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Nutrition during the early life cycle

Free living total energy expenditure in young South Indian children at risk of environmental enteric dysfunction and its relation to faltered linear growth



Chronic immune activation in Environmental Enteric Dysfunction (EED) could lead to increased fed-state metabolic rate (MR) or total energy expenditure (TEE) and limit the energy available for optimal linear growth. In a secondary analysis, MR and TEE were compared in young Indian children from urban slums, with and without stunting or EED.


Children (18–24 months, n = 69) were classified into non-stunted (LAZ ≥ −2) and stunted (LAZ < −2), and no-EED (lactulose rhamnose ratio, LRR < 0.068) and EED (LRR ≥ 0.068) groups. Associations between MR and TEE (kcal per kg bodyweight [BW] or fat free mass [FFM]) with stunting and EED were examined using logistic regression.


Median TEE was significantly higher in the stunted compared to non-stunted group (76.8 versus 92.0 kcal/kg BW/day, p = <0.01). The adjusted (for sex, FFM, EED) odds ratio (AOR) for stunting with TEE (kcal/day) was 1.01 (95% CI: 1.00, 1.01), but importantly, there was no interaction between EED and TEE. The median TEE was also significantly higher in the EED compared to the no-EED group (89.1 vs 76.8 kcal/kg BW/day, p = 0.02), and the AOR (adjusted for sex and TEE) for stunting with EED was 3.56 (95% CI:1.09, 11.63). MR (per kg BW or FFM) was not associated with stunting or EED.


Higher TEE and presence of EED were independently and positively associated with stunting. Children with EED also had higher TEE but not MR. Energetically, the higher TEE in stunted children may not specifically be linked to the presence of EED, although the latter independently had higher odds of stunting.

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Fig. 1: The association of length-for-age z-score and total energy expenditure (as kcal/kg BW/day) by EED categories.

Data availability

Data analyzed for this study are available from the corresponding author on reasonable request.


  1. Millward DJ. Nutrition, infection and stunting: the roles of deficiencies of individual nutrients and foods, and of inflammation, as determinants of reduced linear growth of children. Nut Res Rev. 2017;30:50–72.

    Article  CAS  Google Scholar 

  2. Watanabe K, Petri WA Jr. Environmental enteropathy: elusive but significant subclinical abnormalities in developing countries. EBioMedicine. 2016;10:25–32.

    Article  Google Scholar 

  3. Straub RH. The brain and immune system prompt energy shortage in chronic inflammation and ageing. Nat Rev Rheumatol. 2017;13:743–51.

    Article  CAS  Google Scholar 

  4. Urlacher SS, Ellison PT, Sugiyama LS, Pontzer H, Eick G, Liebert MA, et al. Trade-offs between immune function and childhood growth among Amazonian forager-horticulturalists. PNAS. 2018;115:E3914–21.

    Article  CAS  Google Scholar 

  5. Urlacher SS, Snodgrass JJ, Dugas LR, Sugiyama LS, Liebert MA, Joyce CJ, et al. Constraint and trade-offs regulate energy expenditure during childhood. Sci Adv. 2019;5:eaax1065.

    Article  CAS  Google Scholar 

  6. Urlacher SS, Kramer KL. Evidence for energetic tradeoffs between physical activity and childhood growth across the nutritional transition. Sci Rep. 2018;8:1–0.

    Article  CAS  Google Scholar 

  7. Shivakumar N, Sivadas A, Devi S, Jahoor F, McLaughlin J, Smith CP, et al. Gut microbiota profiles of young South Indian children: Child sex-specific relations with growth. PloS One. 2021;16:e0251803.

    Article  CAS  Google Scholar 

  8. Kashyap S, Shivakumar N, Sejian V, Deutz NE, Preston T, Sreeman S, et al. Goat milk protein digestibility in relation to intestinal function. Am J Clin Nutr. 2021;113:845–53.

