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Am. J. Physiol. Endocrinol. Metab.

278: E308–E315, 2000.

Metabolically active components of fat free mass


and resting energy expenditure in nonobese adults
KIRSTEN ILLNER,1,2 GISBERT BRINKMANN,2 MARTIN HELLER,2
ANJA BOSY-WESTPHAL,1 AND MANFRED J. MÜLLER1
1Institut für Humanernährung und Lebensmittelkunde und 2Klinik für Radiologische Diagnostik,

Christian-Albrechts-Universität zu Kiel, D-24105 Kiel, Germany

Illner, Kirsten, Gisbert Brinkmann, Martin Heller, organ mass substantially differ with respect to their
Anja Bosy-Westphal, and Manfred J. Müller. Metaboli- individual rates of energy expenditure. Estimates of
cally active components of fat free mass and resting energy REE per kilogram organ mass based mainly on in vitro
expenditure in nonobese adults. Am. J. Physiol. Endocrinol. measurements vary between 837 and 1,841 kJ for
Metab. 278: E308–E315, 2000.—Resting energy expenditure
(REE) and components of fat-free mass (FFM) were assessed
internal organs and 54 and 63 kJ for skeletal muscle
in 26 healthy nonobese adults (13 males, 13 females). De- (10, 24). Thus, from a metabolic point of view, different
tailed body composition analyses were performed by the ratios of high vs. low energy-requiring organs may explain
combined use of dual-energy X-ray absorptiometry (DEXA), an unknown part of the variation in REE (25, 29).
magnetic resonance imaging (MRI), bioelectrical impedance Techniques of computed tomography (CT), magnetic
analysis (BIA), and anthropometrics. We found close correla- resonance imaging (MRI), and dual-energy X-ray ab-
tions between REE and FFMBIA (r 5 0.92), muscle massDEXA sorptiometry (DEXA) can be used for the in vivo
(r 5 0.89), and sum of internal organsMRI (r 5 0.90). In a measurement of metabolically active components of
multiple stepwise regression analysis, FFMBIA alone ex-
FFM. Up to now, only four studies have combined these
plained 85% of the variance in REE (standard error of the
estimate 423 kJ/day). Including the sum of internal organsMRI measurements with measurements of REE (6, 12, 21,
into the model increased the r2 to 0.89 with a standard error 27). Using CT in combination with densitometry, De-
of 381 kJ/day. With respect to individual organs, only skeletal riaz et al. (6) measured REE and body composition (i.e.,
muscleDEXA and liver massMRI significantly contributed to skeletal muscle mass and the sum of tissue masses) in
REE. Prediction of REE based on 1) individual organ masses 22 men before and after a 100-day overfeeding period.
and 2) a constant metabolic rate per kilogram organ mass was They found significant correlations between REE and
very close to the measured REE, with a mean prediction error muscle, as well as nonmuscle, compartments of FFM.
of 96 kJ/day. The very close agreement between measured
Using these two variables of body composition did not
and predicted REE argues against significant variations in
specific REEs of individual organs. In conclusion, the mass of improve the prediction of REE over that provided by
internal organs contributes significantly to the variance in muscle mass alone. After overfeeding, body mass, lean
REE. body mass, and skeletal muscle mass were the best
correlates of REE. While the present study was under
body composition; muscle mass; organ mass; dual-energy
X-ray absorptiometry; magnetic resonance imaging; bioelec-
investigation, Sparti et al. (27) simultaneously used
trical impedance analysis; anthropometrics CT, DEXA, and echocardiography for the assessment of
the composition of FFM in 20 females and 20 males,
respectively. These authors also concluded that the
composition of FFM could not improve the prediction of
VARIATION IN THE SIZE of fat-free mass (FFM) has been REE compared with FFM alone. In a further prelimi-
shown to explain 65–90% of the between-subject varia- nary report, McNeill et al. (21) also provided no evi-
tion in resting energy expenditure (REE) (1, 3, 9, 13, 25, dence that liver, kidney, and spleen masses (as deter-
28). REE per unit FFM is not constant, and the ratio of mined by MRI in 30 women) explain any of the variance
REE to FFM varies with body weight. REE per unit in REE between individuals. Taken together, the re-
FFM decreases with increasing body mass, which sug- sults of three studies (6, 21, 27) suggest that the
gests that subjects with higher FFM have lower REEs variance in REE is more dominated by the energy
per kilogram FFM, whereas the opposite is true for expenditure of the individual organs than by the vari-
individuals with lower FFM (25). This finding consigns ance in the internal organ size. This idea is contrary to
the utility of indexing REE to body weight or FFM in a very recent paper by Gallagher et al. (12). These
subjects with different body masses. A potential expla- authors measured body cell mass (as measured by total
nation for this problem is the composition of the body potassium) and organ-tissue volumes by MRI and
metabolically active FFM. Skeletal muscle and internal echocardiography. They found strong associations be-
tween REE and individual or combined organ weights.
Moreover, calculating REE from individual organ
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
masses and previously reported organ metabolic rates
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734 closely predicted measured REE [i.e., the difference
solely to indicate this fact. between measured and calculated REE was less than
E308 0193-1849/00 $5.00 Copyright r 2000 the American Physiological Society http://www.ajpendo.org

