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00005768-200704000-0001500005768_2007_39_688_midorikawa_attributed_4article< 91_0_17_5 >Medicine & Science in Sports & Exercise©2007The American College of Sports MedicineVolume 39(4)April 2007pp 688-693High REE in Sumo Wrestlers Attributed to Large Organ-Tissue Mass[BASIC SCIENCES: Original Investigations]MIDORIKAWA, TAISHI1; KONDO, MASAKATSU2; BEEKLEY, MATTHEW D.3; KOIZUMI, KIYOSHI4; ABE, TAKASHI11Department of Exercise and Sport Science, Tokyo Metropolitan University, Tokyo, JAPAN; 2Department of Exercise Physiology, Nihon University, Tokyo, JAPAN; 3Department of Physical Education, United States Military Academy, West Point, NY; and 4Tokyo Medical University Hachioji Medical Center, Tokyo, JAPANAddress for correspondence: Taishi Midorikawa, Ph.D., Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan; E-mail: taishi@aoni.waseda.jp.Submitted for publication January 2006.Accepted for publication November 2006.ABSTRACTPurpose: It is unknown whether high resting energy expenditure (REE) in athletes is attributable to changes in organ-tissue mass and/or metabolic rate. The purpose of this study was to examine the contribution of organ-tissue mass of fat-free mass (FFM) components to REE for Sumo wrestlers who have large FFM and REE. We investigated the relationship between the REE measured by indirect calorimetry and the REE calculated from organ-tissue mass using a previously published approach.Methods: Ten Sumo wrestlers and 11 male untrained college students (controls) were recruited to participate in this study. FFM was estimated by two-component densitometry. Contiguous magnetic resonance imaging (MRI) images with a 1-cm slice thickness were obtained from the top of head to the ankle joints, and the cross-sectional area and volume were determined for skeletal muscle (SM), liver, kidney, and brain. The volume of adipose tissue, heart, and residual was calculated from each equation. The volume units were converted into mass by an assumed constant density. The measured REE was determined by indirect calorimetry. The calculated REE was estimated as the sum of individual organ-tissue masses (seven body compartments) multiplied by their metabolic rate constants.Results: The measured REE for Sumo wrestlers (2286 kcal·d−1) was higher (P < 0.01) than for controls (1545 kcal·d−1). Sumo wrestlers had a greater amount of FFM and FFM components (e.g., SM, liver, and kidney), except for brain. The ratio of measured REE to FFM and the measured REE adjusted by FFM were similar between the two groups. The measured REE values for Sumo wrestlers were not significantly different from the calculated REE values.Conclusions: The high REE for Sumo wrestlers can be attributed not to an elevation of the organ-tissue metabolic rate, but to a larger absolute amount of low and high metabolically active tissue including SM, liver, and kidney.It is well known that fat-free mass (FFM) is major determinant of resting energy expenditure (REE) (24,28). In general, strength- and power-event athletes have a much larger FFM than nonathletes (31). In particular, Sumo wrestlers have the largest FFM in athletes, although the body composition of Sumo wrestlers is characterized by a relatively high fat content (19,22). Therefore, it would be expected that athletes such as Sumo wrestlers would have a high REE. However, recent studies have reported that FFM is not a single homogenous metabolic compartment (13,17), and it is unknown which metabolically active organ tissues of FFM components are attributed to large REE in Sumo wrestlers.REE is commonly adjusted per unit of FFM to compare individuals of different body size. According to the regression line between FFM and the ratio of REE to FFM (REE/FFM) for nonathletes, as reported by Heymsfield and colleagues (15), the REE/FFM ratio for subjects with a 70-kg FFM was approximately 26 kcal·kg−1·d−1, which was a lower value than for subjects with a 50-kg FFM (about 29 kcal·kg−1·d−1). In other words, the REE/FFM ratio in normal untrained populations is apparently smaller for individuals with greater FFM. In contrast, it has also been reported that the ratio of sleeping metabolic rate to FFM for body builders with about 70 kg of FFM was 29 kcal·kg−1·d−1, and no differences in the REE/FFM ratio were found between body builders and nonathletes (60 kg of FFM) (3). Moreover, the REE/FFM ratio measured for various kinds of athletes (e.g., water polo, judo, and karate) also averaged 28-29 kcal·kg−1·d−1 for approximately 70 kg of FFM (8), which was higher compared with nonathletes with the same amount of FFM (i.e., about 26 kcal·kg−1·d−1). In summary, the REE/FFM ratio seems to decrease with increasing FFM in untrained