Lower daily energy expenditure as measured by a respiratory chamber in subjects with spinal cord injury compared with control subjects 1 3

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1 Lower daily energy expenditure as measured by a respiratory chamber in subjects with spinal cord injury compared with control subjects 1 3 Mary Beth Monroe, Pietro A Tataranni, Richard Pratley, Melinda M Manore, James S Skinner, and Eric Ravussin ABSTRACT Background: This study was designed to determine the effect of chronic spinal cord injury on daily energy expenditure. Objective: We hypothesized that both resting and total energy expenditure would be lower in spinal cord injured (SCI) subjects than in control subjects because of lower sympathetic nervous system activity and reduced levels of physical activity in SCI subjects. Design: Twenty-four hour energy expenditure (24-h EE), resting metabolic rate (RMR), sleeping metabolic rate, spontaneous physical activity, the thermic effect of food (TEF), and 24-h respiratory quotient were measured by using a respiratory chamber in 10 male SCI subjects (injury ranged from level C6 to L3) and 59 age-matched, noninjured, male control subjects. Results: The 24-h EE was lower in SCI than in control subjects (7824 ± 305 compared with 9941 ± 188 kj, P < 0.01). After adjustment for fat-free mass, fat mass, and age, 24-h EE was still lower ( 753 kj/d, P < 0.01) in SCI than in control subjects. Spontaneous physical activity measured by a radar system was also significantly lower (4.6 ± 0.6% compared with 6.5 ± 0.3% of time, P < 0.01) in SCI than in control subjects. In absolute value (7347 ± 268 compared with 9251 ± 1326 kj/d, P < 0.01) or after adjustment for fat-free mass, fat mass, and age ( 678 kj/d, P < 0.01), RMR was also lower in SCI than in control subjects. TEF was significantly lower in SCI than in control subjects (987 ± 142 compared with 1544 ± 213 kj/d, representing 12.9% and 15.9% of total energy intake, respectively, P < 0.05). The sleeping metabolic rate and 24-h respiratory quotient did not differ significantly between groups. Conclusions: The 24-h EE was significantly lower in SCI than in control subjects. This difference can be explained by the lower levels of physical activity, and lower RMR and TEF values, in SCI subjects. Am J Clin Nutr 1998;68: KEY WORDS Respiratory chamber, energy expenditure, sympathetic nervous system, spontaneous physical activity, spinal cord injury, thermic effect of food, respiratory quotient INTRODUCTION Individuals with spinal cord injury undergo numerous changes in body composition as a result of their injury. These changes include muscle paralysis, a reduction in lean tissue mass and bone mineral density, and an increase in fat mass (1, 2). Because of the extreme inactivity imposed by acute spinal cord injury and subsequent wheelchair confinement, this population is at increased risk for developing obesity-related disorders such as diabetes (3 5) and cardiovascular disease (6). We showed recently that, compared with sex- and age-matched control subjects, spinal cord injured (SCI) subjects had lower fat-free mass (FFM) and a higher percentage body fat, particularly in the leg region (1). Wilmet et al (2) reported significant reductions in bone and muscle tissue in subjects studied longitudinally for 1 y after spinal injury. Despite reductions in lean tissue and bone mass in these individuals, however, changes in energy expenditure may play a role in the early development of obesity in this population. A reduction in energy expenditure caused by a loss of lean tissue and bone mass may predispose SCI persons to weight gain and obesity in the event that energy intake exceeds daily energy expenditure (2, 7). The level of spinal injury may be an important determinant of energy balance in this population, such that subjects with higher injury levels (ie, those with cervical injuries) would experience the greatest reduction in body mass and daily energy expenditure. In addition, sympathetic nervous system (SNS) activity has been shown to be lower in persons with spinal cord injury than in control subjects (8). All of these factors would be expected to cause reductions in energy expenditure in SCI persons. However, to our knowledge, 24-h energy expenditure (24-h EE) has never been assessed by direct measurement in SCI individuals and, therefore, the long-term effect of spinal cord injury on the components of daily energy expenditure is unknown. Information regarding energy requirements in this population might be useful for determining the daily energy needs of SCI individuals. Earlier studies of energy expenditure in SCI persons used the heart rate method to estimate 24-h EE, which is based on the 1 From the Department of Exercise Science and Physical Education, Arizona State University, Tempe, and the National Institutes of Health, NIDDK, Phoenix, AZ. 2 Supported by NIH grant OH94-DK-P Reprints not available. Address correspondence to MB Monroe, University of Colorado at Boulder, Campus Box 354, Boulder, CO monroem@colorado.edu. Received December 17, Accepted for publication April 14, Am J Clin Nutr 1998;68: Printed in USA American Society for Clinical Nutrition 1223