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Copyright © 2000 American Physiological Society. All rights reserved.
ORGAN-TISSUE MASS AND ENERGY EXPENDITURE E309

84 kJ/day (12)]. These data suggest a constant organ- Garby et al. (Ref. 13)
tissue respiration rate.
REE 5 27.88 3 FFMDens 1 6.4 3 FM (2)
After reviewing the available literature, we reached
two conclusions. First, the data base on concomitant in Elia (Ref. 10) REE 5 21.11 3 FFMANTHRO 1 405 (3)
vivo measurements of organ size and REE is very
Ravussin and Bogardus (Ref. 25)
small. Second, the available data on the association
between body composition and REE are in part contra- REE 5 20.8 3 FFMDens 1 471 (4)
dictory. Faced with these discrepancies and the limited
information from concomitant in vivo measurements of The indexes clarify which method was used by the investi-
gators to measure or calculate FFM (Calc, calulated from
organ size and REE, we reassessed the relationship of weight and age; Dens, densitometry; ANTHRO, anthropom-
metabolically active components of FFM to REE in a etry, from skinfold measurements). Formulas 1–4 were used
homogeneous group of healthy adults by use of DEXA, because they assume body composition (i.e., FFM 6 fat mass)
MRI, bioelectrical impedance analysis (BIA), and an- as a predictor of REE. The data were therefore compared with
thropometrics for detailed body composition analysis. our approach (i.e., calculating REE from FFM and/or indi-
Our data support the idea that organ sizes are impor- vidual organ masses) to assess the differences between esti-
tant determinants of REE. The use of metabolically mated and measured values.
active components of FFM instead of total FFM re- Body composition analysis. By use of an electronic scale,
duced the variance in REE prediction. weight was measured without shoes, with light clothing, and
after voiding, at an accuracy of 0.1 kg (SECA, Modell 709,
Vogel & Halke, Hamburg, Germany). Height was assessed to
the nearest 0.5 cm with a stadiometer. Body composition was
METHODS assessed by the use of anthropometrics (ANTHRO), BIA,
DEXA, and MRI. ANTHRO and BIA were performed immedi-
Study population. Twenty-six healthy subjects (13 females,
ately after gas exchange measurements. DEXA and MRI were
13 males) participated in the study (see Table 1). The study
both performed on the following day. ANTHRO was used to
protocol was approved by the ethical committee of the Chris-
assess body fat (measurements of 4 skinfolds) and arm
tian-Albrechts-Universität zu Kiel. Before participation, each
muscle area (arm circumference). Skinfold thickness was
subject provided written consent. All subjects were healthy
measured by the use of caliper (Lafayette Instruments,
and weight stable. None had a history of recent illness,
Lafayette, IN). Fat mass was calculated according to Durnin
obesity, diabetes, hyperlipidemia, hypertension, or endocri-
and Wormersley (8), and arm muscle area was calculated
nopathy. Each subject had a normal physical examination.
according to Heymsfield et al. (17). BIA was performed as
Dieting or physical exhaustion were avoided during the 7
described previously (22) as a measure of total body water
days before examination.
(TBW). We used a body impedance analyzer at a frequency of
Measurements and estimations of REE. In females, mea-
50 kHz and the manufacturer’s software for data analyses
surements of REE and body composition were performed in
(BIA 2000-S, Data Input, Frankfurt, Germany). FFMBIA was
the follicular phase of the menstrual cycle (i.e., ,10 days
calculated assuming a water content of FFM of 73.2% (FFM 5
since last menstruation). REE was measured as described
TBW/0.732). Bone mineral content and whole body and
elsewhere (23). Briefly, REE was measured by an open-circuit
regional lean body mass (LBM) were measured by DEXA
indirect calorimeter (Deltatrac Metabolic Monitor, Datex
(Hologic QDR 4500A, Hologic, Waltham, MA). Limb lean
Instruments, Helsinki, Finland). Measurements were per-
mass was used as a measure of muscle mass, as suggested by
formed between 7:00 and 8:00 AM in a metabolic ward at
Heymsfield et al. (18). DEXA scans were analyzed with the
constant humidity (55%) and room temperature (22°C). The
manufacturer’s whole body Version 5.54 (Hologic).
day before testing, the subjects had eaten their last evening
The volume of internal organs (brain, heart, liver, kidneys,
meal between 6:00 and 7:00 PM. For $1 h, gas exchange
spleen) was measured by transversal MRI images. The scans
measurements were done continuously. The first 20 min of
were made by use of a 1.5-Tesla Magnetom Vision scanner
data were omitted. For the residual time of investigation (i.e.,
(Siemens, Erlangen, Germany). All organs were examined
for a period of $40 min), data were integrated for 5-min
native and without distance factors. The slice thickness for
intervals. The means of $40 measurements were presented
the brain was 6 mm, for the heart, 7 mm, and for abdominal
as individual values. Calibrations of the gas analyzers were
organs, 8 mm. The brain and the abdominal organs of the
performed immediately before and after the measurements.
participants were examined by T1-weighted breathhold
Variation caused by the technique was calculated on the basis
FLASH sequences (repetition time, TR: 174.9 ms; echo time,
of five repeated measurements of propane combustion and
TE: 4.1 ms/echo). Because of the movement of the heart and to
was found to be ,4%. The within-day coefficent of variation of
prevent artifacts, ultra-short scans were made by electrocar-
the 5-min oxygen consumption (V̇O2) values was ,7.5%. diogram (ECG)-triggered, T2-weighted HASTE sequences
Intraindividual variances in REE were assessed in a sub- that were taken in breathhold technique (acquisition time: 20
group of 10 weight-stable men, who performed test-retest ms). The volume of the organs was calculated from the sum of
measurements on three different days within a 14-day period. cross-sectional areas as determined ‘‘by hand’’ (i.e., by exactly
The intraindividual variances were ,6%. REE was calcu- drawing a line at the external limits of the organs) and
lated as described by Weir (30): kcal/min 5 V̇O2 (l/min) 3 multiplied by the scan’s slice thickness. All scans were read
[3.9 1 (1.1 3 RQ)], where RQ is respiratory quotient. REE by the same trained observer (K.I.); the coefficient of varia-
(kcal/day) was also calculated using various prediction formu- tion, based on three test-retest measurements, was ,1%.
las as proposed by the following investigators Volume data were transformed into organ weights by use of
Cunningham (Ref. 3) the following densities: 1.036 g/cm3 for brain, 1.06 g/cm3 for
heart and liver, 1.05 g/cm3 for kidneys, and 1.054 g/cm3 for
REE 5 21.6 3 FFMCalc 1 501.6 (1) spleen (7). Total body mass was considered as the sum of

