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The control of partitioning between protein and fat during human starvation: its internal determinants and biological significance

Published online by Cambridge University Press:  09 March 2007

A. G. Dulloo  and
J. Jacquet
A. G. Dulloo*
Affiliation:
Institute of Physiology, University of Fribourg, CH-1700 Fribourg, Switzerland
J. Jacquet
Affiliation:
Computer Unit, Faculty of Medicine, University of Geneva, Switzerland
*
*Corresponding author: Dr Abdul Dulloo, fax +41 26 300 97 34, email [email protected]
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Abstract

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Human subjects vary in the extent to which their body's protein and fat compartments are mobilized for fuel during starvation. Although an inverse association between the initial adiposity and the contribution of protein as fuel during starvation has been known for nearly a century, interest in the quantitative importance and functional significance of the initial percentage fat as a determinant of biological variation in energy-partitioning between protein and fat (and hence in determining the partitioning characteristic of the individual) is relatively recent. The present paper addresses these issues by revisiting the classic Minnesota experiment of semi-starvation and refeeding from a standpoint of system physiology. In a quantitative analysis of the relationship between the initial body composition (ratio FAT0:fat-free mass (FFM)0) and the composition of weight loss (ratio ΔFAT:ΔFFM) in the thirty-two men in the Minnesota study, the arguments are put forward that the fraction of FFM lost when the fat stores reach total depletion is independent of the initial percentage fat, and that this fraction represents the ‘dispensible’ component of the protein compartment that is compatible with life (i.e. the protein energy-reserve, rp). The concepts are developed that (1) the initial percentage body fat (which reflects the initial ratio FAT0:FFM0) provides a ‘memory of partitioning’ which dictates the control of partitioning between protein and fat in such a way that both the protein energy-reserve (rp) and the fat energy-reserve (rf) reach complete depletion simultaneously, a strategy that would ensure maximum length of survival during long-term food scarcity, and that (2) variability in the relative sizes of these two energy reserves (i.e. in rf:rp) could, in addition to the initial percentage fat, also contribute to human variability in energy-partitioning. The basic assumptions underlying this re-analysis of the Minnesota data, and the concepts that are derived from it, have been integrated in the simple mathematical model for predicting the partitioning characteristic of the individual. This model is used to explain how variability in the fraction of the protein compartment that could function as an energy reserve (rp) can be as important as the initial percentage fat in determining inter-individual variability in protein-sparing during the early phase of starvation, in fuel partitioning during prolonged starvation, or in the maximum percentage weight loss during starvation. The elucidation of factors underlying variability in the size of the protein energy-reserve may have important implications for our understanding of the pathophysiology of starvation and age-associated susceptibility to muscle wasting, and in the clinical management of cachexia and obesity.

Keywords

CachexiaObesityMalnutritionEnergy metabolismBody composition
Type
Review – hypothesis article
Information
British Journal of Nutrition , Volume 82 , Issue 5 , November 1999 , pp. 339 - 356
Copyright
Copyright © The Nutrition Society 1999

