Two novel models evaluating the determinants of resting metabolic rate in Indian children
Keywords:resting metabolic rate, Indian children, organ mass, body composition
AbstractBackground: Resting metabolic rate (RMR) quantifies the minimal energy required to sustain vital body functions and is a crucial component of childhood development. Mean RMR per unit body mass (RMR/BM) has very accurately been modelled in references for Caucasian adolescents.
Objectives: Here we address the extent to which such a model can be adapted to explain RMR/BM in Indian children.
Subjects and Methods: The multicenter study (MCS) is a cross-sectional dataset on 495 children (235 girls and 260 boys) aged 9 to 19 years with anthropometric, body composition, and RMR measurements. The RMR-ultrasonography study (RMR-USG) consists of anthropometric data, RMR, and liver and kidney volume measured through ultrasonography in nine girls and nine boys aged 6 to 8 years.
Results: The mean RMR/BM in Indian children is significantly lower compared to their Caucasian counterparts, except in boys in the age group 9–13 years. We present two novel phenomenological models that describe the mean RMR/BM stratified by age in Indian children and adolescents. The first is a modified Wang model in which the relative masses of four major organs are assumed to be uniformly lowered for Indian children. Theoretical predictions of liver size are not uniformly borne out in a pilot validation study; however, the relative mass of the kidney is found to be significantly lower. The second model demonstrates that changes in body composition alone can also explain the Indian data.
Conclusion: A modified Wang model in which the relative masses of four major organs are assumed to be uniformly lower in Indian children and differences in body composition can be used to estimate mean RMR/BM by age in Indian children; however, understanding the mechanistic basis of variation in RMR/BM remains an open problem.
Almond, D./Currie, J. (2011). Killing Me Softly: The Fetal Origins Hypothesis. Journal of Economic Perspectives 25 (3), 153–172. https://doi.org/10.1257/jep.25.3.153
Altman, P. L./Dittmer, D. S. (1962). Growth, including reproduction and morphological development. Federation of American Societies for Experimental Biology, Washington, DC.
Areekal, S. A./Khadilkar, A./Ekbote, V./Kajale, N./Kinare, A. S./Goel, P. (2021). Two Novel Models Evaluating the Determinants of Resting Metabolic Rate in Indian Children (Version 1). Preprint. https://doi.org/10.21203/rs.3.rs-196719/v1
Aub, J. C./Du Bois, E. F. (1917). Clinical calorimetry: nineteenth paper the basal metabolism of old men. Archives of Internal Medicine XIX (5_II), 823–831. https://doi.org/10.1001/archinte.1917.00080250002001
Bedale, E. M. (1923). Energy expenditure and food requirements of children at school. Proceedings of the Royal Society of London. Series B 94 (662), 368–404. https://doi.org/10.1098/rspb.1923.0009
Bosy-Westphal, A./Reinecke, U./Schlörke, T./Illner, K./Kutzner, D./Heller, M./Müller, M. J. (2004). Effect of organ and tissue masses on resting energy expenditure in underweight, normal weight and obese adults. International Journal of Obesity 28 (1), 72–79. https://doi.org/10.1038/sj.ijo.0802526
Bosy-Westphal, A./Wolf, A./Bührens, F./Hitze, B./Czech, N./Mönig, H./Selberg, O./Settler, U./Pfeuffer, M./Schrezenmeir, J./Krawczak, M./Müller, M. J. (2008). Familial influences and obesity-associated metabolic risk factors contribute to the variation in resting energy expenditure: the Kiel Obesity Prevention Study. The American Journal of Clinical Nutrition 87 (6), 1695–1701. https://doi.org/10.1093/ajcn/87.6.1695
Chandramohan, A./Ramakrishna, B./Venkatramani, S. (2012). Formula for calculating standard liver volume in Indians. Indian Journal of Gastroenterology 31 (1), 15–19. https://doi.org/10.1007/s12664-011-0152-2
Cherian, K. S./Shahkar, F./Sainoji, A./Balakrishna, N./Yagnambhatt, V. R. (2018). Resting metabolic rate of Indian Junior Soccer players: Testing agreement between measured versus selected predictive equations. American Journal of Human Biology 30 (1), e23066. https://doi.org/10.1002/ajhb.23066