2 1224 MONROE ET AL relation between heart rate and oxygen consumption (9). However, more reliable and valid measurements are needed to determine energy expenditure in this population because the heart rate response is abnormal in SCI individuals with lesions above T6 (because of a lack of normal innervation of the heart), particularly during exertion (10, 11). Previous studies were performed to measure resting metabolic rate (RMR) in SCI subjects with a ventilated hood system (12, 13). However, no comparison was made with noninjured control subjects; thus, information regarding the effect of spinal injury on daily energy expenditure is unknown. The purpose of the present study was to measure 24-h EE in a group of SCI subjects by using a respiratory chamber and to compare the results with those obtained from age-matched control subjects. We hypothesized that SCI subjects would have reduced resting as well as total daily energy expenditure values as a result of lower overall SNS activity and reduced levels of physical activity. SUBJECTS AND METHODS Subjects Ten male SCI subjects participated in the study. Their injury levels ranged from the sixth cervical (C6) to the third lumbar (L3) vertebra. All subjects were 2 y postinjury (mean time postinjury: 9 ± 2 y). All lesions were complete (Frankel Class A) and none of the subjects had motor or sensory function below the level of the lesion. Injury levels were verified by medical history and sensory-motor examination. Because of the nature of the study, only SCI subjects who could perform their own transfers and activities of daily living were included. As a result, 9 men with paraplegia and 1 highly functional man with quadriplegia participated in the study. All SCI subjects used manually propelled wheelchairs but their physical activity levels (not including time spent in wheelchair locomotion), as determined by a physical activity questionnaire, ranged from completely sedentary (<1 h/wk) to moderately active (3 5 h exercise/wk). Wheelchair exercise activities included basketball, weightlifting, swimming, and arm-crank ergometry. Height was measured with SCI subjects in a supine position, and weight was measured by using a scale adapted for use with wheelchairs. Three SCI subjects with T12 injury levels routinely took medication for the prevention of urinary tract infections. One subject with a cervical (C7) injury took medication to prevent involuntary muscle spasms and one subject with a thoracic (T12) injury took medication to prevent bladder spasms. Subjects who routinely took medication to control involuntary muscle spasms were asked to refrain from taking their medication during their 24-h chamber stay to minimize confounding effects on energy expenditure. Data from 59 age-matched, healthy, male control subjects were retrieved from a database of participants in previous studies at the research unit. Standing height and weight had been measured in control subjects by using standard scales. Data on the physical activity of the control subjects were not available, although, on the basis of maximal oxygen consumption values obtained from previous studies in this subject population, we estimated that most of the control subjects were sedentary. A separate comparison was done by using a group of control subjects (n = 10) matched for age and body weight. However, because results from this separate analysis did not differ from those of the larger comparison, results are presented using the data from the 59 (unmatched) control subjects. All subjects were in good health as determined by physical examination and medical history. Subjects gave written, informed consent before participating in the study, according to the guidelines of the Institutional Review Boards of Arizona State University and the National Institute of Diabetes and Digestive and Kidney Diseases. Energy expenditure measurements All subjects were admitted to the metabolic ward for 2 d and spent 1 d in the respiratory chamber so that 24-h EE, RMR, basal metabolic rate, sleeping metabolic rate (SMR), spontaneous physical activity, the thermic effect of food (TEF), and the 24-hour respiratory quotient could be measured. All subjects were fed a weight-maintenance diet (50% carbohydrate, 30% fat, and 20% protein) for 24 h before and during their chamber stay. Procedures for the respiratory chamber were described in detail previously (14). Measurements of carbon dioxide production and oxygen consumption were performed continuously