. 44, 417–424.

    Article  CAS  Google Scholar 

  • Lukaski HC, Johnson PE, Bolonchuk WW & Lykken GE (1985): Assessment of fat free mass using bioelectrical impedance measurements of the human body. Am. J. Clin. Nutr. 41, 810–817.

    Article  CAS  Google Scholar 

  • Lunn PG (2000): The impact of infection and nutrition on gut function and growth in childhood. Proc. Nutr. Soc. 59, 147–154.

    Article  CAS  Google Scholar 

  • Lusseveld EM, Peters ETJ & Deurenberg P (1993): Multifrequency bioelectrical impedance as a measure of differences in body water distribution. Ann. Nutr. Metab. 37, 44–51.

    Article  CAS  Google Scholar 

  • Mayfield SR, Uauy R & Waidelich D (1991): Body composition of low-birth-weight infants determined by using bioelectrical resistance and reactance. Am. J. Clin. Nutr. 54, 296–303.

    Article  CAS  Google Scholar 

  • Mendez MA & Adair LS (1999): Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J. Nutr. 129, 1555–1562.

    Article  CAS  Google Scholar 

  • Molina S, Arango T, Pineda O & Solomons NW (1987): Response of bioelectrical impedance analysis (BIA) indices to rehydration therapy in severe infantile diarrhea. Am. J. Clin. Nutr. 45, 837 (abstract).

    Google Scholar 

  • Nair RH, Kesavachandran C & Shashidhar S (1999): Spirometric impairments in undernourished children. Indian J. Physiol. Pharmacol. 43, 467–473.

    CAS  PubMed  Google Scholar 

  • Neumann CG & Harrison GG (1994): Onset and evolution of stunting in infants and children. Examples from the Human Nutrition Collaborative Research Support Program. Kenya and Egypt studies. Eur. J. Clin. Nutr. 48(Suppl 1), S90–S102.

    PubMed  Google Scholar 

  • Ogle GD, Rosenberg AR & Kainer G (1992): Renal effects of growth hormone. II. Electrolyte homeostasis and body composition. Pediatr. Nephrol. 6, 483–489.

    Article  CAS  Google Scholar 

  • Pencharz PB & Azcue M (1996): Use of bioelectrical impedance analysis measurements in the clinical management of malnutrition. Am. J. Clin. Nutr. 64(Suppl), 485S–488S.

    Article  CAS  Google Scholar 

  • Quirk PC, Ward LC, Thomas BJ, Holt TL, Shepherd RW & Cornish BH (1997): Evaluation of bioelectrical impedance for prospective nutritional assessment in cystic fibrosis. Nutrition 13, 412–415.

    Article  CAS  Google Scholar 

  • Randall HT (1988): Water, electrolytes and acid-base balance. In Modern Nutrition in Health and Disease, ME Shils & VR Young (eds). Philidelphia: Lea & Febiger. pp 108–141.

    Google Scholar 

  • Roth HP & Kirchgessner M (1994): Influence of alimentary zinc deficiency on the concentration of growth hormone (GH), insuline-like growth factor-I (IGF-1) and insulin in the serum of force-fed rats. Horm. Metab. Res. 26, 404–408.

    Article  CAS  Google Scholar 

  • Sawaya AL, Grillo LP, Verreschi I, da Silva AC & Roberts SB (1998): Mild stunting is associated with higher susceptibility to the effects of high-fat diets: studies in a shantytown population in Sao Paulo, Brazil. J. Nutr. 128(Suppl), 415S–420S.

    Article  CAS  Google Scholar 

  • Segal KR, Gutin B, Presta E, Wang J & van Itallie TB (1985): Estimation of human body composition by electrical impedance methods: a comparative study. J. Appl. Physiol. 58, 1565–1571.

    Article  CAS  Google Scholar 

  • Shetty PS (1999): Adaptation to low energy intakes: the responses and limits to low intakes in infants, children and adults. Eur. J. Clin. Nutr. 53(Suppl 1), S14–S33.

    Article  Google Scholar 

  • Simondon KS, Gartner A, Berger J, Cornu A, Massamba JP, San Miguel JL, Ly C, Missotte I, Simondon F, Traissac P, Delpeuch F & Maire B (1996): Effect of early, short-term supplementation on weight and linear growth of 4–7-mo-old infants in developing countries: a four-country randomized trial. Am. J. Clin. Nutr. 64, 537–545.

    Article  CAS  Google Scholar 

  • Smith DN (1993): Bioelectrical impedance index and body composition. Lancet 341, 569–570.

    Article  CAS  Google Scholar 

  • Soares-Wynter SY & Walker SP (1996): Resting metabolic rate and body composition in stunted and nonstunted children. Am. J. Clin. Nutr. 64, 137–141.

    Article  CAS  Google Scholar 

  • Spurr GB, Reina JC & Barac-Nieto M (1986): Marginal malnutrition in school-aged Colombian boys: metabolic rate and estimated daily energy expenditure. Am. J. Clin. Nutr. 44, 113–126.

    Article  CAS  Google Scholar 

  • Underwood L, Smith EP, Clemmons DR, Maes M, Maiter D & Ketelslegens JM (1989): The production and actions of insuline-like growth factors: their relationship to nutrition and growth. In Auxology 88. Perspectives in the Science of Growth and Development, JM Tanner (ed). London: Smith & Gordon. pp 235–249.

