Human pattern of food intake and fuel-partitioning during weight recovery after starvation: A theory of autoregulation of body composition

A paradox in human bioenergetics today is the contrast between our detailed knowledge of complex biochemical pathways of intermediary metabolism, and the large gap which exists in our understanding of basic physiological laws which govern weight regulation.The widespread application of powerful techniques of molecular biology to nutritional energetics promises to sharpen this contrast even further.A striking example, of particular relevance to the present symposium on Mechanisms of Energy Compensation, is the recent identification of an adipocyte-specific gene (Zhang et al. 1994) whose expression is 'apparently' consistent with the notion of a feedback signal between adipose tissue depletion and compensatory increases in food intake (Flier, 1995; Trayhurn, 1996).Yet, the relative importance of fat depletion as a determinant of post-starvation hyperphagia in human subjects is unknown, and the increase in appetite predicted to occur after lipectomy in animal models has been difficult to demonstrate (Weigle, 1994).On the other hand, the question of whether the depletion of lean tissues can provide a feedback signal on the hunger-appetite drive is rarely a subject for debate, despite evidence that food intake during growth is dominated by the impetus for lean tissue deposition (Webster, 1993), and in spite of the strong arguments put forward by Millward (1995) for the existence of a protein-stat mechanism for the regulation of lean body mass.In fact, a feedback loop between fat depletion and the food intake control centres cannot explain why human subjects recovering weight after a period of energy deprivation continue to overeat well after body weight and body fat have been restored to pre-starvation levels.This phenomenon of post-starvation energy over-compensation and overshoot in body weight, first documented by Benedict (1907) andBenedict et al. (1919) in studies of experimental starvation and refeeding, was subsequently observed during follow-up studies of famine victims of World War I1 (Table 1). THE SWISS FOOD RATIONING 'EXPERIMENT'In Switzerland, when food rationing was implemented in 1941, the physiologist Fleisch was asked by the 'Federal Commission for Wartime Feeding' to monitor the health consequences of this intervention.In addition to the assessment of mortality and morbidity related to cardiovascular, digestive and infectious diseases, the nutritional status was also determined in 700 persons of different ages, social status, and living areas, every 1-2 months between Autumn 1941 and Spring 1946 (Schwaben, 1947).The data collected on food consumption and body weight, compiled and published about 30 years later by Martin & Demole (1973), are shown in Fig. l(a).Food intake and body weight dropped to the lowest level during the summer of 1945.At the end of that year, food rationing was abandoned and products were available again in larger quantities; food consumption and body weight rose rapidly.Of particular interest in these results of food deprivation in freeliving human subjects is that they reveal that even under conditions when food intake was