from 0800 to 0700 the following day and calculated energy expenditure was extrapolated to 24 h. The basal metabolic rate was measured by using a ventilated hood system and measurements were taken for 21 min beginning at 0715 with subjects lying quietly in bed after an overnight fast. The SMR was defined as the average energy expenditure of all 15- min periods between 2300 and 0500 (extrapolated to 24 h) when the radar revealed that subjects were active <1.5% of the time. The level of spontaneous physical activity in the respiratory chamber was assessed by using 2 microwave radar sensors (MICD 930; Honeywell, Minneapolis), as described previously (15). These sensors emit signals continuously and the frequency of the signal changes when it hits a moving object, according to the Doppler principle. The output of radar sensors was averaged over a 15-min period such that one activity unit (expressed as a percentage) represents the proportion of time during which the subject was moving. For example, an average activity value of 5% over 24 h would correspond to 72 min of continuous motion. Note that this system measures motion only (including involuntary muscle spasms in SCI individuals) and does not account for differences in work intensity. Vigorous exercise, smoking, and caffeine consumption were not permitted in the chamber. Each subject s RMR was determined on the basis of the relation between physical activity in the chamber and energy expenditure, as described previously (14). The intercept of the linear regression between energy expenditure and physical activity represents the energy expenditure value at the level of zero physical activity (ie, RMR), and provides an accurate representation of each subject s resting energy expenditure averaged over the 24-h period. This measurement includes the basal metabolic rate plus energy expenditure due to TEF. TEF was calculated over a 15-h period for each subject by using the method proposed by Schutz et al (15, 16). Body composition Body composition was measured by dual-energy X-ray absorptiometry (DXA) in all SCI subjects and in 33 control subjects by using a total-body scanner (DPX-1, software version 1.3z; Lunar Radiation Corp, Madison, WI). Nonbone fat-free soft tissue, fat soft tissue, bone mineral content, and percentage body fat were measured. Subject position and scan procedures were similar to those described by Mazess et al (17). In the remaining

3 ENERGY EXPENDITURE IN SPINAL CORD INJURED SUBJECTS control subjects, body composition had been estimated by hydrodensitometry. Hydrodensitometry had been performed with simultaneous determination of lung residual volume, and percentage body fat, FFM, and fat mass were calculated with the equations of Siri (18). Values of FFM used for all analyses included bone mineral content as well as nonbone fat-free tissue so that we could compare results obtained from DXA and hydrodensitometry. Results from our laboratory have previously shown close agreement between percentage body fat, FFM, and fat mass values estimated by hydrodensitometry and DXA (19). Statistical analyses All data were analyzed by using procedures from the SAS Institute (Cary, NC). Values of height, weight, fat mass, FFM (eg, bone mineral content and nonbone fat-free tissue), and percentage body fat were compared between SCI and control subjects by using Student s t tests. The energy expenditure results were compared between SCI and control subjects by using the general linear model procedure with the covariates of FFM, fat mass, and age, as described previously by Ravussin and Bogardus (20). The 24-h respiratory quotient values were also compared between SCI and control subjects by using an analysis of covariance after percentage body fat and energy balance were adjusted for on the day of measurement. Results are expressed as means ± SDs. The significance level was set at P < RESULTS Physical characteristics of the subjects are presented in Table 1. There were no significant differences between SCI and control subjects for height or percentage fat, but control subjects were significantly heavier (P < 0.01). In terms of body composition, the groups did not differ significantly in fat mass but control subjects had more FFM than SCI subjects (P < 0.001). Unadjusted energy expenditure values are presented in Table 2. In absolute value (Table 2) and after adjusting for age, FFM, and fat mass ( 753 kj/24 h, P < 0.01; Figure 1), 24-h EE was significantly lower in SCI than in control subjects. Spontaneous physical activity (P < 0.01), RMR (P < 0.01), and SMR (P < 0.05) were also significantly lower in SCI than in control subjects. After FFM, fat mass, and age were adjusted for, RMR was still lower ( 678 kj/24 h, P < 0.01; Figure 2) in SCI subjects whereas SMR did not differ significantly between groups. Energy intake was lower ( 1105 kj/24 