controls. In contrast, athletes with larger FFM have a higher REE/FFM ratio compared with untrained controls who have similar FFM.To explain why the REE/FFM ratio for untrained populations is smaller for those with greater FFM, it was recently reported that a reduction in the proportion of internal organ-tissue mass to FFM was coupled with an increase in that of skeletal muscle (SM) mass in untrained individuals (13,15). The proportion of low-metabolic active tissue (e.g., SM) and high-metabolic active tissue (e.g., liver and kidney) relative to FFM could account for the REE/FFM ratio for normal untrained populations. At the present time, because there are no published data for athletes' body composition at the organ-tissue level, it is unknown why the REE/FFM ratio for athletes with greater FFM does not decrease as well. On the basis of the apparent decline in REE/FFM ratio for untrained populations, we hypothesized that both SM and internal organ mass in athletes are increased with FFM accumulation, and that the ratio of internal organ mass to FFM does not decline, unlike untrained individuals. Thus, the purpose of this study was to examine the contribution of organ-tissue mass of FFM components to REE for Sumo wrestlers (who have a large FFM). To test our hypotheses, we examined the relationship between the measured REE by indirect calorimetry and the calculated REE from organ-tissue mass and the assumed metabolic rate constants for nonathletes based on a previously published approach (13). If the calculated REE for Sumo wrestlers can be accurately estimated compared with the measured REE, then we can conclude that the REE for Sumo wrestlers is attributed to the amount of organ-tissue mass and that the metabolic rate for individual organ-tissue is not different from that for nonathletes.METHODSSubjects.Ten male college Sumo wrestlers and 11 male untrained college students (controls) were recruited for the study. College Sumo wrestlers had participated in regular training (termed "Kei-ko") for an average of 9 yr. Kei-ko normally consists of wrestling exercises (e.g., pushing and throwing other Sumo wrestlers) and additional technical drills that consist of a mix of power, agility, and endurance training (22). None of the subjects had a history of cardiovascular, endocrine, or orthopedic disorders, nor had they ever tested positive for anabolic steroids or taken any medication during the given measurement time. All subjects received a verbal and written description of the study and gave their informed consent to participate before testing. The study was approved by the Tokyo Metropolitan University ethics committee for human experiments.Body composition measurements.Standing height was measured barefoot using a wall-mounted stadiometer. Body mass was measured with minimal clothing (only swimwear), and body mass index (BMI) was calculated. Body density was measured by hydrostatic weighing, with simultaneous measurement of residual lung volume by oxygen dilution (1). Body fat percentage was calculated from body density using Brozek's equation (5). FFM was estimated as total body mass minus fat mass. The estimated coefficient of variation (CV) of this FFM measurement from test-retest procedures was 0.7% (21).Organ-tissue mass measurements by MRI.The volumes of whole-body SM, internal organs (liver and kidney), and brain were measured using a General Electric Signa 1.5-T scanner (Milwaukee, WI). A T1-weighted spin-echo, axial-plane sequence was performed with a 150-ms repetition time and a 4.2-ms echo time. Subjects rested quietly in the magnet bore in the supine position with hands placed on the abdomen. Contiguous transverse images with a 1.0-cm slice thickness (0-cm interslice gap) were obtained from the top of head to the ankle joints for each subject (approximately 160 slices per person). Four sets of acquisitions extended from the top of head to the femoral head during breath holding (23 s). The other three sets of acquisitions were obtained from the femoral head to the ankle joints during normal breathing (2).The volumes of SM, liver, kidney, and brain were calculated from the sum of the cross-sectional areas (cm2), which were determined by tracing the images and multiplying by the slice thickness (1 cm). Volume (cm3) was converted to mass (kg) by use of the following densities: 1.041 g·cm−3 for SM, 271.060 g·cm−3 for liver, 1.050 g·cm−3 for kidney, and 1.036 g·cm−3 for brain (11). The percentage of measurement differences for the same scan on two separate days by the same observer in our laboratory was 1.0% for SM (27), 1.4% for liver, 2.7% for kidney, and 2.5% for brain (N = 3).Because the constantly pulsing heart produced artifacts, heart mass was estimated from body