  • VanderJagt DJ, Okolo SN, Rabasa AI & Glew RH (2000): Bioelectrical impedance analysis of the body composition of Nigerian children with sickle cell disease. J. Trop. Pediatr. 46, 67–72.

    Article  CAS  Google Scholar 

  • Vettorazzi C, Molina S, Grazioso C, Mazariegos M, Siu ML & Solomons NW (1990): Bioelectrical impedance analysis in protein-energy malnourished children as an indicator of total body water status. In Advances in in vivo Body Composition Studies, S Yasumura, JE Harrison, KG McNeil, AD Woodhead & FA Dilmanian (eds). New York: Plenum Press. pp 45–49.

    Chapter  Google Scholar 

  • Vettorazzi C, Smits E & Solomons NW (1994): The interobserver reproducibility of bioelectrical impedance analysis measurements in infants and toddlers. J. Pediatr. Gastroenterol. Nutr. 19, 277–282.

    Article  CAS  Google Scholar 

  • Wahlqvist M & Marks S (1990): A clinical approach to body composition in wasting. Basic Life Sci. 55, 133–142.

    CAS  PubMed  Google Scholar 

  • Walker SP, Grantham-McGregor S, Powell C, Fletcher P & Himes JH (1990): Bioelectrical impedance, anthropometry and body composition in stunted and non-stunted children. Eur. J. Clin. Nutr. 44, 763–768.

    CAS  PubMed  Google Scholar 

  • Walker SP, Walker SP, Gaskin PS, Powell CA & Bennett FI (2002): The effects of birth weight and postnatal linear growth retardation on body mass index, fatness and fat distribution in mid and late childhood. Publ. Health Nutr. 5, 391–397.

    Article  Google Scholar 

  • Wang Z, Deurenberg P & Heymsfield SB (2000): Cellular-level body composition model: a new approach to studying fat-free mass hydration. Ann. N. Y. Acad. Sci. 904, 306–311.

    Article  CAS  Google Scholar 

  • Waterland RA & Garza C (1999): Potential mechanisms of metabolic imprinting that lead to chronic disease. Am. J. Clin. Nutr. 69, 179–197.

    Article  CAS  Google Scholar 

  • Waterlow JC (1986): Mechanisms of adaptation to low protein and energy intakes. Annu. Rev. Nutr. 6, 495–526.

    Article  CAS  Google Scholar 

  • Waterlow JC, Tomkins AM & Grantham-McGregor SM (1992): Protein-Energy Malnutrition. London: Edward Arnold.

    Google Scholar 

  • Waterlow JC (1988): Observations on the natural history of stunting. In Linear growth retardation in less developed countries, JC Waterlow (ed). New York: Raven Press. pp 1–16.

    Google Scholar 

  • Waterlow JC (1994): Summary of causes and mechanisms of linear growth retardation. Eur. J. Clin. Nutr. 48(Suppl 1), S210.

    Google Scholar 

  • WHO (1983): Measuring Change in Nutritional Status: Guidelines For Assessing The Nutritional Impact of Supplementary Feeding Programs. Geneva: World Health Organization.

  • Wren RE, Blume H, Mazariegos M, Solomons N, Alvarez JO & Goran MI (1997): Body composition, resting metabolic rate, and energy requirements of short- and normal-stature, low-income Guatemalan children. Am. J. Clin. Nutr. 66, 406–412.

    Article  CAS  Google Scholar 

  • Zverev Y (2001): Prediction of peak expiratory flow rates in stunted children. Cent. Afr. J. Med. 47, 74–78.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Rozenn Nicolas and Jean-Pierre Massamba for their participation in the Congolese setting, Aldiouma Diallo for medical care of ill infants in the Senegalese setting, Wilma Tellez, Carmen Lujan and Myriam Perez for their help in Bolivia, and Isabelle Missotte for her help in the New Caledonia study

Author information

Authors and Affiliations

  1. Nutrition, Food, Societies Unit, Institut de Recherche pour le Développement (IRD), WHO Collaborating Centre for Nutrition, Montpellier, France

    A Gartner, J Berger, B Maire, P Traissac & F Delpeuch

  2. Epidemiology and Prevention Unit, Institut de Recherche pour le Développement (IRD), Montpellier, France

    K B Simondon & F Simondon

  3. Organisme de Recherche sur l'Alimentation et la Nutrition Africaines, (ORANA), Dakar, Sénégal

    C Ly

  4. Instituto Boliviano de Biologia de Altura, IBBA La Paz, Bolivia

    J L San Miguel

Authors
  1. A Gartner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J Berger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K B Simondon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B Maire
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P Traissac
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C Ly
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J L San Miguel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. F Simondon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. F Delpeuch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Contributors: B Maire (Guarantor) and F Delpeuch initiated the study and contributed to writing the manuscript. A Gartner (Guarantor) was in charge of the study in Congo. J Berger and JL San Miguel were in charge of the study in Bolivia. C Ly, F Simondon and KB Simondon were in charge of the study in Senegal. A Gartner and P Traissac were responsible for data management and analysis, and contributed to writing the manuscript.

Corresponding author

Correspondence to A Gartner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gartner, A., Berger, J., Simondon, K. et al. Change in body water distribution index in infants who become stunted between 4 and 18 months of age. Eur J Clin Nutr 57, 1097–1106 (2003). https://doi.org/10.1038/sj.ejcn.1601649

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.ejcn.1601649

Keywords

Search

Advanced search

Quick links