    Article  Google Scholar 

  9. Ford RP, Menzies IS, Phillips AD, Walker-Smith JA, Turner MW. Intestinal sugar permeability: relationship to diarrhoeal disease and small bowel morphology. J Pediatr Gastroenterol Nutr. 1985;4:568–74.

    Article  CAS  Google Scholar 

  10. International Atomic Energy Agency. Assessing Body Composition and Total Energy Expenditure in Humans Using Stable Isotope Techniques. IAEA Human. Vienna, Austria: International Atomic Energy Agency; 2009.

    Google Scholar 

  11. Psaki SR, Seidman JC, Miller M, Gottlieb M, Bhutta ZA, Ahmed T, et al. Measuring socioeconomic status in multicountry studies: results from the eight-country MAL-ED study. Popul Health Metr. 2014;12:1–1.

    Article  Google Scholar 

  12. Institute of Medicine (US) Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. DRI Dietary Reference Intakes: applications in dietary assessment. Washington (DC): National Academies Press (US); 2000. p. 1–267.

    Google Scholar 

  13. Ravelli MN, Schoeller DA. An objective measure of energy intake using the principle of energy balance. Int J Obes. 2021;45:725–32.

    Article  Google Scholar 

  14. Friedman SM, Rodriguez PN, Boyer PM, Lifshitz F. Decreased energy expenditure—an adaptive mechanism of nutritional growth retardation. Nutr Res. 2006;26:345–9.

    Article  CAS  Google Scholar 

  15. Said-Mohamed R, Bernard JY, Ndzana AC, Pasquet P. Is overweight in stunted preschool children in Cameroon related to reductions in fat oxidation, resting energy expenditure and physical activity? PLoS One. 2012;7:e39007.

    Article  CAS  Google Scholar 

  16. Hoffman DJ, Sawaya AL, Coward WA, Wright A, Martins PA, de Nascimento C, et al. Energy expenditure of stunted and nonstunted boys and girls living in the shantytowns of São Paulo, Brazil. Am J Clin Nutr. 2000;72:1025–31.

    Article  CAS  Google Scholar 

  17. Thompson AL. Greater male vulnerability to stunting? Evaluating sex differences in growth, pathways and biocultural mechanisms. Ann Hum Biol. 2021;48:466–73.

    Article  Google Scholar 

  18. Bines JE, Truby HD. Measurement of resting energy expenditure in infants. J Paediatr Child Health. 2004;40:380–3.

    Article  CAS  Google Scholar 

  19. Denno DM, VanBuskirk K, Nelson ZC, Musser CA, Hay Burgess DC, Tarr PI. Use of the lactulose to mannitol ratio to evaluate childhood environmental enteric dysfunction: a systematic review. Clin Infect Dis. 2014;59:S213–9.

    Article  CAS  Google Scholar 

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We acknowledge Jean Wei-Chen Hsu for her contribution to the lactulose and rhamnose analyses. This research was supported by a grant (award number: OPP1133329) from the Bill and Melinda Gates Foundation to FJ and AVK. The funders were not part of the design, implementation, analysis and interpretation of the data.

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The authors’ responsibilities were as follows: NS and TT performed the secondary analyses. All the authors critically read and approved the final manuscript. AVK had primary responsibility for final content. The authors declare no competing financial interests.

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Correspondence to Anura V. Kurpad.

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The authors declare no competing interests.

Ethics approval

The study protocol was approved by the Institutional Ethical Review Board of St. John’s Medical College and Hospital and by the Institutional Review Board for Human Subject Research of Baylor College of Medicine & Affiliated Hospitals. A written informed consent was obtained from the primary caregivers of the participating children. The study was registered at the Clinical Trials Registry of India (; registration number: CTRI/2017/02/007921.

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Shivakumar, N., Thomas, T., Devi, S. et al. Free living total energy expenditure in young South Indian children at risk of environmental enteric dysfunction and its relation to faltered linear growth. Eur J Clin Nutr (2023).

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