Differences in resting metabolic rate between paraplegic and able-bodied subjects are explained by differences in body composition

¹ From the Departments of Nutritional Sciences (ACB and PBP), Medicine (CFM), and Pediatrics (PBP), University of Toronto; The Research Institute, The Hospital for Sick Children, Toronto (ACB and PBP); and the Toronto Rehabilitation Institute (CFM).

² Supported in part by the Ontario Neurotrauma Foundation (ONBO-00026). Nestle Canada Inc provided the Carnation Instant Breakfast.

³ Address reprint requests to PB Pencharz, Room 8263, Division of Gastroenterology and Nutrition, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario M5G 1X8. E-mail: paul.pencharz{at}sickkids.ca.

ABSTRACT  
Background: Little is known about the relation between body composition and energy metabolism in paraplegia.

Objective: We investigated the relation between body composition and energy metabolism in healthy paraplegics as compared with able-bodied control subjects. We hypothesized that paraplegics would have lower fat-free mass (FFM), body cell mass (BCM), resting metabolic rate (RMR), and thermic effect of feeding (TEF).

Design: This cross-sectional study included 34 control subjects and 28 paraplegics (mean age: 29.1 ± 7.6 and 33.9 ± 9.2 y, respectively) with body mass indexes (in kg/m²) of 23.5 ± 1.8 and 24.3 ± 6.0, respectively. We measured RMR and TEF with indirect calorimetry, total body water with deuterium dilution, and extracellular water with corrected bromide space. We calculated FFM (total body water/0.732) and BCM [(total body water - extracellular water)/0.732)].

Results: FFM was higher in control subjects than in paraplegics (77.2 ± 7.2% and 69.2 ± 8.7%, respectively; P = 0.0002), as were BCM (47.4 ± 6.7% and 35.9 ± 8.1%, respectively; P < 0.0001) and RMR (7016 ± 935 and 6159 ± 954 kJ/d, respectively; P = 0.0007). FFM was the single best predictor of RMR in both groups (r² = 0.83 for control subjects and 0.70 for paraplegics, P < 0.0001 for both). RMR adjusted for FFM did not differ significantly between control subjects and paraplegics (6670 ± 504 and 6588 ± 501 kJ/d, respectively). TEF also did not differ significantly between control subjects and paraplegics (6.25 ± 2.2% and 5.53 ± 1.8% of energy intake, respectively).

Conclusions: FFM, BCM, and RMR, but not obligatory TEF, are lower in paraplegics than in control subjects. RMR does not differ between control and paraplegic subjects after adjustment for FFM, indicating similar metabolic activity in the fat-free compartment of the body.

Key Words: Paraplegia • disability • spinal cord injury • body composition • fat-free mass • resting metabolic rate • thermic effect of feeding

INTRODUCTION  
Obesity is one of many secondary complications found in the paraplegic population. Similar to obesity in the able-bodied population, obesity in spinal cord injury (SCI) is associated with numerous metabolic sequelae, including glucose intolerance and insulin resistance (1, 2), hyperlipidemia (3), and coronary artery disease (4). Additional sequelae unique to the SCI population include pulmonary emboli (5), reduced function below the level predicted by the neurological lesion (6), pain (7), and compromised mobility (8).

Positive energy balance increases the risk of obesity. Total daily energy expenditure comprises resting metabolic rate (RMR), thermic effect of feeding (TEF), and physical activity. RMR in able-bodied individuals accounts for 65% of total daily energy expenditure and is largely determined by body size and composition. We and others have shown that fat-free mass (FFM) explains 70–85% of the variation in RMR (9–11). A low RMR, expressed in relation to FFM, was found to be a risk factor for weight gain (12). Therefore, the relation between these 2 variables was investigated to explain differing rates of weight gain in various clinical populations (13–17). A limited number of studies indicate that persons with chronic SCI have low absolute resting or basal metabolic rates (18–21). Only one study adjusted RMR for body composition and found that RMR adjusted for FFM, fat mass (FM), and age was 678 kJ/d lower in SCI patients than in able-bodied subjects (P < 0.01) (18). However, the generalizability of the results from the above studies is limited, because of either small sample sizes (18, 19), lack of able-bodied control subjects for comparison (19–21), or inclusion of men only (18, 19, 21). Also, to the best of our knowledge, no study has related body cell mass (BCM) to energetics in this population. FFM includes both extracellular mass and the metabolically active BCM (skeletal muscle and organs); the latter is responsible for all of the oxygen consumption, carbon dioxide production, and work performed by the body. It is not known whether RMR adjusted for body composition, including FFM and BCM, is lower in men and women with paraplegia than in those who are able-bodied.

