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24-h energy expenditure in people with type 1 diabetes: impact on equations for clinical estimation of energy expenditure

European Journal of Clinical Nutrition (2024)Cite this article

Subjects

Abstract

Background/Objectives

Type 1 diabetes (T1D) is associated with an increase in resting metabolic rate (RMR), but the impact of T1D on other components of 24-h energy expenditure (24-h EE) is not known. Also, there is a lack of equations to estimate 24-h EE in patients with T1D. The aims of this analysis were to compare 24-h EE and its components in young adults with T1D and healthy controls across the spectrum of body mass index (BMI) and derive T1D-specific equations from clinical variables.

Subjects/Methods

Thirty-three young adults with T1D diagnosed ≥1 year prior and 33 healthy controls matched for sex, age and BMI were included in this analysis. We measured 24-h EE inside a whole room indirect calorimeter (WRIC) and body composition with dual x-ray absorptiometry.

Results

Participants with T1D had significantly higher 24-h EE than healthy controls (T1D = 2047 ± 23 kcal/day vs control= 1908 ± 23 kcal/day; P < 0.01). We derived equations to estimate 24-h EE with both body composition (fat free mass + fat mass) and anthropometric (weight + height) models, which provided high coefficients of determination (R2 = 0.912 for both). A clinical model that did not incorporate spontaneous physical activity yielded high coefficients of determination as well (R2 = 0.897 and R2 = 0.880 for body composition and anthropometric models, respectively).

Conclusion

These results confirm that young adults with established T1D have increased 24-h EE relative to controls without T1D. The derived equations from clinically available variables can assist clinicians with energy prescriptions for weight management in patients with T1D.

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Fig. 1: Differences in energy expenditure, substrate oxidation and physical activity between young adults with type 1 diabetes and healthy control matches assessed inside a whole room indirect calorimeter (WRIC).
Fig. 2: Concordance and agreement of anthropometric and body composition energy expenditure models for people with Type 1 diabetes.

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Data availability

Data can be available upon reasonable request and approval of the principal investigator of each study involved in this publication.

References

  1. Baskaran C, Volkening LK, Diaz M, Laffel LM. A decade of temporal trends in overweight/obesity in youth with type 1 diabetes after the diabetes control and complications trial. Pediatr Diabetes. 2015;16:263–70. https://doi.org/10.1111/pedi.12166.

    Article  CAS  PubMed  Google Scholar 

  2. Conway B, Miller RG, Costacou T, Fried L, Kelsey S, Evans RW, et al. Temporal patterns in overweight and obesity in Type 1 diabetes. Diabet Med. 2010;27:398–404. https://doi.org/10.1111/j.1464-5491.2010.02956.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Minges KE, Whittemore R, Weinzimer SA, Irwin ML, Redeker NS, Grey M. Correlates of overweight and obesity in 5529 adolescents with type 1 diabetes: The T1D Exchange Clinic Registry. Diabetes Res Clin Pr. 2017;126:68–78. https://doi.org/10.1016/j.diabres.2017.01.012.

    Article  Google Scholar 

  4. Vilarrasa N, San Jose P, Rubio MA, Lecube A. Obesity in patients with type 1 diabetes: links, risks and management challenges. Diabetes Metab Syndr Obes. 2021;14:2807–27. https://doi.org/10.2147/DMSO.S223618.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Woods SC, Seeley RJ, Porte D, Schwartz MW. Signals that regulate food intake and energy homeostasis. Science. 1998;280:1378–83. https://doi.org/10.1126/science.280.5368.1378.

    Article  CAS  PubMed  Google Scholar 

  6. Corbin KD, Driscoll KA, Pratley RE, Smith SR, Maahs DM, Mayer-Davis EJ, et al. Obesity in type 1 diabetes: pathophysiology, clinical impact, and mechanisms. Endocr Rev. 2018;39:629–63. https://doi.org/10.1210/er.2017-00191.

