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Growth retardation at early life and metabolic adaptation among North Korean children

Published online by Cambridge University Press:  22 May 2015

S.-K. Lee ,
S.-Y. Nam  and
D. J. Hoffman
S.-K. Lee*
Affiliation:
Department of Food and Nutrition, Inha University, Incheon, Korea
S.-Y. Nam
Affiliation:
Department of Food and Nutrition, Inha University, Incheon, Korea
D. J. Hoffman
Affiliation:
Department of Nutritional Sciences, Rutgers University, New Brunswick, NJ, USA
*
*Address for correspondence: S.-K. Lee, Department of Food and Nutrition, Inha University, 100 Inharo, Incheon 402-751, Korea. (Email skleenutrition@inha.ac.kr)
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Abstract

The high prevalence of obesity is a major public health issue and contributes to the ‘double burden’ of disease in developing countries. Early exposure to poor nutrition may cause metabolic adaptations that, when accompanied by exposure to ‘affluent’ nutrition, may increase the risk for obesity and other metabolic disorders. The aim of this study was to determine differences in energy metabolism and nutritional status between normal-height and growth-retarded North Korean children living in South Korea. A total of 29 children were recruited and underwent measurements of resting energy expenditure (REE), respiratory quotient (RQ), anthropometrics and dietary intake. There was no difference in REE or any assessment of obesity between the growth-retarded and normal-height children. Children who were classified as growth retarded (HAZ<−1.0) or stunted (HAZ<−2.0) had a significantly higher RQ (β=0.036 or 0.060, respectively, P=0.018 or 0.016), independent of sex, age, fat-free mass, fat mass and food quotient, compared with children with normal height. The results from this study, the first from an Asian population, add to the growing body of literature suggesting that undernutrition early in life results in adaptations in energy metabolism that favor fat deposition, increasing the risk of stunted children becoming overweight or obese later in life. Continued research on this topic is warranted, given the continued rise in the prevalence of the double burden in transitional countries.

Keywords

childrenfat oxidationgrowth retardationNorth KoreaRQ
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 6 , Issue 4 , August 2015 , pp. 291 - 298
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