TEF accounts for 3–10% of total daily energy expenditure and may play a role in the development and maintenance of obesity (22). Only 2 studies have investigated TEF in the SCI population. One found that TEF (expressed as a percentage of total daily energy intake) in male SCI subjects was lower than that of able-bodied control subjects (18), whereas the other study found no differences in TEF, expressed as a percentage of either test energy intake or RMR (23).

Our objective was to investigate factors that influence RMR and TEF in a group of healthy adult men and women with paraplegia. We hypothesized that paraplegia would result in lower FFM, BCM, RMR, and TEF.

SUBJECTS AND METHODS  
Subjects
Able-bodied men and women (n = 34) were recruited from the University of Toronto, Ryerson University, and the staff of The Hospital for Sick Children in Toronto. Paraplegic men and women (n = 32) were recruited from The Toronto Rehabilitation Institute, Ontario Wheelchair Sports Association, Ontario March of Dimes, Canadian Paraplegic Association, and Spina Bifida and Hydrocephalus Association of Toronto. The subjects were group-matched on the basis of body mass index (in kg/m²). Four subjects with paraplegia were excluded from the analyses because of technical difficulties with our indirect calorimeter, resulting in a total of 28 paraplegic subjects. The most common cause of paraplegia in these remaining 28 subjects was motor vehicle accident (n = 11), followed by hemorrhage (n = 4), spina bifida (n = 4), and falls (n = 3). The remaining causes were mixed and included transverse myelitis (n = 2), gunshot wound (n = 1), bacterial infection (n = 1), scuba diving accident (n = 1), and Von Hippel Lindau syndrome (n = 1). The mean number of years since the onset of paraplegia was 11.4 ± 9.5 (range: 1.5–39 y). Eighteen of the 28 paraplegic subjects (11 men and 7 women) had complete lesions (no sensory or motor function in the sacral segments) and 10 subjects (6 men and 4 women) had incomplete lesions (partial sensory function, motor function, or both below the lesion and sensory or motor function in the S4–5 sacral segments) (24). All subjects underwent a screening health history, and none reported a history of diabetes, Crohn’s disease, renal disease, heart disease, hypothyroidism, or hyperthyroidism. None of the subjects had any active decubitus ulcers. Women were in the follicular phase (days 1–12) of their menstrual cycles according to their self-reports.

Data collection began in January 2000 and was completed in August 2001. The study was approved by the Research Ethics Boards of The Hospital for Sick Children and The Toronto Rehabilitation Institute. Subjects were given a small honorarium for their participation.

Procedures
Studies were carried out during a 1-d visit to the Clinical Investigation Unit of The Hospital for Sick Children. Subjects were told that they should not exercise or consume alcohol or caffeine for the 24 h preceding the study day. Subjects arrived in the morning after a 12-h fast, provided informed consent, and completed a second health history. All measures were obtained by the same investigator (ACB) with subjects wearing light clothing and no shoes.

First, subjects were asked to empty their bladders so that a urine sample could be analyzed for nitrogen and metanephrine contents. For each subject, between 0830 and 1030, a urine sample was collected into a plastic container and treated with 4 mL of a 30% HCl solution to prevent microbial growth. Body weight was measured to the nearest 0.1 kg on a beam balance scale (Detecto Model; Cardinal Scales, Web City, MO) for the control subjects and on a digital wheelchair scale (Scale-Tronix 6006; Wheaton, IL) for the paraplegic subjects. The CV between the 2 instruments was determined in a subsample of 6 able-bodied control subjects, and was found to be 0.36 ± 0.15%. Height was measured to the nearest 0.1 cm with a wall-mounted stadiometer (Holtain Ltd, Crymych, United Kingdom) for the control subjects and on an adult-sized Plexiglas length board (made specifically for the study by the Medical Engineering Department of The Hospital for Sick Children) for the paraplegic subjects. Subjects were asked to transfer from their wheelchairs, first to a bed and then onto the length board. With the subject’s head resting against the immovable headboard, legs outstretched and feet in dorsiflexion, the movable foot board was pressed against the heels. Subjects looked up at the ceiling during the measurement, while the investigator ensured that the hips were straight and centered on the board. The CV between the stadiometer and the length board in the able-bodied subsample was 0.78 ± 0.23%.