Chiplonkar, S./Kajale, N./Ekbote, V./Mandlik, R./Parthasarathy, L./Borade, A./Patel, P./Patel, P./Khadilkar, V./Khadilkar, A. (2017). Reference centile curves for body fat percentage, fat-free mass, muscle mass and bone mass measured by bioelectrical impedance in Asian Indian children and adolescents. Indian Pediatrics 54 (12), 1005–1011. https://doi.org/10.1007/s13312-017-1201-4
Chugani, H. T./Phelps, M. E./Mazziotta, J. C. (1987). Positron emission tomography study of human brain functional development. Annals of Neurology 22 (4), 487–497. https://doi.org/10.1002/ana.410220408
Corrigan, J. K./Ramachandran, D./He, Y./Palmer, C. J./Jurczak, M. J./Chen, R./Li, B./Friedline, R. H./Kim, J. K./Ramsey, J. J./Lantier, L./McGuinness, O. P./Mouse Metabolic Phenotyping Center Energy Balance Working Group, Banks, A. S. (2020). A big-data approach to understanding metabolic rate and response to obesity in laboratory mice. eLife 9, e53560. https://doi.org/10.7554/eLife.53560
Cunningham, J. J. (1980). A reanalysis of the factors influencing basal metabolic rate in normal adults. The American Journal of Clinical Nutrition 33 (11), 2372–2374. https://doi.org/10.1093/ajcn/33.11.2372
Elia, M. (1992). Organ and tissue contribution to metabolic rate, in: Kinney, J.M., Tucker, H.N. (Eds.), Energy Metabolism: Tissue Determinants and Cellular Corollaries. Raven Press, New York, pp. 61–79.
Esht, V./Midha, D./Chatterjee, S./Sharma, S. (2018). A preliminary report on physical activity patterns among children aged 8–14 years to predict risk of cardiovascular diseases in Malwa region of Punjab. Indian Heart Journal 70 (6), 777–782. https://doi.org/10.1016/j.ihj.2018.01.015
FAO/WHO/UNU (2004). Human energy requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. Rome, 17–24 October 2001, FAO Food and Nutrition Technical Support Series. Food and Agriculture Organization of the United Nations, Rome.
FAO/WHO/UNU (1985). Energy and Protein Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. Rome, 5–17 October 1981, World Health Organization Technical Report Series. World Health Organization, Geneva.
Fomon, S. J./Haschke, F./Ziegler, E. E./Nelson, S. E. (1982). Body composition of reference children from birth to age 10 years. The American Journal of Clinical Nutrition 35 (5), 1169–1175. https://doi.org/10.1093/ajcn/35.5.1169
Forbes, G. B. (1987). Human Body Composition. Growth, Aging, Nutrition, and Activity. Springer, New York. https://doi.org/10.1007/978-1-4612-4654-1
Gallagher, D./Belmonte, D./Deurenberg, P./Wang, Z./Krasnow, N./Pi-Sunyer, F. X./Heymsfield, S. B. (1998). Organ-tissue mass measurement allows modeling of REE and metabolically active tissue mass. The American Journal of Physiology 275 (2), E249–E258. https://doi.org/10.1152/ajpendo.1998.275.2.E249
Hall, K. D./Butte, N. F./Swinburn, B. A./Chow, C. C. (2013). Dynamics of childhood growth and obesity: development and validation of a quantitative mathematical model. The Lancet Diabetes & Endocrinology 1 (2), 97–105. https://doi.org/10.1016/S2213-8587(13)70051-2
Harris, J. A./Benedict, F. G. ((1918). A Biometric Study of Human Basal Metabolism. Proceedings of the National Academy of Sciences 4 (12), 370–373. https://doi.org/10.1073/pnas.4.12.370
Haugen, H. A./Melanson, E. L./Tran, Z. V./Kearney, J. T./Hill, J. O. (2003). Variability of measured resting metabolic rate. The American Journal of Clinical Nutrition 78 (6), 1141–1144. https://doi.org/10.1093/ajcn/78.6.1141
Henry, C. J. K. (2005). Basal metabolic rate studies in humans: measurement and development of new equations. Public Health Nutrition 8 (7a), 1133–1152. https://doi.org/10.1079/PHN2005801
Hsu, A./Heshka, S./Janumala, I./Song, M.-Y./Horlick, M./Krasnow, N./Gallagher, D. (2003). Larger mass of high-metabolic-rate organs does not explain higher resting energy expenditure in children. The American Journal of Clinical Nutrition 77 (6), 1506–1511. https://doi.org/10.1093/ajcn/77.6.1506
ICRP (2009). Adult reference computational phantoms. ICRP Publication 110. Ann. ICRP 39 (2). Available online at https://www.icrp.org/publication.asp?id=icrp%20publication%20110 (accessed 3/13/23).