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References

1. Finucane, MM, Stevens, GA, Cowan, MJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011; 377, 557–567.CrossRefGoogle ScholarPubMed
2. Prentice, AM. The emerging epidemic of obesity in developing countries. Int J Epidemiol. 2006; 35, 93–99.CrossRefGoogle ScholarPubMed
3. Prospective Studies Collaboration. Body mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet. 2009; 373, 1083–1096.CrossRefGoogle Scholar
4. World Health Organization. Global Health Risks: Mortality and Burden of Disease Attributable to Selected Major Risks. 2009. WHO Press: Geneva, Switzerland.Google Scholar
5. Marshall, SJ. Developing countries face double burden of disease. Bull World Health Organ. 2004; 82, 556.Google ScholarPubMed
6. Uauy, R, Corvalan, C, Dangour, A. Global nutrition challenges for optimal health and well-being. Proc Nutr Soc. 2009; 68, 34–42.CrossRefGoogle ScholarPubMed
7. Fernald, LC, Neufeld, LM. Overweight with concurrent stunting in very young children from rural Mexico: prevalence and associated factors. Eur J Clin Nutr. 2007; 61, 623–632.Google Scholar
8. Kimani-Murage, EW, Kahn, K, Pettifor, JM, et al. The prevalence of stunting, overweight and obesity, and metabolic disease risk in rural South African children. BMC Public Health. 2010; 10, 158–171.Google Scholar
9. Cardoso, I, Bovet, P, Viswanathan, B, et al. Nutrition transition in a middle-income country: 22-year trends in the Seychelles. Eur J Clin Nutr. 2013; 67, 135–140.CrossRefGoogle Scholar
10. Lee, SK, Sobal, J. Socioeconomic, dietary, activity, nutrition, and weight transitions in South Korea. Public Health Nutr. 2003; 6, 665–674.Google Scholar
11. Popkin, BM, Adair, LS, Ng, SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012; 70, 3–21.CrossRefGoogle ScholarPubMed
12. Wells, JCK. Obesity as malnutrition: the role of capitalism in the obesity global epidemic. Am J Hum Biol. 2012; 24, 261–276.CrossRefGoogle ScholarPubMed
13. Martins, PA, Hoffman, DJ, Fernandes, MTB, et al. Stunted children gain less lean body mass and more fat mass than their non-stunted counterparts: a prospective study. Br J Nutr. 2004; 92, 819–825.Google Scholar
14. Barker, DJP, Gluckman, PD, Godfrey, KM, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993; 341, 938–941.CrossRefGoogle ScholarPubMed
15. Gluckman, P, Hanson, M. Developmental Origins of Health and Disease. 2006. Cambridge University Press: Cambridge.CrossRefGoogle Scholar
16. Bruce, KD, Hanson, MA. The developmental origins, mechanisms, and implications of metabolic syndrome. J Nutr. 2010; 140, 648–652.CrossRefGoogle ScholarPubMed
17. Prentice, AM, Moore, SE. Early programming of adult diseases in resource poor countries. Arch Dis Child. 2005; 90, 429–432.Google Scholar
18. Popkin, BM, Richards, MK, Montiero, CA. Stunting is associated with overweight in children of four nations that are undergoing the nutrition transition. J Nutr. 1996; 126, 3009–3016.Google Scholar
19. Martorell, R, Stein, AD, Schoroeder, DG. Early nutrition and later adiposity. J Nutr. 2001; 131, 874S–880S.CrossRefGoogle ScholarPubMed
20. Grillo, LP, Siqueira, AFA, Silva, AC, et al. Lower resting metabolic rate and higher velocity of weight gain in a prospective study of stunted vs nonstunted girls living in the shantytowns of Sao Paulo, Brazil. Eur J Clin Nutr. 2005; 59, 835–842.CrossRefGoogle Scholar
21. Cameron, N, Wright, MM, Griffiths, PL, et al. Stunting at 2 years in relation to body composition at 9 years in African urban children. Obes Res. 2005; 13, 131–136.Google Scholar
22. Gigante, DP, Victora, CG, Horta, BL, et al. Undernutrition in early life and body composition of adolescent males from a birth cohort study. Br J Nutr. 2007; 97, 949–954.Google Scholar
23. Hoffman, DJ, Sawaya, AL, Verreschi, I, et al. Why are nutritionally stunted children at increased risk of obesity? Studies of metabolic rate and fat oxidation in shantytown children from Sao Paul, Brazil. Am J Clin Nutr. 2000; 72, 702–707.Google Scholar
24. Frisancho, AR. Reduced rate of fat oxidation: a metabolic pathway to obesity in the developing nations. Am J Hum Biol. 2003; 15, 522–532.CrossRefGoogle ScholarPubMed
25. Kensara, OA, Wooton, SA, Phillips, DI, et al. Substrate-energy metabolism and metabolic risk factors for cardiovascular disease in relation to fetal growth and adult body composition. Am J Physiol Endocrinol Metab. 2006; 291, E365–E371.Google Scholar
26. Leonard, WR, Sorensen, MV, Mosher, MJ, et al. Reduced fat oxidation and obesity risks among the Buryat of Southern Siberia. Am J Hum Biol. 2009; 21, 664–670.Google Scholar
27. Wren, RE, Blume, H, Mazariegos, M, et al. Body composition, resting metabolic rate, and energy requirements of short- and normal-stature, low-income Guatemalan children. Am J Clin Nutr. 1997; 66, 406–412.CrossRefGoogle Scholar
28. Friedman, SM, Rodriguez, PN, Boyer, PM, et al. Decreased energy expenditure – an adaptive mechanism of nutritional growth retardation. Nutr Res. 2006; 26, 345–349.Google Scholar
29. Said-Mohamed, R, Bernard, JY, Ndzana, AC, et al. Is overweight in stunted preschool children in Cameroon related to reduction in fat oxidation, resting energy expenditure and physical activity. PLoS One. 2012; 7, e39007.Google Scholar