After a baseline blood sample was obtained (15 mL, drawn into a heparin-containing syringe), each subject was given an oral dose of water labeled with ²H₂O for the measurement of total body water (TBW) and with sodium bromide for the measurement of extracellular water (ECW). The dosages were as follows: 0.25 g 99.9 atom percent (AP) ²H₂0 (CDN Isotope, Pointe-Claire, Quebec) per kg estimated TBW (60% of body weight) and 1.0 mL 30% NaBr (Fisher Scientific, Nepean, Ontario) per kg body weight. The container was then rinsed with 15 mL deionized water, which the subject subsequently drank to wash any remaining isotope from the mouth into the stomach. A plateau blood sample (15 mL) was obtained 3 h after administration of the ²H₂O and NaBr (25, 26). Subjects continued to fast during the equilibration period. Blood samples were centrifuged (Beckman J6B Centrifuge; Beckman Coulter Inc, Fullerton, CA) at 1200 x g for 10 min at -4°C, and the plasma samples were subsequently stored at -20°C until analyzed.

Body composition
Plasma samples were analyzed for their ²H₂O content by using an isotope ratio mass spectrometer (CF-IRMS, model ANCA GSL; Europa Scientific Inc, Crewe, United Kingdom) after equilibration with hydrogen gas (27). The following equation was used to calculate TBW:

RESULTS  
Age and body-composition characteristics of the 2 groups are shown in Table 1. There was no significant difference in the sex distribution between the 2 groups. Control subjects were slightly younger than were paraplegic subjects. Weight and body mass index did not differ significantly between groups, but control subjects were taller. Expressed as a percentage of body weight, TBW, FFM, intracellular water, and BCM were higher in the control group, and FM and ECW were lower in the control group. Differences in all of the above parameters were maintained when we compared male control and paraplegic subjects and female control and paraplegic subjects, with one exception. Male control subjects were slightly younger than were male paraplegics (29.1 ± 8.5 and 36.3 ± 10.1 y, respectively; P = 0.0119), whereas age did not differ significantly between female control and paraplegic subjects (29.2 ± 5.4 and 30.3 ± 6.6, respectively; P = 0.7458). There was no significant correlation between years since onset of paraplegia and FFM (r² = 0.047, P = 0.2681).

View this table:
TABLE 1 . Age and body composition of able-bodied control subjects and paraplegic subjects  
Thermogenic hormones and energy metabolism
There were no significant differences between the control and paraplegic groups in any of the hormones measured. The values for the control and paraplegic groups, respectively, were as follows: thyroid stimulating hormone, 1.75 ± 0.74 and 1.57 ± 0.66 mIU/L (P = 0.3442); T₃, 1.57 ± 0.32 and 1.57 ± 0.33 nmol/L (P = 0.9746); free T₄, 15.5 ± 2.4 and 16.1 ± 1.4 pmol/L (P = 0.2535); and metanephrine, 1.16 ± 0.63 and 1.07 ± 0.53 µmol/L (P = 0.6346). The parameters of energy metabolism are shown in Table 2. The Schofield equation (30) closely predicted RMR in the control group ( -99 kJ/d, P = 0.2633) but significantly overestimated RMR in the paraplegic group ( 339 kJ/d, P = 0.0025). As expected, measured RMR was significantly higher (by 14%) in the control group than in the paraplegic group. This difference remained significant when RMR was adjusted separately for age, weight, FM, T_3, and metanephrine but was reduced to <2% when adjusted for FFM (P = 0.5467), both FM and FFM (P = 0.3692), and BCM (P = 0.5780).

View this table:
TABLE 2 . Energetics in able-bodied control subjects and paraplegic subjects¹  
Similar results were obtained when the groups were divided by sex: RMR was significantly higher in male control subjects than in male paraplegics (7415 ± 737 and 6649 ± 749 kJ/d, respectively; P = 0.0023) and in female control subjects than in female paraplegics (6056 ± 609 and 5401 ± 721 kJ/d, respectively; P = 0.0373). The differences were no longer significant when RMR was adjusted for FFM [7197 ± 503 and 6957 ± 514 kJ/d for men (P = 0.1643) and 5440 ± 461 and 5873 ± 447 kJ/d for women (P = 0.0820)]. Protein oxidation did not differ significantly between the 2 groups. There were trends toward lower fat oxidation and higher carbohydrate oxidation and fasting RQ in the control group. Postprandial RQ was significantly higher in the control group (P < 0.0001). TEF (expressed either as a percentage of RMR or a percentage of test energy intake) was not significantly different between the 2 groups.