h, P < 0.05) in SCI subjects during the chamber stay because of the experimental design in which energy intake was calculated on the basis of body mass. TEF was found to be significantly lower in SCI than in control subjects (987 compared with 1544 kj, representing 12.1% and 15.3% of total TABLE 1 Physical characteristics of control and spinal cord injured male subjects 1 Control (n = 59) Spinal cord injured (n = 10) Age (y) 31.9 ± ± 8.0 Height (cm) ± ± 5.4 Weight (kg) 89.9 ± ± Fat-free mass (kg) 64.1 ± ± Fat mass (kg) 25.8 ± ± 11.9 Percentage body fat (%) 26 ± ± 12 1 x ± SD. 2,3 Significant effect of group (t test): 2 P < 0.01, 3 P < energy intake, respectively, P < 0.05). The mean 24-h respiratory quotient did not differ significantly between groups. DISCUSSION In this study we found a lower daily energy expenditure in SCI individuals than in control subjects. This lower energy expenditure in SCI persons can be explained by lower values of spontaneous physical activity, RMR, FFM, and TEF. It has long been assumed that the reduced energy expenditure in the SCI population is due to lower physical activity levels as a result of wheelchair confinement, as well as to lower FFM. Reductions in 24-h EE would be expected on the basis of the relative inactivity imposed on these individuals combined with reductions in FFM; however, this has not been shown experimentally. In our study the measured reduction in 24-h EE was independent of differences in body weight and body composition between the 2 groups. The magnitude of the reduction in 24-h EE in SCI subjects was 750 kj/24 h compared with that of control subjects; this can be explained, in part, by the lower levels of spontaneous physical activity in SCI subjects. The amount of daily energy expenditure that can be accounted for by differences in physical activity level can be calculated as the product of the spontaneous physical activity and the slope of the linear regression line between energy expenditure and physical activity, as described previously (15). The slope of the regression line gives a value of energy expenditure per unit physical activity. Thus, energy expenditure due to physical activity can be calculated for each group, and the difference between these 2 values represents the difference in 24-h EE that can be attributed to physical activity. With this method, it can be estimated that 250 kj/d can be accounted for by differences in physical activity between the groups. Note that the respiratory chamber is not the ideal condition for detecting differences between groups in physical activity levels because subjects are restricted to a small area and are therefore not under free-living conditions. In free-living conditions, it is likely that the difference in total energy expenditure between the 2 groups would have been much greater because differences in components other than spontaneous physical activity would have become more apparent (21, 22). Studies using doubly labeled water techniques would provide additional quantitative information about reductions in total daily physical activity levels in SCI TABLE 2 Unadjusted energy expenditure values for control and spinal cord injured male subjects 1 Control Spinal cord injured Energy variable (n = 59) (n = 10) Energy intake (kj/24 h) 9745 ± ± h Energy expenditure (kj/24 h) 9941 ± ± Resting metabolic rate (kj/24 h) 9251 ± ± Sleeping metabolic rate (kj/24 h) 6933 ± ± Spontaneous physical activity 6.5 ± ± (%/24 h) Thermic effect of food 15.3 ± ± (% of energy intake) 24-h Respiratory quotient 0.87 ± ± x ± SD. 2 4 Significant effect of group (SAS general linear models procedure): 2 P < (by design because subjects were fed on the basis of body weight), 3 P < 0.01, 4 P < 0.05.

4 1226 MONROE ET AL FIGURE 1. Relation between fat-free mass and unadjusted values of 24-h energy expenditure in spinal cord injured (SCI, ) and noninjured control ( ) subjects. The regression line (y = 132x ; r = 0.82, P < 0.05) is shown for control subjects. Daily energy expenditure was reduced in SCI subjects. After adjustment for fat-free mass, fat mass, and age, 24-h energy expenditure was, on average, 753 kj/d lower in SCI subjects than in control subjects (P < 0.01). persons under free-living conditions. In addition, note that the SCI subjects in the present study were necessarily highly mobile individuals: a requirement for participation was that subjects be able to perform their own transfers and all activities of daily living. Methodologic constraints prevented us from including more disabled individuals (eg, those with higher injury levels such as persons with high quadriplegia), who would be expected to have even greater reductions in total daily physical activity levels. RMR was significantly lower in SCI subjects in absolute value and after FFM, fat mass, and age were adjusted for. This suggests