    Article  PubMed  Google Scholar 

  7. Carlson MG, Campbell PJ. Intensive insulin therapy and weight gain in IDDM. Diabetes. 1993;42:1700–7. https://doi.org/10.2337/diab.42.12.1700.

    Article  CAS  PubMed  Google Scholar 

  8. Greco AV, Tataranni PA, Mingrone G, De Gaetano A, Manto A, Cotroneo P, et al. Daily energy metabolism in patients with type 1 diabetes mellitus. J Am Coll Nutr. 1995;14:286–91.

    Article  CAS  PubMed  Google Scholar 

  9. Jacob AN, Salinas K, Adams-Huet B, Raskin P. Potential causes of weight gain in type 1 diabetes mellitus. Diabetes Obes Metab. 2006;8:404–11. https://doi.org/10.1111/j.1463-1326.2005.00515.x.

    Article  CAS  PubMed  Google Scholar 

  10. Nair KS, Halliday D, Garrow JS. Increased energy expenditure in poorly controlled Type 1 (insulin-dependent) diabetic patients. Diabetologia. 1984;27:13–16. https://doi.org/10.1007/BF00253494.

    Article  CAS  PubMed  Google Scholar 

  11. Rigalleau V, Lasseur C, Pecheur S, Chauveau P, Combe C, Perlemoine C, et al. Resting energy expenditure in uremic, diabetic, and uremic diabetic subjects. J Diabetes Complicat. 2004;18:237–41. https://doi.org/10.1016/S1056-8727(03)00077-1.

    Article  CAS  Google Scholar 

  12. Leslie P, Jung RT, Isles TE, Baty J, Newton RW, Illingworth P. Effect of optimal glycaemic control with continuous subcutaneous insulin infusion on energy expenditure in type I diabetes mellitus. Br Med J (Clin Res Ed. 1986;293:1121–6. https://doi.org/10.1136/bmj.293.6555.

  13. Molnar D, Decsi T, Soltesz G. Resting energy expenditure and food-induced thermogenesis in diabetic children receiving continuous subcutaneous insulin infusion. Diabetes Res. 1988;7:117–21.

    CAS  PubMed  Google Scholar 

  14. Chen KY, Smith S, Ravussin E, Krakoff J, Plasqui G, Tanaka S, et al. Room indirect calorimetry operating and reporting standards (RICORS 1.0): a guide to conducting and reporting human whole-room calorimeter studies. Obes (Silver Spring). 2020;28:1613–25. https://doi.org/10.1002/oby.22928.

    Article  Google Scholar 

  15. Carnero EA, Bock CP, Distefano G, Corbin KD, Stephens NA, Pratley RE, et al. Twenty-four hour assessments of substrate oxidation reveal differences in metabolic flexibility in type 2 diabetes that are improved with aerobic training. Diabetologia. 2021;64:2322–33. https://doi.org/10.1007/s00125-021-05535-y.

    Article  CAS  PubMed  Google Scholar 

  16. Ethical Principles for Medical Research Involving Human Subjects. In: The World Medical Association I, (ed.) 64th WMA General Assembly. Fortaleza, Brazil, (2013).

  17. Hall KD, Chen KY, Guo J, Lam YY, Leibel RL, Mayer LE, et al. Energy expenditure and body composition changes after an isocaloric ketogenic diet in overweight and obese men. Am J Clin Nutr. 2016;104:324–33. https://doi.org/10.3945/ajcn.116.133561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Schutz Y, Bessard T, Jequier E. Diet-induced thermogenesis measured over a whole day in obese and nonobese women. Am J Clin Nutr. 1984;40:542–52. https://doi.org/10.1093/ajcn/40.3.542.

    Article  CAS  PubMed  Google Scholar 

  19. Lam YY, Redman LM, Smith SR, Bray GA, Greenway FL, Johannsen D, et al. Determinants of sedentary 24-h energy expenditure: equations for energy prescription and adjustment in a respiratory chamber. Am J Clin Nutr. 2014;99:834–42. https://doi.org/10.3945/ajcn.113.079566.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986;78:1568–78. https://doi.org/10.1172/JCI112749.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Lin LI. A concordance correlation coefficient to evaluate reproducibility. Biometrics. 1989;45:255–68.