Indian Council of Medical Research (ICMR) (2010). Nutrient Requirements and Recommended Dietary Allowances for Indians. A Report of the Expert Group of the Indian Council of Medical Research. National Institute of Nutrition, Hyderabad, India.
Johnstone, A. M./Murison, S. D./Duncan, J. S./Rance, K. A./Speakman, J. R. (2005). Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. The American Journal of Clinical Nutrition 82 (5), 941–948. https://doi.org/10.1093/ajcn/82.5.941
Kajale, N./Khadilkar, A./Oza, C./Gondhalekar, K./Khadilkar, V. (2022). Resting metabolic rate and its association with body composition parameters in 9- to 18-year-old Indian children and adolescents. Nutrition 99–100, 111652. https://doi.org/10.1016/j.nut.2022.111652
Katch, V. L./Marks, C. C./Becque, M. D./Moorehead, C./Rocchini, A. (1990). Basal metabolism of obese adolescents: Evidence for energy conservation compared to normal and lean adolescents. American Journal of Human Biology 2 (5), 543–551. https://doi.org/10.1002/ajhb.1310020510
Khadilkar, A. V./Lohiya, N./Mistry, S./Chiplonkar, S./Khadilkar, V./Kajale, N./Ekbote, V./Vispute, S./Mandlik, R./Prasad, H./Singh, N./Agarwal, S./Palande, S./Ladkat, D. (2019). Random Blood Glucose Concentrations and their Association with Body Mass Index in Indian School Children. Indian Journal of Endocrinology and Metabolism 23 (5), 529–535. https://doi.org/10.4103/ijem.IJEM_536_19
Kleiber, M. (1932). Body size and metabolism. Hilgardia 6 (11), 315–353. https://doi.org/10.3733/hilg.v06n11p315
Krishnan, B. T./Vareed, C. (1932). Basal Metabolism of Young College Students, Men and Women, in Madras. Indian Journal of Medical Research 19 (3), 831–858.
Kumar, S./Kumar, N./Sachar, R. S. (1961). Basal metabolic rate in normal Indian adult males. Indian Journal of Medical Research 49, 702–709.
Kyle, U. G./Bosaeus, I./De Lorenzo, A. D./Deurenberg, P./Elia, M./Gómez, J. M./Heitmann, B. L./Kent-Smith, L./Melchior, J.-C./Pirlich, M., Scharfetter, H./Schols, A. M. W. J./Pichard, C. (2004). Bioelectrical impedance analysis—part II: utilization in clinical practice. Clinical Nutrition 23 (6), 1430–1453. https://doi.org/10.1016/j.clnu.2004.09.012
Mason, E. D./Benedict, F. G. (1931). The basal metabolism of South Indian women. Indian Journal of Medical Research 19, 75–98.
Mason, E. D./Mundkur, V./Jacob, M. (1963). Basal energy metabolism and heights, weights, arm skinfold and muscle of young Indian women in Bombay, with prediction standards for B.M.R. Indian Journal of Medical Research 51, 925–932.
McMurray, R. G./Soares, J./Caspersen, C. J./McCurdy, T. (2014). Examining Variations of Resting Metabolic Rate of Adults: A Public Health Perspective. Medicine & Science in Sports & Exercise 46 (7), 1352–1358. https://doi.org/10.1249/MSS.0000000000000232
Menzel, H.-G./Clement, C./DeLuca, P. (2009). Realistic reference phantoms: An ICRP/ICRU joint effort. Annals of the ICRP, ICRP Publication 110: Adult Reference Computational Phantoms 39 (2), 3–5. https://doi.org/10.1016/j.icrp.2009.09.001
Mifflin, M. D./St. Jeor, S. T./Hill, L. A./Scott, B. J./Daugherty, S. A./Koh, Y. O. (1990). A new predictive equation for resting energy expenditure in healthy individuals. The American Journal of Clinical Nutrition 51 (2), 241–247. https://doi.org/10.1093/ajcn/51.2.241
Mukherjee, H. N./Gupta, P. C. (1931). The basal metabolism of Indians (Bengalis). Indian Journal of Medical Research 18, 807–812.