mass using the following formula: 0.006 × body mass0.98 (7). Adipose tissue mass was calculated from fat mass with the assumption that 85% of the adipose tissue was fat and that 15% of the adipose tissue consisted of the remaining calculated fat-free component (fat/adipose tissue = 0.85) (15). Total body mass was defined as the sum of the organ masses. Residual mass was calculated as total body mass minus the sum of the SM, adipose tissue, brain, liver, kidney, and heart masses. Therefore, residual mass was mainly composed of bone, blood, skin, intestine, connective tissue, and lung tissue (27).Measured REE.REE was measured by open-circuit indirect calorimetry using the Douglas bag technique (10). The subjects did not eat or consume any liquids, except water, for 12 h before testing. None of the subjects performed any exercise 36 h before testing. Subjects got to the laboratory from their home by car and were asked to minimize exertion before REE determination. All REE measurements were performed between 0730 h and 1000 h. After entering the laboratory, subjects rested in the supine position for 30 min, and a face mask (Vise Medical, Japan) was attached. Expired air was collected for 10 min, two times, and the mean value was used for analysis. During the test, the room was maintained at a stable temperature (20-25°C), and noise was kept to a minimum. The subjects were instructed to remain awake, quiet, and motionless before and throughout the measuring periods. An oxygen and carbon dioxide analyzer (MG-360, Minato, Japan) was used to analyze the rates of oxygen consumption and carbon dioxide production. The volume of expired air was determined using a dry gas volume meter (DC-5, Shinagawa, Japan) and was converted to standard temperature, standard pressure and dry gas. Gas exchange results were converted to REE (kcal·d−1) using Weir's equation (30). The average CV based on the test-retest measurements was 3.6% for REE, 3.8% for V˙O2, 3.7% for V˙CO2, and 5.2% for respiratory quotient (RQ) (N = 5).Calculated REE.Calculation of REE was based on the sum of seven body compartments (SM, adipose tissue, brain, liver, kidney, heart, and residual mass) times the corresponding tissue-respiration rate, on the basis of specific tissue-metabolic rates (12). The calculated REE was computed using the following equation (13):Equation (Uncited)Statistical analysis.Results are expressed as means ± standard deviation for all variables. The differences between college Sumo wrestlers and control subjects were tested for significance by unpaired t-test. The difference between the measured REE and the calculated REE was examined using a paired t-test. Pearson's product-moment analysis was used to determine all correlations. In addition, the measured REE was presented via absolute value, the ratio of REE to FFM, and adjusted value for FFM based on logistic regression analysis. All statistical analyses were done using SPSS 10.0 software. Statistical significance was set at the P < 0.05 level.RESULTSBody composition and measured REE.Mean body mass was higher in Sumo wrestlers compared with controls. Sumo wrestlers had a higher (P < 0.01) body fat percentage and mass than controls. FFM was 47% greater (P < 0.01) in Sumo wrestlers than controls (78.6 vs 53.3 kg) (Table 1). The measured REE, V˙O2, and V˙CO2 were also 47% higher (P < 0.01) in Sumo wrestlers compared with controls (2286 vs 1545 kcal·d−1) (Table 2). The ratio of measured REE to FFM and the measured REE adjusted by FFM were similar between the two groups (Table 2).TABLE 1. Subject characteristics.TABLE 2. Measured and calculated resting energy expenditure.Organ-tissue mass and calculated REE.Sumo wrestlers had greater (P < 0.01) SM, liver, and kidney masses, but not brain, compared with controls (Table 3). The ratios of SM mass to FFM (46.9 vs 45.9%) and kidney mass to FFM (0.6 vs 0.6%) were similar between Sumo wrestlers and controls. However, the ratio of liver mass to FFM was higher (P < 0.05) in Sumo wrestlers than controls (3.1 vs 2.6%) (Table 3). The calculated REE was 47% higher (P < 0.01) in Sumo wrestlers compared with controls (2322 vs 1573 kcal·d−1). There was no difference between measured REE and calculated REE in Sumo wrestlers or controls (Table 2). A significant relationship between measured REE and calculated REE was also observed in the two groups (Sumo wrestlers: r = 0.93, P < 0.01; controls: r = 0.72, P < 0.05) (Figure 1). A Bland-Altman plot showed no significant trend for controls (r = −0.23, P = 0.50), whereas the plot for Sumo wrestlers approached significance (r = 0.61, P = 0.06).TABLE 3. Organ-tissue-level body composition.FIGURE 1- Relationship between measured resting energy expenditure (REE) and calculated