    Article  CAS  PubMed  Google Scholar 

  22. Holiday DB, Ballard JE, McKeown BC. PRESS-related statistics: regression tools for cross-validation and case diagnostics. Med Sci Sports Exerc. 1995;27:612–20.

    Article  CAS  PubMed  Google Scholar 

  23. Byrne NM, Weinsier RL, Hunter GR, Desmond R, Patterson MA, Darnell BE, et al. Influence of distribution of lean body mass on resting metabolic rate after weight loss and weight regain: comparison of responses in white and black women. Am J Clin Nutr. 2003;77:1368–73. https://doi.org/10.1093/ajcn/77.6.1368.

    Article  CAS  PubMed  Google Scholar 

  24. Heymsfield SB, Gallagher D, Kotler DP, Wang Z, Allison DB, Heshka S. Body-size dependence of resting energy expenditure can be attributed to nonenergetic homogeneity of fat-free mass. Am J Physiol Endocrinol Metab. 2002;282:E132–138. https://doi.org/10.1152/ajpendo.2002.282.1.E132.

    Article  CAS  PubMed  Google Scholar 

  25. Wang Z, Heshka S, Wang J, Gallagher D, Deurenberg P, Chen Z, et al. Metabolically active portion of fat-free mass: a cellular body composition level modeling analysis. Am J Physiol Endocrinol Metab. 2007;292:E49–53. https://doi.org/10.1152/ajpendo.00485.2005.

    Article  CAS  PubMed  Google Scholar 

  26. Habib SL. Kidney atrophy vs hypertrophy in diabetes: which cells are involved? Cell Cycle. 2018;17:1683–7. https://doi.org/10.1080/15384101.2018.1496744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Starzl TE, Porter KA, Kashiwagi N. Portal hepatotrophic factors, diabetes mellitus and acute liver atrophy, hypertrophy and regeneration. Surg Gynecol Obstet. 1975;141:843–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Monaco CMF, Perry CGR, Hawke TJ. Alterations in mitochondrial functions and morphology in muscle and non-muscle tissues in type 1 diabetes: implications for metabolic health. Exp Physiol. 2020;105:565–70. https://doi.org/10.1113/EP088096.

    Article  PubMed  Google Scholar 

  29. Caron N, Peyrot N, Caderby T, Verkindt C, Dalleau G. Energy expenditure in people with diabetes mellitus: a review. Front Nutr. 2016;3:56. https://doi.org/10.3389/fnut.2016.00056. e-pub ahead of print 20161222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Boden G, Cheung P, Homko C. Effects of acute insulin excess and deficiency on gluconeogenesis and glycogenolysis in type 1 diabetes. Diabetes. 2003;52:133–7. https://doi.org/10.2337/diabetes.52.1.133.

    Article  CAS  PubMed  Google Scholar 

  31. Boden G, Chen X, Stein TP. Gluconeogenesis in moderately and severely hyperglycemic patients with type 2 diabetes mellitus. Am J Physiol Endocrinol Metab. 2001;280:E23–30. https://doi.org/10.1152/ajpendo.2001.280.1.E23.

    Article  CAS  PubMed  Google Scholar 

  32. Bray GA, Smith SR, DeJonge L, de Souza R, Rood J, Champagne CM, et al. Effect of diet composition on energy expenditure during weight loss: the POUNDS LOST Study. Int J Obes (2005). 2012;36:448–55. https://doi.org/10.1038/ijo.2011.173.

    Article  CAS  Google Scholar 

  33. Bosy-Westphal A, Muller MJ, Boschmann M, Klaus S, Kreymann G, Luhrmann PM, et al. Grade of adiposity affects the impact of fat mass on resting energy expenditure in women. Br J Nutr. 2009;101:474–7. https://doi.org/10.1017/s0007114508020357.