References

Allison, SP (1992) The uses and limitations of nutritional support. Clincial Nutrition 11, 319–330.CrossRefGoogle ScholarPubMed
Armitage, P & Berry, G (1987) Statistical Methods in Medical Research, 2nd ed. Oxford: Blackwell Scientific Publications.Google Scholar
Ashley, BCE & Whyte, HM (1961) Metabolic studies in starvation. Australian Annals of Medicine 10, 92–111.CrossRefGoogle ScholarPubMed
Benedict, FG (1915) A Study of Prolonged Fasting. Carnegie Institute of Washington Publication no. 203, Washington, DC: Carnegie Institute.CrossRefGoogle Scholar
Berkman, JM, Weir, JF & Kepler, EJ (1947) Clinical observations on oedema, serum protein and the effects of forced feeding in anorexia nervosa. Gastroenterology 9, 357–390.Google ScholarPubMed
Bortz, WM, Wroldson, A & Morris, P (1967) Fat, carbohydrate, salt and weight loss. American Journal of Clinical Nutrition 20, 1104–1114.CrossRefGoogle ScholarPubMed
Cahill, GF (1970) Starvation in man. New England Journal of Medicine 282, 668–675.Google ScholarPubMed
Dulloo, AG (1997) Human pattern of food intake and fuel-partitioning during weight recovery after starvation: a theory of autoregulation of body composition. Proceedings of the Nutrition Society 56, 25–40.CrossRefGoogle ScholarPubMed
Dulloo, AG (1998) Partitioning between protein and fat during starvation and refeeding: is the assumption of intra-individual constancy of P-ratio valid? British Journal of Nutrition 79, 107–109.CrossRefGoogle ScholarPubMed
Dulloo, AG & Jacquet, J (1998) Adaptive reduction in basal metabolic rate in response to food deprivation in humans: a role for feedback signal from the fat stores. American Journal of Clinical Nutrition 68, 599–606.CrossRefGoogle ScholarPubMed
Dulloo, AG, Jacquet, J & Girardier, L (1996) Autoregulation of body composition during weight recovery in humans: the Minnesota Experiment revisited. International Journal of Obesity 20, 393–405.Google ScholarPubMed
Dulloo, AG, Jacquet, J & Girardier, L (1997) Poststarvation hyperphagia and body fat overshooting in humans: a role for feedback signals from lean and fat tissues. American Journal of Clinical Nutrition 65, 717–723.CrossRefGoogle ScholarPubMed
Elia, M (1991) Effect of starvation and very low calorie diets on protein–energy interrelationships in lean and obese subjects. In Protein–Energy Interactions, pp. 249–284 [Scrimshaw, NS and Schurch, B, editors]. Lausanne, Switzerland: IDECG.Google Scholar
Elia, M & Parkinson, S (1989) Protein economy during human starvation. European Journal of Clinical Nutrition 43, 139–142.Google ScholarPubMed
Ferro-Luzzi, A, Branca, F & Pastore, G (1994) Body mass index defines the risk of seasonal energy stress in the Third World. European Journal of Clinical Nutrition 48, Suppl. 3, S165–S178.Google ScholarPubMed
Fliederbaum, J (1979) Metabolic changes in hunger disease. In Hunger Disease: Studies by Jewish Physicians in the Warsaw Ghetto. New York, NY: John Wiley & Sons.Google Scholar
Forbes, GB (1987) Lean body mass–body fat interrelationship in humans. Nutrition Reviews 45, 225–231.CrossRefGoogle ScholarPubMed
Forbes, RM, Cooper, AR & Mitchell, HH (1953) The composition of the human body as determined by chemical analysis. Journal of Biological Chemistry 203, 359–366.CrossRefGoogle ScholarPubMed
Forbes, RM, Mitchell, HH & Cooper, AR (1956) Further studies on the gross composition and mineral elements of the adult human body. Journal of Biological Chemistry 223, 969–975.CrossRefGoogle Scholar
Frayn, KN (1996) Metabolic Regulation: A Human Perspective, pp. 166–174. London: Portland Press Ltd.Google Scholar
Gilder, H, Cornell, GN, Grafe, WR, Macfarlane, FR, Asaph, JW, Stubenbord, WT, Watkins, GM, Rees, JR & Thorbjarnarson, B (1967 a) Components of weight loss in obese patients subjected to prolonged starvation. Journal of Applied Physiology 23, 304–310.CrossRefGoogle ScholarPubMed
Gilder, H, Cornell, GN & Thorbjarnarson, B (1967 b) Human energy expenditure in starvation estimated by expired air analysis. Journal of Applied Physiology 23, 297–303.CrossRefGoogle ScholarPubMed
