Effect of Reduced

Dietary Intake on Energy Expenditure, and Glucose Cycling in Man

T.P. Stein, W.V. Rumpler,

M.J. Leskiw, M.D. Schluter,

Protein

Turnover,

R. Staples, and C.E. Bodwellt

The effect of a 50% reduction in food intake on energy expenditure, protein metabolism, glucose cycling, and body composition was investigated in eight moderately overweight men. The prestudy mean calorie and protein intake was determined for eight subjects. They were then maintained on this diet for 6 weeks (mean + SEM, 3,269 2 75 kcal/d, 20.0 ? 0.5 g N/d, period I), after which the diet was reduced uniformly in the major foodstuffs by 50% for the next 4 weeks (1,555 + 38 kcal/d, 9.6 2 5 g N/d, period II). At the end of each period we measured (1) body fat and fat free mass by underwater weighing, (2) 24-hour energy expenditure by indirect calorimetry in a calorimeter, (3) whole body protein synthesis and breakdown rates with “N glycine, and (4) glucose cycling between glucose and glucose-6-phosphate and fructose cycling between fructose-g-phosphate and fructose-l,6 bisphosphate with 6,6-D,- and P-D,-labeled glucose. The results were subjects lost 4.0 2 0.1 kg fat (by underwater weighing) during the 4 weeks on the reduced-energy regimen. Protein turnover and glucose cycling were reduced by 20% and 15%. respectively. Twenty-four-hour energy expenditure was 2,553 2 166 kcal/d for period I and 2,369 ? 69 kcal/d for period II, giving a difference of 184 i 34 kcal/d between the two periods. In conclusion, (1) although energy intake was reduced by 50%, the decrease in energy expenditure was small due to the buffering effect of body fat. (2) The reductions in protein turnover and glucose cycling could account for approximately 28% and 7% of the 184-kcal/d difference in energy expenditure between the two periods. Copyright 0 7991 by W.B. Saunders Company

W

THIN LIMITS, humans are able to adapt to low energy diets. Adaptive processes include decreased body mass size, reduced activity, and metabolic adaptations.’ The relative importance of these processes has proven to be difficult to determine. Likely processes for metabolic adaptations are decreased substrate cycling. The term substrate cycling is used to describe the loss and subsequent gain of the same molecules of substrate. The forward and reverse reactions are catalyzed by separate enzymes. Although the actual molecules are conserved, energy is lost because there is a net use of adenosine triphosphate (ATP) in the process. This energy loss may make a significant contribution to energy expenditure. Substrate cycles were initially proposed by Newsholme and Crabtree as being able to serve two metabolic functions: (1) to increase the sensitivity to metabolic regulation, and (2) as a means of disposing of excess energy (futile cycling).’ A number of such cycles have been proposed, for example, the glucose-6-phosphate cycle, fructose-6-phosphate-fructose 1,6 bisphosphate cycle, and the fatty acidtriacylglycerol cycle.’ Protein turnover can also be regarded as a cycle (the amino acid-protein cycle), although not a simple cycle with just one foreword and one back reaction, but rather as the sum of a series of forward and opposing reactions. It is probably the most important cycle in regard to its role in the regulation of metabolism and energy COStS.‘.3

From the Deputiment of Sutgety, University of Medicine and Dent&y of New Jersq-School of Osteopathic Medicine, Camden, NJ; and the Energy and Protein Nutrition Laboratory, US Department of Agriculture, BeltsliNe, MD. Supposed by US Public Health Senice Grant No. DK35612, NASA contract No. NAS9-I 7276, and Internal USDAfunds. f Deceased. Address reprint requests to T.P. Stein, PhD, Department of Surgrry, LJMDNJ-SOM. 401 Haddon Ave. Camden, NJ 08103. Copyright 0 1991 by W.B. Saunders Company 00260495191/4005-0007$03.00/0 478

Numerous studies have reported that protein turnover is reduced with undernutrition.” Klein et al’ and Elia et al” reported that the triacylglycerol-free fatty acid (TG-FFA) cycling is increased with starvation, but there is no information on the effect of energy reduction on the carbohydrate cycles in man. The objectives of this experiment were to investigate the effect of a moderately severe (-50%) energy reduction on glucose cycling, protein turnover, and energy balance. We used the methodology described by Shulman ct al’ and Wolfe et al” for measuring glucose cycling. The single-pulse “N glycine was used for measuring protein synthesis and breakdown.’ Endogenous fat utilization was determined by measuring body fat content by underwater weighing before and after the reduced-energy diet. Twenty-four-hour energy expenditure was measured by whole body calorimetry. METHODS Eight moderately overweight. healthy adult volunteers were studied at the US Department of Agriculture (USDA) human nutrition research facility in Beltsville, MD. Informed consent was obtained in accordance with the policies of the USDA and the University of Medicine and Dentistry of New Jersey. The prestudy mean energy intake was available from a previous study for the eight subjects.“’ They were then maintained on thih diet for 2 to 4 weeks (period I), after which the type of food supplied remained the same. but the amount of each item was reduced by approximately 50% for the next 4 weeks (period II). For the 8 to 10 weeks of dietary control, subjects were allowed to eat only foods provided by the facility. On weekdays. breakfast and dinner were consumed at the facility and a package lunch provided. For weekends. subjects were given prepackaged meals and allowed to eat meals at home. Measurements were made at the end of each period. Body density was determined by underwater weighing combined with simultaneous determination of residual volume.” Body fat was estimated from body density using the Siri equation.” Twenty-fourhour energy expenditure rates were made using a room-sized calorimeter at the beginning and end of the weight reduction period.“‘,” While in the calorimeter, subjects followed a standard Metabokm, Vol40, No 5 (May), 1991:

pp 478-483

ENERGY EXPENDITURE AND SUBSTRATE

CYCLING

479

activity protocol, which was the same for all subjects each time in the calorimeter. Energy expenditure values were reported when energy intake in the calorimeter was the same each time in the chamber and was at the reduced calorie intake level. These values are assumed to be the most representative of the day of the isotope studies The whole body protein synthesis and breakdown rates were measured with “N glycine (ICON, Summit, NJ)” and glucose cycling was determined with 6,6-D:- and 2-D,-labeled glucose (Tracer Technologies, Cambridge, MA).” The Isotope studies lasted 9 hours.‘J The study was started after an overnight fast by (1) having the subject void. (2) taking 6 mL of venous blood from a forearm vein, (3) ingesting a bolus of “N glycine (6 mg/kg). and (4) starting the subjects on half hourly aliquots of Ensure (1.06 kcallkgih, Ross Laboratories, Columbus, OH). E

Effect of reduced dietary intake on energy expenditure, protein turnover, and glucose cycling in man.

The effect of a 50% reduction in food intake on energy expenditure, protein metabolism, glucose cycling, and body composition was investigated in eigh...
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