    Article  CAS  PubMed  Google Scholar 

  34. Levine JA, Eberhardt NL, Jensen MD. Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science. 1999;283:212–4. https://doi.org/10.1126/science.283.5399.212.

    Article  CAS  PubMed  Google Scholar 

  35. Garland T Jr., Schutz H, Chappell MA, Keeney BK, Meek TH, Copes LE, et al. The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol. 2011;214:206–29. https://doi.org/10.1242/jeb.048397.

    Article  PubMed  Google Scholar 

  36. Aydin BN, Stinson EJ, Cabeza De Baca T, Ando T, Travis KT, Piaggi P, et al. Investigation of seasonality of human spontaneous physical activity and energy expenditure in respiratory chamber in Phoenix, Arizona. Eur J Clin Nutr. 2024;78:27–33. https://doi.org/10.1038/s41430-023-01347-y. e-pub ahead of print 20231013.

    Article  PubMed  Google Scholar 

  37. Jeran S, Steinbrecher A, Haas V, Mahler A, Boschmann M, Westerterp KR, et al. Prediction of activity-related energy expenditure under free-living conditions using accelerometer-derived physical activity. Sci Rep. 2022;12:16578. https://doi.org/10.1038/s41598-022-20639-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liguori G, American College of Sports Medicine. ACSM’s Guidelines for Exercise Testing and Prescription, 11th edn Lippincott®, (2021).

  39. Borsheim E, Bahr R. Effect of exercise intensity, duration and mode on post-exercise oxygen consumption. Sports Med. 2003;33:1037–60. https://doi.org/10.2165/00007256-200333140-00002.

    Article  PubMed  Google Scholar 

  40. LaForgia J, Withers RT, Gore CJ. Effects of exercise intensity and duration on the excess post-exercise oxygen consumption. J Sports Sci. 2006;24:1247–64. https://doi.org/10.1080/02640410600552064.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We sincerely thank to Christopher P. Bock for his help running the WRIC studies.

Funding

The main dataset of this analysis was funded by the National Institute of Diabetes and Digestive and Kidney Diseases (DP3DK113358). Additionally, a data subset was funded by Eli Lilly and Company (NCT02211586), NIDDK (R01DK105829) and Nutrition Sciences Initiative (NCT01967563).

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Authors and Affiliations

  1. AdventHealth Translational Research Institute, 301 E. Princeton St., Orlando, FL, 32804, USA

    Elvis A. Carnero, Karen D. Corbin, Anna Casu, Daria Igudesman, Anika Bilal, Steven R. Smith & Richard E. Pratley

  2. Department of Biostatistics, University of North Carolina at Chapel Hill, 3101 McGavran-Greenberg Hall, Chapel Hill, NC, 27599, USA

    Michael R. Kosorok

  3. Department of Pediatrics, Division of Endocrinology, Stanford University, School of Medicine. 300 Pasteur Dr., Stanford, CA, 94305, USA

    David M. Maahs

  4. Stanford Diabetes Research Center, Stanford, CA, 94305, USA

    David M. Maahs

  5. Department of Epidemiology, Stanford University, School of Medicine, Stanford, CA, 94305, USA

    David M. Maahs

  6. Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Elizabeth J. Mayer-Davis

  7. School of Medicine, University of North Carolina at Chapel Hill, 135 Dauer Drive, Chapel Hill, NC, 27599, USA

    Elizabeth J. Mayer-Davis

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Contributions

EAC and REP were involved in the conception, design and the analysis and interpretation of the results. EAC wrote the first draft of the manuscript, and all authors edited, reviewed, and approved the final version of the manuscript. REP is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Correspondence to Elvis A. Carnero.

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All procedures were approved by AdventHealth Institutional Review Board which follows the Declaration of Helsinki for medical research involving human subjects.

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Carnero, E.A., Corbin, K.D., Casu, A. et al. 24-h energy expenditure in people with type 1 diabetes: impact on equations for clinical estimation of energy expenditure. Eur J Clin Nutr (2024). https://doi.org/10.1038/s41430-024-01446-4

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