REE.DISCUSSIONIt was previously found that the REE/FFM ratio for those untrained with large FFM was lower than for those with small FFM for in untrained populations (15). In contrast, the REE/FFM ratio for athletes was not lower despite having a large FFM (3,8). The reasons for this discrepancy had not been clarified. Our data demonstrate that although Sumo wrestlers had a greater FFM by 25 kg compared with controls, the measured REE/FFM ratio was similar between the two groups (29.1 kcal·kg−1·d−1 for Sumo wrestlers vs 29.2 kcal·kg−1·d−1 for controls; Table 2), in contrast to what is seen with untrained populations (15). As predicted from the regression line between FFM and the REE/FFM ratio for the normal population reported by Heymsfield and colleagues (15), the REE/FFM ratio for nonathletes with an 80-kg FFM (which was approximately the same as the FFM of the Sumo wresters in the present study) was only about 25 kcal·kg−1·d−1. This value was lower by 4 kcal·kg−1·d−1 than the value for Sumo wrestlers in the present study. Moreover, the present study found that the estimated REE/FFM ratio (29.5 kcal·d−1 = (2322 kcal·d−1)/(78.6 kg)) for Sumo wrestlers, using an approach previously validated in nonathletes (13,17), was very similar to the measured REE/FFM ratio (29.1 kcal·d−1 = (2286 kcal·d−1)/(78.6 kg)) (Table 2). This supports our hypothesis that the REE/FFM ratio for heavy-weight athletes can be attributed to an increase in both SM and internal organ mass during FFM accumulation.Previous studies also have found that a reduction in the proportion of internal organ-tissue mass to FFM was coupled with an increase in that of SM mass in untrained individuals, which was assumed to contribute to the fact that the REE/FFM ratio for normal populations deceases with increasing FFM (13,15). In a recent study comparing the body composition of the untrained obese subjects with intermediate-weight subjects, there were no differences of liver and kidney masses between groups (obese subjects: 1.64 and 0.32 kg, intermediate-weight subjects: 1.64 and 0.36 kg, respectively) even though obese subjects have a greater FFM (i.e., liver mass and kidney mass/FFM ratios, obese subject: 2.5 and 0.5%, intermediate weight subjects: 3.0 and 0.7%, respectively) (4). However, the Sumo wrestlers in the present study had greater absolute liver and kidney masses (2.40 and 0.49 kg), respectively, in comparison with untrained controls (1.40 and 0.33 kg). Additionally, the present study found that the ratio of internal organ mass to FFM for Sumo wrestlers does not decline with greater FFM, unlike untrained individuals, and the value of liver mass to FFM for Sumo wrestlers was higher than for controls (i.e., liver mass and kidney mass/FFM ratios, Sumo wrestlers: 3.1 and 0.6%, controls: 2.6 and 0.6%, respectively). However, the cause of the phenomenon for Sumo wrestlers has not yet been clarified. One possible explanation for the increase in liver and kidney mass may be attributed to an increase in protein intake by Sumo wrestlers. Increased dietary protein intake has been shown to induce increases in liver and kidney mass in animals (25). Additionally, it is reasonable to speculate that the liver and kidney masses increased to attenuate the extra burden that these tissues might experience the metabolic stress of high-intensity exercise training, which is similar to results found in male rats (14).On the other hand, the metabolic rate of liver and kidney mass is proposed to decline with increasing absolute organ-tissue mass (29). However, the present study indicates that the metabolic coefficients per unit of organ-tissue mass remain almost constant between Sumo wrestlers with large organ-tissue mass and controls. This result is consistent with that of a previous study on subjects with a wider range of FFM (4). Moreover, a previous study on rats found that the tissue oxygen consumption of liver slices in 60-g rats did not differ from that of 350-g rats (16). Similarly, the glomerular filtration rate (GFR), which is a direct function of oxygen consumption, increased with changes in kidney mass, whereas the GFR per unit of kidney mass was stable from rats of about 100 to 400 g (16). Thus, although Sumo wrestlers had greater body fat than controls, it is expected that the volume of liver and renal tissue for Sumo wrestlers is related not to the lipid content of each organ tissue but to the number of hepatocytes and nephrons, respectively.According to longitudinal training experiments, the exercise training-induced change in FFM elicits the change in REE (6,9,23). However, it is not clear whether the REE/FFM ratio, which is an indicator of the variation in the organ-tissue metabolic rate, is simultaneously increased