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Phenotyping in clinical nutrition

Issues related to the assessment of energy balance during short-term over-, under- and refeeding in normal weight men

Abstract

Background

In humans, it is unclear how different estimates of energy balance (EB) compare with each other and whether the resulting changes in body weight (bw) and body composition (BC) are predictable and reproducible.

Methods

This is a secondary data analysis of effects of sequential 7d over- (OF), 21d under- (UF) and 14d refeeding (RF) on EB. Energy intake (EI) was controlled at +/− 50% of energy needs in a 32 normal weight men (see Am J Clin Nutr. 2015; 102:807–819). EB was calculated (i) directly from the difference between EI and energy expenditure (EE) and (ii) indirectly from changes in BC. Changes in fat mass (FM) were compared with predicted changes according to Hall et al. (Lancet 2011; 378:826–37). Finally, within-subject reproducibility of changes in bw and BC was tested in a subgroup.

Results

There were interindividual and day-by-day variabilities in changes in bw and BC. During OF and RF, the two estimates of EB were similar while with UF the indirect approach underestimated the direct estimate by 10593 ± 7506 kcal/21d (p < 0.001). Considerable differences became evident between measured and predicted changes in FM. Adjusting measured for predicted values did not reduce their interindividual variance. During UF, changes in bw and BC were reproducible, while corresponding changes during OF were not.

Conclusion

During hypercaloric nutrition the direct estimate of EB corresponded to the indirect estimate whereas this was not true during UF. Changes in bw and BC in response to OF were not reproducible while they were during UF.

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Fig. 1: Changes in body weight.
Fig. 2: Apparent macronutrient balances during overfeeding (upper panel), underfeeding (middle panel) and refeeding (lower panel) assessed in 32 healthy, young normal weight men.
Fig. 3: Reproducibility of changes in body weight, fat mass (FM) and fat-free mass (FFM) in a subgroup of 8 of the 32 healthy young men undergoing 7 d overfeeding (at +50% of individual energy needs) followed by 7 d underfeeding (at −50% of individual energy needs).

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References

  1. Hall KD, Farooqi IS, Friedman JM, Klein S, Loos RJF, Mangelsdorf DJ, et al. The energy balance model of obesity: beyond calories in, calories out. Am J Clin Nutr. 2022;115:1243–54.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hall KD, Heymsfield SB, Kemnitz JW, Klein S, Schoeller DA, Speakman JR. Energy balance and its components: implications for body weight regulation. Am J Clin Nutr. 2012;95:989–94.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Jebb SA, Murgatroyd PR, Goldberg GR, Prentice AM, Coward A. In vivo measurement of changes in body composition: description of methods and their validation against 12d continuous whole-body calorimetry. Am J Clin Nutr. 1993;58:455–62.

    Article  CAS  PubMed  Google Scholar 

  4. Müller MJ, Bosy-Westphal A, Lagerpusch M, Heymsfirld SB. Use of balance methods for assessment of short-term changes in body composition. Obesity. 2012;20:701–7.

    Article  PubMed  Google Scholar 

  5. Hall KD. Modeling metabolic adaptations and energy regulation in humans. Ann Rev Nutr. 2012;32:35–54.

    Article  CAS  Google Scholar 

  6. Müller MJ, Body-Westphal A. Effect of over- and underfeeding on body composition and related metabolic functions in humans. Curr Diab Rep. 2019; https://doi.org/10.1007/s11892-019-1221-7.

  7. Müller MJ, Heymsfield SB, Bosy-Westphal A. Are metabolic adaptations to weight changes an artefact? Am J Clin Nutr. 2021;114:1386–95.

    Article  PubMed  Google Scholar 

  8. Shetty P. Adaptation to low energy intakes: the responses and limits to low intakes in infants, children and adults. Eur J Clin Nutr. 1999;53:S14–33.

    Article  PubMed  Google Scholar 

  9. Bray GA, Bouchard C. The biology of human overfeeding: a systematic review. Obes Rev. 2020;21:e13040.

    Article  CAS  PubMed  Google Scholar 

  10. Müller MJ, Enderle J, Pourhassan M, Braun W, Eggeling B, Lagerpusch M, et al. Metabolic adaptation to caloric restriction and subsequent refeeding: the Minnesota Starvation Experiment revisited. Am J Clin Nutr. 2015;102:807–19.

    Article  PubMed  Google Scholar 

  11. Hall KD, Sacks G, Chandramohan D, Chow CC, Wang YC, Gortmaker SL, et al. Quantification of the effect of energy imbalance on bodyweight. Lancet. 2011;378:826–37.

    Article  PubMed  Google Scholar 

  12. Elia M, Livesey G. Theory and validity of indirect calorimetry during net lipid synthesis. Am J Clin Nutr. 1988;47:591–607.

    Article  CAS  PubMed  Google Scholar 

  13. Kahlhöfer J, Lagerpusch M, Enderle J, Eggeling B, Braun W, Pape D, et al. Carbohydrate intake and glycemic index affect substrate oxidation during a controlled weight cycle in healthy men. Eur J Clin Nutr. 68:1060–6.