30. DPRK Central Bureau of Statistics. Democratic People’s Republic of Korea Final report of the National Nutrition Survey 2012. Retrieved 26 March 2014 from http://www.unicef.org/eapro/DPRK_National_Nutrition_Survey_2012.pdfl.Google Scholar
31. Hoffman, DJ, Lee, SK. The prevalence of wasting, but not stunting, has improved in the Democratic People’s Republic of Korea. J Nutr. 2005; 135, 452–456.CrossRefGoogle Scholar
32. Lee, SK, Nam, SY, Hoffman, DJ. Changes in nutritional status among displaced North Korean children living in South Korea. Annal Human Biol. (In press).Google Scholar
33. Lee, SK, Nam, SY. Comparison of food and nutrient consumption status between displaced North Korean children in South Korea and South Korean children. Kor J Community Nutr. 2012; 17, 407–418.CrossRefGoogle Scholar
34. Gibson, RS. Principles of Nutritional Assessment, 2nd edn, 1990. Oxford University Press: Oxford.Google Scholar
35. Black, AE, Prentice, AM, Coward, WA. Use of food quotients to predict respiratory quotients for the doubly-labeled water method of measuring energy expenditure. Hum Nutr Clin Nutr. 1986; 40, 381–391.Google Scholar
36. Lim, JS, Hwang, JS, Lee, JA, et al. Cross-calibration of multi-frequency bioelectrical impedance analysis with eight-point tactile electrodes and dual-energy X-ray absorptiometry for assessment of body composition in healthy children aged 6-18 years. Pediatr Int. 2009; 51, 263–268.CrossRefGoogle ScholarPubMed
37. World Health Organization. WHO Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight-for-Height and Body Mass Index-for-Age: Methods and Development. 2006. World Health Organization: Geneva.Google Scholar
38. Johnstone, AM, Murison, SD, Duncan, JS, Rance, KA, Speakman, JR. Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr. 2005; 82, 941–948.Google Scholar
39. Galgani, JE, de Jonge, L, Most, MM, Bray, GA, Smith, SR. Effect of a 3-day high-fat feeding period on carbohydrate balance and ad libitum energy intake in humans. Int J Obes (Lond). 2010; 34, 886–891.Google Scholar
40. Astrup, A, Buemann, B, Christensen, NJ, et al. The contribution of body composition, substrates, and hormones to the variability in energy expenditure and substrate utilization in premenopausal women. J Clin Endocrinol Metab. 1992; 74, 279–286.Google Scholar
41. Allison, DB, Paultre, F, Goran, MI, et al. Statistical considerations regarding the use of ratios to adjust data. Int J Obes Relat Metab Disord. 1995; 19, 644–652.Google ScholarPubMed
42. Hoffman, DJ, Sawaya, AL, Coward, WA, et al. Energy expenditure of stunted and nonstunted boys and girls living in the shantytowns of Sao Paulo, Brazil. Am J Clin Nutr. 2000; 72, 1025–1031.Google Scholar
43. Zurlo, F, Lillioja, S, Esposito-Del Puente, A, et al. Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am J Physiol. 1990; 259, E650–E657.Google Scholar
44. Seidell, JC, Muller, DC, Sorkin, JD, et al. Fasting respiratory exchange ratio and resting metabolic rate as predictors of weight gain: the Baltimore Longitudinal Study on Aging. Int J Obes Relat Metab Disord. 1992; 16, 667–674.Google ScholarPubMed
45. DeLany, JP, Bray, GA, Harsha, DW, et al. Energy expenditure and substrate oxidation predict changes in body fat in children. Am J Clin Nutr. 2006; 84, 862–870.CrossRefGoogle ScholarPubMed
46. Hoffman, DJ, Martins, PA, Roberts, SB, et al. Body fat distribution in stunted compared with normal-height children from the shantytowns of Sao Paulo, Brazil. Nutrition. 2007; 23, 640–646.Google Scholar
47. Martins, PA, Hoffman, DJ, Fernandes, MT, et al. Stunted children gain less lean body mass and more fat mass than their non-stunted counterparts: a prospective study. Br J Nutr. 2004; 92, 819–825.Google Scholar
48. Sichieri, R, Dos Santos Barbosa, F, Moura, EC. Relationship between short stature and obesity in Brazil: a multilevel analysis. Br J Nutr. 2010; 103, 1534–1538.Google Scholar
49. Benefice, E, Garnier, D, Simondon, KB, et al. Relationship between stunting in infancy and growth and fat distribution during adolescence in Senegalese girls. Eur J Clin Nutr. 2001; 95, 50–58.Google Scholar
50. Schroeder, DG, Martorell, R, Flores, R. Infant and child growth and fatness and fat distribution in Guatemalan adults. Am J Epidemiol. 1999; 149, 177–185.Google Scholar
51. Koziel, S, Jankowska, EA. Birthweight and statue, body mass index and fat distribution of 14-year-old Polish adolescents. J Paediatr Child Health. 2002; 38, 55–58.Google Scholar
52. Mukuddem-Petersen, J, Kruger, HS. Association between stunting and overweight among 10-15-y-old children in the North West Province of South Africa: the THUSA BANA Qstudy. Int J Obes Relat Metab Disord. 2004; 28, 842–851.CrossRefGoogle Scholar
53. Doak, CM, Hoffman, DJ, Norris, SA, et al. Is body mass index an appropriate proxy for body fat in children? Global Food Security. 2013; 2, 65–138.CrossRefGoogle Scholar
54. Timaus, IM. Stunting and obesity in childhood: a reassessment using longitudinal data from South Africa. Int J Epidemiol. 2012; 41, 764–772.Google Scholar