after exercise training. The disparate results can be attributed to long-term, excess postexercise O2 consumption (28). Moreover, it has been reported that acute and sustained energy restriction induce low concentrations of thyroid hormones and decrease protein synthesis, which are related to REE variability (28). Byrne and Wilmore (6) performed training experiments designed to exclude these confounding effects. According to this excellent study, on a 20-wk whole-body resistance training program, the subjects gained 1.9 kg of FFM and 44 kcal·d−1 of REE but did not increase their REE/FFM ratio. On the basis of the results of that study and those of the present cross-sectional study, the increase in REE after exercise training can be attributed to the change in mass of organ tissue, not to a change in the metabolic rate of organ tissue. Additionally, Byrne and Wilmore (6) observed that the exercise training-induced change in REE per kilogram of FFM was about 25 kcal·kg−1 FFM·d−1 (REE 44 kcal·d−1/FFM 1.9 kg), and the REE/FFM ratio for Sumo wrestlers in the present study was about 30 kcal·kg−1·d−1 (Table 2). Therefore, it is likely that REE increases by about 30 kcal·d−1 for each 1-kg increase in FFM after exercise training. Future studies should take into consideration the relationship between changes in REE and organ-tissue-level body composition after exercise training.There are four possible limitations of this study. First, we assumed that the constants for organ-tissue energy expenditure were completely static. However, it is known that some of these constants may change-for instance, in the case of obesity (26). Because Sumo wrestlers can be considered obese by some measures, we cannot exclude the possibility that the organ-tissue energy expenditure constants were different in our subjects. On the other hand, Sumo wrestlers are athletes who participate in vigorous activity on a daily basis. In any event, further research is needed to clarify whether changes in organ-tissue energy expenditure constants are altered in Sumo wrestlers. Second, in the present study, a Bland-Altman plot showed no significant trend for controls (r = −0.23, P = 0.50), whereas the plot among Sumo wrestlers approached significance (r = 0.61, P = 0.06). Although the reason for the marginal systematic error was unclear, one possible explanation may be related to the error of the estimated heart mass from body mass. Because the heart has the highest assumed metabolic rate (i.e., 440 kcal·kg−1·d−1), the contribution to the whole-body REE is relatively large. Therefore, although a previous study has reported that body size is an optimal index for left ventricular size (20), we need to assess heart mass more precisely, using ECG-triggered MRI, in our future study. Thirdly, in the present study, we have observed that the ratio of liver mass to FFM was higher in Sumo wrestlers than in controls. The possibility that a greater proportion of liver mass for Sumo wrestlers may be partly attributable to increased intrahepatic lipids cannot be ruled out. However, a previous study on Japanese subjects has reported that the difference in liver fat content was only about 5% between nonobese healthy subjects (BMI < 25) and mildly obese subjects (BMI ≍ 30) (18). Therefore, the lipid content of the liver should have little impact on absolute mass and constant density. A last limitation concerns FFM density for Sumo wrestlers. Assuming that bone mineral density for the Sumo wrestlers is higher that normal secondary to the regular training, this will introduce an error in the body density measure from hydrostatic weighting such that percent fat will be underestimated and FFM will be overestimated. It is possible that this assumption can affect the results significantly. Future studies should take into consideration how the density of the FFM might be affected by various organ-tissue masses.CONCLUSIONIn this study, there was a very strong agreement between measured REE and calculated REE in Sumo wrestlers. Thus, high REE for Sumo wrestlers can be attributed not to an elevation of the organ-tissue metabolic rate but, instead, to a larger absolute amount of low and high metabolically active tissue, including SM, liver, and kidney.Heartfelt thanks are due to the subjects who participated in this study. We would like to thank Sumie Komuro for her assistance in MRI analysis. This study was supported in part by The Ministry of Education, Science, Sports and Culture of Japan (grant No 15300221).REFERENCES1. Abe, T., M. Kondo, Y. Kawakami, and T. Fukunaga. Prediction equations for body composition of Japanese adults by B-mode ultrasound. Am. J. Hum. Biol. 6:161-170, 1994. 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