  14. Bosy-Westphal A, Müller MJ. Assessment of fat and lean mass by quantitative magnetic resonance: a future technology of body composition research? Curr Opin Clin Nutr Metab Care. 2015;18:446–51.

    Article  PubMed  Google Scholar 

  15. Lemos T, Gallagher D. Current body composition measurement techniques. Curr Opin Endocrinol Diabetes Obes. 2017;24:310–4.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Myint KS, Napolitano A, Miller SR, Murgatroyd PR, Elkhawad M, Nunez DJ, et al. Quantitative Magnetic Resonance (QMR) longitudinal evaluation of body composition changes with two dietary regimens. Obesity. 2010;18:391–6.

    Article  Google Scholar 

  17. Bosy-Westphal A, Danielzik S, Becker C, Geisler C, Onur S, Korth O, et al. Need for optimal body composition data analysis using Air Displacement Plethysmography in children and adolescents. J Nutr. 2005;135:2257–62.

    Article  CAS  PubMed  Google Scholar 

  18. Hall KD. Estimating human energy intake using mathematical models. Am J Clin Nutr. 2014;100:806–12.

    Article  Google Scholar 

  19. Gillmore A, Ravussin E, Bray GA, Han H, Redman L. An objective estimate of energy intake during weight gain using the intake-balance method. Am J Clin Nutr. 2014;100:806–12.

    Article  Google Scholar 

  20. Southgate DAT, Durnin JVGA. Calorie conversion factors. An experimental reassessment of the factors used in the calculation of the energy value of human diets. Br J Nutr. 1970;24:517–35.

    Article  CAS  PubMed  Google Scholar 

  21. Emery PW Protein. Digestion and absorption of protein and nitrogen balance. In: Encyclopedia of Food Sciences and Nutrition, 2nd ed. (L Trugo, PM Finglas, B Caballero ed.) Elsevier Science, Amsterdam, NL, 2003.

  22. Jequier E, Acheson K, Schutz Y. Assessment of energy expenditure and fuel utilization in man. Ann Rev Nutr. 1987;7:187–208.

    Article  CAS  Google Scholar 

  23. Hall KD. Body fat and fat-free mass inter-relationships: Forbes’s theory re-visited. Br J Nutr. 2007;97:1059–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Forbes GB. Lean body mass-body fat interrelation in humans. Nutr Rev. 1987;45:225–31.

    Article  CAS  PubMed  Google Scholar 

  25. Dulloo AG, Jacquet J. The control of partitioning between protein and fat during human starvation: its internal determinants and biological significance. Br J Nutr. 1999;81:339–56.

    Article  Google Scholar 

  26. Hall KD. What is the required energy deficit per unit weight loss. Int J Obes. 2008;32:573–6.

    Article  CAS  Google Scholar 

  27. Stubbs RJ, Harbron CG, Murgatroyd PR, Prentice AM. Covert manipulation of dietary fat and energy density: effect on substrate flux and food intake in men eating ad libitum. Am J Clin Nutr. 1995;62:316–29.

    Article  CAS  PubMed  Google Scholar 

  28. Galgani J, Ravussin E. Energy metabolism, fuel selection and body weight regulation. Int J Obes. 2008;32:S109–19.

    Article  CAS  Google Scholar 

  29. Flatt JP. Mc Collum Award Lecture, 1995: Diet, lifestyle and weight maintenance. Am J Clin Nutr. 1995;62:820–36.

    Article  CAS  PubMed  Google Scholar 

  30. Hall KD, Guo J, Chen KY, Leibel RL, Reitman ML, Rosenbaum M, et al. Methodological considerations for measuring energy expenditure differences between diets varying in carbohydrate using the doubly labeled water method. Am J Clin Nutr. 2019;109:1328–34.

    Article  PubMed  PubMed Central  Google Scholar 

  31. De Jonge L, DeLany JP, Nguyen T, Howard J, Hadley EC, Redman LM, et al. Validation of energy expenditure and intake during caloric restriction using doubly labelled water and changes in body composition. Am J Clin Nutr. 2007;85:73–9.

    Article  PubMed  Google Scholar 

  32. Bosy-Westphal A, Deurenberg P, Müller MJ. Body composition. In: Introduction in Human Nutrition, 3rd ed., The Nutrition Society by SA Lanham-New, Hill, TR, Gallagher AM abd Vorster HH (Eds.), John Wiley & Sons Ltd. (Hoboken, USA), 2020; pp 85–112.

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Funding

The study was funded by a grant of the Germany Ministry of Education and Research (BMBF 0315681) and the German Research Foundation (DFG Bo 3296/1-1). Data described in the manuscript, code book, and analytic code cannot be made available because the strict German Data Protection law.

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MJM had the idea and the concept together with ABW. ABW, MJM, WB contributed to data analyses. MJM wrote the 1st version of the manuscript. All authors added to the discussion of the results, the final version and the approval of this manuscript.

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Correspondence to Manfred J. Müller.

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Müller, M.J., Braun, W., Enderle, J. et al. Issues related to the assessment of energy balance during short-term over-, under- and refeeding in normal weight men. Eur J Clin Nutr 77, 538–545 (2023). https://doi.org/10.1038/s41430-022-01208-0

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