that reductions in peripheral SNS activity in these individuals may lead to a reduction in the overall metabolic rate and supports previous findings of a lower RMR in persons with reduced SNS activity (23 25). Spraul et al (23) reported that SNS activity, as measured by muscle sympathetic nerve activity, correlated with RMR in healthy, white subjects. In a similar study, Saad et al (24) used 24-h urinary norepinephrine measurements to confirm the relation between SNS activity and RMR. They concluded that individuals with lower SNS activity may be at greater risk for weight gain because of a lower metabolic rate. A second factor that may have contributed to the reduced 24- h EE in the SCI subjects was a lower TEF, both in absolute terms and relative to energy intake. TEF is defined as an increase in energy expenditure in response to food intake (26). It has been estimated that the TEF can be as high as 18% of energy intake when calculated over a 24-h period in the respiratory chamber (27). In the present study, TEF was 15% and 12% of energy intake for control and SCI subjects, respectively, which agrees with values reported previously (16, 27). On the basis of these values, it can be calculated that 188 kj of the difference in 24-h EE was the result of a greater TEF in control subjects. The finding of a reduced TEF in SCI subjects compared with control subjects does not agree with previous findings by Aksnes et al (28). Using a short-duration (2 h) method for determining the thermic response to a standardized mixed meal (40% of basal 24-h energy requirements), these authors FIGURE 2. Relation between fat-free mass and unadjusted values of resting metabolic rate in spinal cord injured (SCI, ) and noninjured control ( ) subjects. The regression line (y = 114x ; r = 0.78, P < 0.05) is shown for control subjects. On average, the resting metabolic rate was 678 kj/d lower in SCI subjects than in control subjects (P < 0.01). found no difference in the TEF between 9 quadriplegic men and 6 healthy, male control subjects. The TEF was measured in the present study under physiologic conditions and over a longer period of time with subjects consuming normal meals (27). Results from the present study support the hypothesis that central activation of the sympathoadrenal system plays a role in stimulating nutrient-induced thermogenesis. Previous studies (8) have shown lower SNS activity, as measured by microneurography, in SCI subjects than in healthy control subjects. It is generally accepted that central activation of the sympathoadrenal system is an essential component of the mechanism whereby food ingestion stimulates resting energy expenditure (26, 29). Several studies have shown that TEF is reduced by -blockade (29 31). Acheson et al (30) showed a significant reduction in the thermic effect of infused glucose after -adrenergic blockade with propranolol. These authors concluded that -adrenergically mediated SNS activity is responsible for almost the entire rise in energy expenditure in excess of the obligatory requirements for processing and storing glucose in healthy men. On the basis of these findings, it is reasonable to assume that the process of nutrient-induced thermogenesis should be defective in SCI patients, who have a disruption in neural pathways between the central nervous system and peripheral sympathetic nerves. Our results support this hypothesis. The fact that SMR did not differ between the 2 groups after FFM and fat mass were adjusted for is surprising in light of the significantly lower RMR in the SCI subjects. A lower metabolic rate as a result of reduced SNS activity would be expected to cause lower SMR values as well. One explanation for this discrepancy may be differences in sleeping patterns between the 2 groups. Many SCI subjects reported the need to perform frequent postural adjustments during the night and many also experienced involuntary muscle spasms. Both of these factors could serve to increase the SMR, negating any reductions caused by lower sympathetic outflow to the lower part of the body. As a result, these potential confounders may have diminished our chance to detect differences in metabolic rate during sleep.