Müller, M. J./Langemann, D./Gehrke, I./Later, W./Heller, M./Glüer, C. C./Heymsfield, S. B./Bosy-Westphal, A. (2011). Effect of Constitution on Mass of Individual Organs and Their Association with Metabolic Rate in Humans—A Detailed View on Allometric Scaling. PLOS ONE 6 (7), e22732. https://doi.org/10.1371/journal.pone.0022732
NCD Risk Factor Collaboration (2017). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. The Lancet 390 (10113), 2627–2642. https://doi.org/10.1016/S0140-6736(17)32129-3
Nieman, D. C./Austin, M. D./Benezra, L./Pearce, S./McInnis, T./Unick, J./Gross, S. J. (2006). Validation of Cosmed’s FitMateTM in Measuring Oxygen Consumption and Estimating Resting Metabolic Rate. Research in Sports Medicine 14 (2), 89–96. https://doi.org/10.1080/15438620600651512
Niyogi, S. P./Patwardhan, V. N./Mordecai, J. ((1939). Studies on Basal Metabolism in Bombay. Part I. Indian Journal of Medical Research 27, 99–113.
Owen, O.E., Holup, J.L., D’Alessio, D.A., Craig, E.S., Polansky, M., Smalley, K.J., Kavle, E.C., Bushman, M.C., Owen, L.R., Mozzoli, M.A., 1987. A reappraisal of the caloric requirements of men. The American Journal of Clinical Nutrition 46 (6), 875–885. https://doi.org/10.1093/ajcn/46.6.875
Owen, O. E./Kavle, E./Owen, R. S./Polansky, M./Caprio, S./Mozzoli, M. A./Kendrick, Z. V./Bushman, M.C./Boden, G. (1986). A reappraisal of caloric requirements in healthy women. The American Journal of Clinical Nutrition 44 (1), 1–19. https://doi.org/10.1093/ajcn/44.1.1
Patil, S. R./Bharadwaj, J. (2013). Development of new equations for basal metabolic rate for adolescent student Indian population. Journal of Postgraduate Medicine 59 (1), 25–29. https://doi.org/10.4103/0022-3859.109491
Poehlman, E. T./Toth, M. J. (1995). Mathematical ratios lead to spurious conclusions regarding age- and sex-related differences in resting metabolic rate. The American Journal of Clinical Nutrition 61 (3), 482–485. https://doi.org/10.1093/ajcn/61.3.482
Psota, T./Chen, K. Y. (2013). Measuring energy expenditure in clinical populations: rewards and challenges. European Journal of Clinical Nutrition 67 (5), 436–442. https://doi.org/10.1038/ejcn.2013.38
Purcell, S. A./Johnson-Stoklossa, C./Tibaes, J. R. B./Frankish, A./Elliott, S. A./Padwal, R./Prado, C. M. (2020). Accuracy and reliability of a portable indirect calorimeter compared to whole-body indirect calorimetry for measuring resting energy expenditure. Clinical Nutrition ESPEN 39, 67–73. https://doi.org/10.1016/j.clnesp.2020.07.017
R Core Team (2019). The R Project for Statistical Computing. Available online at https://www.r-project.org/ (accessed 12/2/22).
Rahman, S. A. (1936). The basal metabolism of young men at Hyderabad (Deccan) with a study of their physical characters. Indian Journal of Medical Research 24, 173–199.
Rahmandad, H. (2014). Human Growth and Body Weight Dynamics: An Integrative Systems Model. PLOS ONE 9, e114609. https://doi.org/10.1371/journal.pone.0114609
Rajagopal, K. (1938). The Basal Metabolism of Indian and European Men on the Nilgiri Hills (S. India). Indian Journal of Medical Research 26, 411–426.
Reneau, J./Obi, B./Moosreiner, A./Kidambi, S. (2019). Do we need race-specific resting metabolic rate prediction equations? Nutrition & Diabetes 9, 21. https://doi.org/10.1038/s41387-019-0087-8
Schofield, W. N. (1985). Predicting basal metabolic rate, new standards and review of previous work. Human Nutrition. Clinical Nutrition 39c (Suppl. 1), 5–41.
Shirley, M. K./Arthurs, O. J./Seunarine, K. K./Cole, T. J./Eaton, S./Williams, J. E./Clark, C. A./Wells, J. C. K. (2019). Metabolic rate of major organs and tissues in young adult South Asian women. European Journal of Clinical Nutrition 73 (8), 1164–1171. https://doi.org/10.1038/s41430-018-0362-0
Snyder, W./Cook, M./Nasset, E./Karhausen, L./Howells, G./Tipton, I. (1975). Report of the Task Group on Reference Man, ICRP Publication. Pergamon Press, Oxford.