Partial correlation coefficients between RMR and selected predictor variables for both groups are shown in Table 3. The best single predictor of RMR was FFM, which accounted for 83% of the variation in RMR in control subjects and 70% of the variation in paraplegics (P < 0.0001 for both).

View this table:
TABLE 3 . Pearson’s product-moment partial correlation coefficients between resting metabolic rate and selected predictor variables in able-bodied control subjects and paraplegic subjects  
The relation between unadjusted RMR and FFM for both groups is shown in Figure 1. FM was not predictive of RMR in the control group (P = 0.4267) but was predictive of RMR in the paraplegic group (P = 0.0223). The most statistically significant prediction equation for RMR in the paraplegic group, as determined by forward stepwise regression, was as follows:

DISCUSSION  
The 2 major findings of this study were that the obligatory phase of TEF is not lower in persons with paraplegia and that absolute RMR is lower in persons with chronic paraplegia than in able-bodied persons, but is not different when adjusted for FFM. This suggests that the metabolic activity of the fat-free body is similar in paraplegic subjects and able-bodied control subjects.

As expected, persons with chronic paraplegia had significantly lower FFM and BCM and higher FM than did able-bodied control subjects. Despite the loss of metabolically active tissue, a significant amount of variation in RMR in the paraplegic group was explained by FFM (r² = 0.70, P < 0.0001) and BCM (r² = 0.46, P = 0.0001). Furthermore, the difference in absolute RMR was reduced from 14% to <2% when RMR was adjusted for FFM and BCM (P = 0.5467 and P = 0.5780, respectively). These findings differ from those of Monroe et al (18), who found that RMR adjusted for FFM, FM, and age was 678 kJ lower per day in persons with SCI than in able-bodied subjects (P < 0.01). This may reflect methodologic differences between the 2 studies, because in the study of Monroe et al (18), RMR was determined indirectly by extrapolation of a linear regression between spontaneous physical activity and energy expenditure. As a result, RMR may have been overestimated in the study of Monroe et al (18); this is supported by the finding that RMR in control subjects was 8–16% higher than was predicted by the Schofield equations (30).

When adjusted for weight, which is at best a crude indicator of body composition, RMR remained significantly lower in the paraplegic group. This may be the reason why the Schofield equations (30) overestimated RMR in this group. These equations were validated in healthy, able-bodied men and women and include weight as a predictor of RMR. When used in populations with altered body composition, such as the paraplegic group in the present study, the predictive ability of the equations decreases. Together with the above findings regarding the relation between FFM and RMR, this was the rationale for including FFM, and not weight, in our RMR prediction equation. Adjusting RMR for thermogenic hormones did not decrease the difference in RMR between the control and paraplegic subjects, most likely because there were no significant differences in T₃ or metanephrine concentrations. The latter finding was unexpected, but may reflect the fact that we studied persons with paraplegia. We might have seen altered sympathetic activity in persons with tetraplegia, as a result of a higher level of interruption of the sympathetic pathways (37).

TEF was not significantly lower in the paraplegic group. This agrees with the findings of Aksnes et al (23), who measured TEF for 2 h after ingestion of a mixed liquid meal (similar in composition to the one used in the present study) in 9 tetraplegic and 6 able-bodied men. However, our results do not agree with those of Monroe et al (18), who found that TEF was lower (P < 0.05) in 10 men with SCI than in 59 able-bodied men. This may reflect methodologic differences between our 2 studies. Monroe et al (18) measured TEF for 14 h in a respiratory chamber and calculated TEF as a percentage of test energy intake as follows:

ACKNOWLEDGMENTS  
We gratefully acknowledge the participation of the study subjects.

AC Buchholz contributed to the design of the study and was responsible for collecting and analyzing the data and for writing the manuscript; this work forms part of her doctoral thesis. CFM provided significant clinical consultation and helped recruit the paraplegic subjects, and PB Pencharz was the primary investigator responsible for the study design and the scientific and clinical rationale. None of the authors had any financial or personal interest (including advisory board affiliations) in any company or organization sponsoring the research.

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