5 ENERGY EXPENDITURE IN SPINAL CORD INJURED SUBJECTS 1227 In conclusion, the current study showed a significantly lower total and resting energy expenditure in SCI than in healthy control subjects. This lower energy expenditure was independent of differences in body composition and can be explained by lower levels of spontaneous physical activity and a smaller TEF in SCI subjects. A reduction in SNS activity, as a result of spinal injury, may have contributed to a lower metabolic rate in this population. We thank the nurses, metabolic kitchen, and technical staff of the Clinical Diabetes and Nutrition Section and, in particular, the individuals who volunteered for this study. REFERENCES 1. Monroe M. Energy metabolism and adipose tissue lipolysis in spinal cord injured and non-injured control subjects. PhD dissertation. Arizona State University, Tempe, AZ, Wilmet E, Ismail AA, Heilporn A, Welraeds, Bergmann P. Longitudinal study of the bone mineral content and of soft tissue composition after spinal cord section. Paraplegia 1995;33: Bauman WA, Spungen AM. Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. J Clin Invest 1990;85: Duckworth WC, Solomon SS, Jallepalli P, Heckemeyer C, Finnern J, Powers A. Glucose intolerance due to insulin resistance in patients with spinal cord injury. Diabetes 1980;29: Ohlson LO, Larsson B, Svardsudd K. The influence of body fat distribution on the incidence of diabetes mellitus: 13.5 years of followup of the participants in the study of men born in Diabetes 1985;34: Krum H, Howes LG, Brown DJ, et al. Risk factors for cardiovascular disease in chronic spinal cord injury patients. Paraplegia 1992;30: Ravussin E, Lillioja S, Knowler WC, et al. Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med 1988;318: Stjernberg L, Blumberg H, Wallin BG. Sympathetic activity in man after spinal cord injury: outflow to muscle below the lesion. Brain 1986;109: Yamasaki M, Irizawa M, Komura T, et al. Daily energy expenditure in active and inactive persons with spinal cord injury. J Hum Ergol (Tokyo) 1992;21: Glaser RM. Exercise and locomotion for the spinal cord injured. Exerc Sport Sci Rev 1985;15: Palmer-McLean K, Jones, PP, Skinner JS. Exercise prescription for sitting and supine exercise in subjects with quadriplegia. Med Sci Sports Exerc 1995;27: Mollinger LA, Spurr GB, El Ghatit AZ, et al. Daily energy expenditure and basal metabolic rates of patients with spinal cord injury. Arch Phys Med Rehabil 1985;66: Sedlock DA, Laventure SJ. Body composition and resting energy expenditure in long term spinal cord injury. Paraplegia 1990;28: Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man: methods and results using a respiratory chamber. J Clin Invest 1986;78: Schutz Y, Ravussin E, Diethelm R, Jequier E. Spontaneous physical activity measured by radar in obese and control subjects studied in a respiration chamber. Int J Obes 1982;6: Schutz Y, Bessard T, Jequier E. Diet-induced thermogenesis measured over a whole day in obese and nonobese women. Am J Clin Nutr 1984;40: Mazess RB, Barden HS, Bisek JP, Hanson J. Dual-energy x-ray absorptiometry for total-body and regional bone-mineral and softtissue composition. Am J Clin Nutr 1990;51: Siri WE. Body composition from fluid density: analysis of methods. In: Brozek J, Herschel A, eds. Techniques for measuring body composition. Washington, DC: National Research Council, 1961: Tataranni PA, Ravussin E. Use of dual-energy X-ray absorptiometry in obese individuals. Am J Clin Nutr 1995;62: Ravussin, E, Bogardus C. Relationship of genetics, age and physical fitness to daily energy expenditure and fuel utilization. Am J Clin Nutr 1989;49: Ravussin E, Rising R. Daily energy expenditure in humans: measurements in a respiratory chamber and by doubly-labeled water. In: Kinney JM, Tucker HN, eds. Energy metabolism: tissue determinants and cellular corollaries. New York: Raven Press, 1992: Seale JL, Rumpler WV, Conway JM, Miles MW. Comparison of doubly labeled water, intake-balance, and direct- and indirectcalorimetry methods for measuring energy expenditure in adult men. Am J Clin Nutr 1990;52: Spraul M, Ravussin E, Fontvielle AM, Rising R, Larson DE, Anderson EA. Reduced sympathetic nervous activity. A potential mechanism predisposing to body weight gain. J Clin Invest 1993;92: Saad MF, Alger SA, Zurlo F, Young JB, Bogardus C, Ravussin E. Ethnic differences in sympathetic nervous system-mediated energy expenditure. Am J Physiol 1991;261:E Ravussin E. Low resting metabolic rate as a risk factor for weight gain: role of the sympathetic nervous system. Int J Obes 1995; 19(suppl):S Jequier E, Schutz Y. Energy expenditure in obesity and diabetes. Diabetes Metab Rev 1988;4: Tataranni PA, Larson DE, Snitker S, Ravussin E. Thermic effect of food in humans: methods and results from use of a respiratory chamber. Am J Clin Nutr 1995;61: Aksnes AK, Brundin T, Hjeltnes N, Maehlum S, Wahren J. Mealinduced rise in resting energy expenditure in patients with complete cervical spinal cord lesions. Paraplegia 1993;31: Astrup A, Bulow J, Christensen NJ, Madsen J, Quaade F. Facultative thermo-genesis induced by carbohydrate: a skeletal muscle component mediated by epinephrine. Am J Physiol 1986;250: E Acheson KJ, Ravussin E, Wahren J, Jequier E. Thermic effect of glucose in man: obligatory and facultative thermogenesis. J Clin Invest 1984;74: Thorin D, Golay A, Simonsen C, Jequier E, Felber JB. The effect of selective -adrenergic blockade on glucose-induced thermogenesis in man. Metabolism 1986;35:524 8.