Grande, F (1964) Man under caloric deficiency. In Handbook of Physiology. Adaptation to the Environment, vol. 4, pp. 911–937. Washington, DC: American Physiology Society.Google Scholar
Heitmann, BL (1990) Evaluation of body fat estimated from body mass index, skinfolds and impedence. A comparative study. European Journal of Clinical Nutrition 44, 831–837.Google ScholarPubMed
Henry, CJK (1984) Protein: energy inter-relationships and the regulation of body composition. PhD Thesis, University of London.Google Scholar
Henry, CJK, Ghusain-Choueiri, A & Payne, RR (1998) Energy partitioning between body storage of protein and fat during starvation and refeeding: sources of intra-individual variation of P-ratios. British Journal of Nutrition 79, 109–110.CrossRefGoogle Scholar
Henry, CJK, Rivers, J & Payne, RR (1988) Protein and energy metabolism in starvation reconsidered. European Journal of Clinical Nutrition 42, 543–549.Google ScholarPubMed
Keys, A, Brozek, J, Henschel, A, Mickelson, O & Taylor, HL (1950) The Biology of Human Starvation. Minneapolis, MN: University of Minnesota Press.CrossRefGoogle Scholar
Leiter, A & Marliss, EB (1982) Survival during fasting may depend on fat as well as on protein stores. Journal of the American Medical Association 248, 2306–2307.CrossRefGoogle ScholarPubMed
Le Maho, Y, Robin, JP & Cherel, Y (1988) Starvation as a treatment for obesity: the need to conserve body protein. News in Physiological Science 3, 21–24.Google Scholar
Livesey, G & Elia, M (1988) Estimation of energy expenditure, carbohydrate utilization, and net fat utilization and synthesis by indirect calorimetry: evaluation of errors with special to the detailed composition of fuels. American Journal of Clinical Nutrition 47, 608–628.CrossRefGoogle Scholar
Marliss, EB (1978) The physiology of fasting and semistarvation: roles of 'caloristat' and 'aminostat' mechanisms. In Recent Advances in Obesity Research, vol. 2, pp. 345–369 [Bray, GA, editor]. Westport, CT: Food and Nutrition Press.Google Scholar
Marliss, EB, Aoki, TT, Unger, RH, Soeldner, JS & Cahill, GF (1971) Glucagon levels and metabolic effects in fasting man. Journal of Clinical Investigation 49, 2256–2270.CrossRefGoogle Scholar
McFarlan, D (1991) The Guinness Book of Records. Barcelona, Spain: Guinness Publishing Co.Google Scholar
Meyers, AW (1917) Some morphological effects of prolonged initiation. Journal of Medical Research 36, 51–77.Google Scholar
Millward, DJ & Wijesinghe, DGNG (1998) Energy partitioning and the regulation of body weight. British Journal of Nutrition 79, 111–113.CrossRefGoogle Scholar
Mitchell, PB & Truswell, AS (1987) Body composition in anorexia nervosa and starvation. In Handbook of Eating Disorders, part 1: Anorexia and Bulimia Nervosa, pp. 45–77 [Beumont, PJV, Burrows, GD and Casper, RC, editors]. Amsterdam: Elsevier.Google Scholar
Owen, OE, Morgan, AP, Kemp, HG, Sullivan, JM, Herrera, MG & Cahill, GF (1967) Brain metabolism during fasting. Journal of Clinical Investigation 46, 1589–1595.CrossRefGoogle ScholarPubMed
Passmore, R, Strong, JA & Ritchie, FH (1958) The chemical composition of the tissue lost by obese patients on a reducing regimen. British Journal of Nutrition 12, 113–122.CrossRefGoogle ScholarPubMed
Payne, PR & Dugdale, AE (1977) Mechanisms for the control of body weight. Lancet i, 583–586.CrossRefGoogle Scholar
Prentice, AM, Goldberg, GR, Jebb, SA, Black, AE, Murgatroyd, PR & Diaz, EO (1991) Physiological responses to slimming. Proceedings of the Nutrition Society 50, 441–458.CrossRefGoogle ScholarPubMed
Sokoloff, L (1960) Metabolism of the central nervous system in vivo. In Handbook of Physiology. Section I, Neuro-physiology, pp. 1843–1864. Baltimore, MD: Waverly Press Inc.Google Scholar
Strong, JA, Passmore, R & Ritchie, FJ (1958) Clinical observations on obese patients during a strict reducing regimen. British Journal of Nutrition 12, 105–112.CrossRefGoogle ScholarPubMed
Takahira, H (1925) Metabolism during fasting and subsequent re-feeding. Imperial Government Institute for Nutrition (Tokyo) 1, 63–82.Google Scholar
Voit, E (1901) Die Grösse des Eiweisszerfalles im Hunger (Extent of protein catabolism during starvation). Zeitschrift für Biologie 16, 167–195.Google Scholar