Metabolizable energy intake during long-term calorie restriction in rhesus monkeys☆,☆☆
Introduction
Calorie restriction (CR) without malnutrition has been shown to delay aging and attenuate age-related diseases in various organisms (Weindruch and Walford, 1988, Hunt et al., 2006). Reduced energy intake rather than a reduction in any specific macronutrient has been shown to be the primary cause of the life span extension (Iwasaki et al., 1988, Masoro, 1988). CR’s ability to retard aging has been attributed to many reasons including a decrease in the metabolic rate (Harman, 1981) and associated reduction in oxidative damage (Bevilacqua et al., 2004, Masoro et al., 1991, Sohal and Weindruch, 1996). Although it is well established that an acute decrease in energy intake decreases lean mass-adjusted metabolic rate (McCarter, 1991, McCarter et al., 1985, McCarter and McGee, 1989), it is still debated whether this reduction is maintained during long-term CR or if the long-term reduction is explained by a decrease in body and organ mass (Gallagher et al., 1998).
While the effects of reduced energy intake have been studied extensively, many studies have estimated the degree of restriction based on the degree of reduction in the mass of diet that disappears from the food holder. This, however, may not accurately reflect the true degree of restriction. For example, it is known that the energy released when food is completely combusted in a bomb calorimeter does not exactly equal the metabolic energy provided to the body due to digestibility and incomplete utilization – i.e. energy losses in urine and feces. This reduction in energy available to the body has given rise to the term ‘metabolizable energy’ (ME), which is defined as the energy available to the body after correcting for losses in urine and feces (Moe, 1994). The systematic approach to measuring metabolizable energy was refined by Atwater and coworkers as extensively discussed in USDA Handbook #74 (Merrill and Watt, 1973). This body of work resulted in the determination of the general Atwater factors, which are the well-known values of 4, 9, and 4 kcal/g of metabolizable energy for average dietary carbohydrate, fat and protein, respectively. In addition, specific Atwater factors for the macronutrients in specific foods have been developed for an increasingly wide range of food items.
Calorie restriction in itself may also influence the metabolizable energy of a diet. Long-term CR has been shown to cause a variable decrease in the organ masses (Weindruch and Sohal, 1997) including intestinal mass which decreases to a greater extent than the degree of restriction (Weindruch and Sohal, 1997, Greenberg, 1999, Greenberg and Boozer, 2000). This decrease in intestinal mass could lead to a decrease in absorption of nutrients (Karasov et al., 2004). Notwithstanding, the feeding behavior in CR monkeys is such that all the food given to them is eaten in a relatively short amount of time followed by long post-absorptive periods. This may lengthen the transit time in the gut leading to better absorption of nutrients. Published data, however, is lacking with regard to either of these hypothesized effects of long-term CR on the absorption of nutrients.
The main aim of this study was to accurately determine the difference in metabolizable energy intake between CR and C monkeys. We assessed the effects of reduced food intake on the digestibility and metabolizability of food by measuring the waste energy in two consecutive 24-h urinary and fecal collections in 23- to 29-year-old male monkeys. We also tested the accuracy of the estimates metabolizable energy by comparing the results against measured energy expenditure and changes in body composition.
Section snippets
Animals
Twenty (n = 11, CR; n = 9, C) late middle aged (23–29 years old) rhesus monkeys (Macaca mulata) that are part of an ongoing, long-term (14 y) caloric restriction study (Ramsey et al., 1997) were studied. When the study was initiated, the CR group was restricted by 30% based on individually measured food intake prior to the imposition of CR. During the subsequent 14 years, the control group has reduced its voluntary energy intake and the weight of diet provided to the CR group was reduced
Results
Table 1 summarizes the characteristics of the animals at the time of this study (year 14 of CR). The two groups were of similar age and the CR monkeys had significantly lower mean body weight than the C monkeys at the time of this study (p < 0.001).
Discussion
We have demonstrated that although use of weight of food disappearance provides a good measure of the level of CR, the estimate of metabolizable energy intake was in error in that it slightly overestimated the degree of energy restriction. The correction factors are individually small, but together do influence the true metabolizable energy intake values. These factors include feed moisture content, unmeasured food spillage, and energy lost in body waste.
Had we estimated the energy intakes
Acknowledgements
The authors gratefully acknowledge the excellent technical assistance provided by J.A. Adriansjach, C.E. Armstrong and the animal care and veterinary staff of the Wisconsin National Primate Research Center.
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This work was supported by Grants P01 AG-11915 to R. Weindruch and P51 RR000167 to the Wisconsin National Primate Research Center, University of Wisconsin, Madison. This research was conducted in part at a facility constructed with support from Research Facilities Improvement Program Grant Nos. RR15459-01 and RR020141-01.
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There are no conflicts of interest and no online supplementary material.