Soares, M. J./Piers, L. S./O’Dea, K./Shetty, P. S. (1998). No evidence for an ethnic influence on basal metabolism: an examination of data from India and Australia. British Journal of Nutrition 79 (4), 333–341. https://doi.org/10.1079/BJN19980057
Srivastava, R./Batra, A./Dhawan, D./Bakhshi, S. (2017). Association of energy intake and expenditure with obesity: A cross-sectional study of 150 pediatric patients following treatment for leukemia. Pediatric Hematology and Oncology 34 (1), 29–35. https://doi.org/10.1080/08880018.2016.1272025
Swaminathan, S./Thomas, T./Yusuf, S./Vaz, M. (2013). Clustering of diet, physical activity and overweight in parents and offspring in South India. European Journal of Clinical Nutrition 67 (2), 128–34. https://doi.org/10.1038/ejcn.2012.192
Swinburn, B. A./Jolley, D./Kremer, P. J./Salbe, A. D./Ravussin, E. (2006). Estimating the effects of energy imbalance on changes in body weight in children. The American Journal of Clinical Nutrition 83 (4), 859–863. https://doi.org/10.1093/ajcn/83.4.859
Talbot, F.B., 1938. Basal metabolism standards for childern. American Journal of Diseases of Children 55 (3), 455–459. https://doi.org/10.1001/archpedi.1938.01980090003001
The MathWorks Inc. (2019). MATLAB version: 9.7.0 (R2019b), Natick, Massachusetts. Available online at https://in.mathworks.com/ (accessed 11/30/22).
Tschöp, M. H./Speakman, J. R./Arch, J. R. S./Auwerx, J./Brüning, J. C./Chan, L./Eckel, R. H./Farese, R. V./Galgani, J. E./Hambly, C./Herman, M. A./Horvath, T. L./Kahn, B. B./Kozma, S. C./Maratos-Flier, E./Müller, T. D./Münzberg, H./Pfluger, P. T./Plum, L./Reitman, M. L./Rahmouni, K./Shulman, G. I./Thomas, G./Kahn, C. R./Ravussin, E. (2012). A guide to analysis of mouse energy metabolism. Nature Methods 9 (1), 57–63. https://doi.org/10.1038/nmeth.1806
Vandarakis, D./Salacinski, A. J./Broeder, C. E. (2013). A Comparison of Cosmed Metabolic Systems for the Determination of Resting Metabolic Rate. Research in Sports Medicine 21 (2), 187–194. https://doi.org/10.1080/15438627.2012.757226
Wang, Z. (2012). High ratio of resting energy expenditure to body mass in childhood and adolescence: A mechanistic model. American Journal of Human Biology 24 (4), 460–467. https://doi.org/10.1002/ajhb.22246
Wang, Z./Heshka, S./Heymsfield, S. B./Shen, W./Gallagher, D. (2005). A cellular-level approach to predicting resting energy expenditure across the adult years. The American Journal of Clinical Nutrition 81 (4), 799–806. https://doi.org/10.1093/ajcn/81.4.799
Wang, Z./Heshka, S./Zhang, K./Boozer, C. N./Heymsfield, S. B. (2001). Resting Energy Expenditure: Systematic Organization and Critique of Prediction Methods. Obesity Research 9 (5), 331–336. https://doi.org/10.1038/oby.2001.42
Wang, Z./Ying, Z./Bosy-Westphal, A./Zhang, J./Schautz, B./Later, W./Heymsfield, S. B./Müller, M. J. (2010). Specific metabolic rates of major organs and tissues across adulthood: evaluation by mechanistic model of resting energy expenditure. The American Journal of Clinical Nutrition 92 (6), 1369–1377. https://doi.org/10.3945/ajcn.2010.29885
Weir, J. B. de V. (1949). New methods for calculating metabolic rate with special reference to protein metabolism. The Journal of Physiology 109 (1-2), 1–9. https://doi.org/10.1113/jphysiol.1949.sp004363
WHO (2020). The double burden of malnutrition: policy brief. Available online at https://apps.who.int/iris/handle/10665/255413 (accessed 3/9/20).
Wlodek, M. E./Westcott, K./Siebel, A. L./Owens, J. A./Moritz, K. M. (2008). Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney International 74 (2), 187–195. https://doi.org/10.1038/ki.2008.153
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