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Copyright © 2000 American Physiological Society. All rights reserved.
E310 ORGAN-TISSUE MASS AND ENERGY EXPENDITURE

organ masses. Residual mass was calculated as body mass c 1 (k2 3 kg FFMBIA 1 k3 3 kg FMDEXA ) (7)
minus the sum of skeletal muscleDEXA, brainMRI, heartMRI,
liverMRI, kidneysMRI, spleenMRI, bone mineralDEXA, and fat d 1 (k4 3 kg muscle massDEXA
massDEXA (5 residual 1 in Tables 1–3). Because skeletal 1 k5 3 kg liver weightMRI ) (8)
muscleDEXA assesses appendicular, and not whole body skel-
etal muscle mass, residual mass was reanalyzed using skel- In addition, whole body REE (REEc) was calculated as the
etal muscleANTHRO (5 residual 2 in Tables 1–3). Residual sum of seven individual organs (brainMRI, liverMRI, skeletal
mass was also calculated assuming constant contributions of muscleDEXA, fat massDEXA, plus residual organs) times organ-
blood volume (i.e., 7.9% body wt), skin (3.7% body wt), tissue metabolic rates, on the basis of organ-tissue metabolic
connective tissue (2.3% body wt), lung tissue (1.4% body wt), rates reported by Elia et al. (10)

REEc 5 (1.008 3 brain massMRI) 1 (840 3 liver massMRI ) 1 (1.848 3 heart massMRI ) 1 (1.848 3 kidney massMRI )
(9)
1 (55 3 skeletal muscle massDEXA ) 1 (19 3 fat massDEXA ) 1 (50 3 residual mass 1)

intestine (1.7% body wt) to body weight, as given in Ref. 9 (5 The agreement between calculated and measured REE
residual 3 in Tables 1–3). was analyzed by plotting the difference between mea-
Methodological limitations. Calculation of organ masses sured and calculated REE vs. the average of REE mea-
from data obtained by imaging techniques is based on 1) the sured and REE calculated, as described by Bland and Alt-
sum of cross-sectional areas multiplied by the distance be- man (2).
tween scans [coefficient of variation (CV) ,1%] and 2) approxi-
mate organ densities taken from the literature (7). In vivo
organ weight was measured to the nearest 0.1 kg. This is RESULTS
within the order of the accuracy reached for radiographic
volume and mass determination by use of excised human
Body composition data. Body masses, as well as the
cadaver organs (i.e., 63–5%; Refs. 15, 16). If a standard organ sizes of the subjects, are shown in Table 1.
deviation for organ weights of #0.4 kg and a mean specific Significant sex-dictated differences were seen for weight,
energy expenditure of ,1,255 kJ/kg organ weight are as- height, total body waterBIA, FFMBIA, fat massDEXA, fat
sumed (15), the precision of the imaging techniques may
introduce a considerable error (i.e., 7–9% of REE). This may
contribute to the residual variance in REE and also limit the Table 1. Characterization of study population
value of modeling REE from metabolically active tissue mass.
Females Males
There is also evidence that our approach to assessing metaboli- n 5 13 n 5 13
cally active components of FFM left a considerable amount of
so-called ‘‘residual masses’’ unexplained. Residual mass is a Age, yr 24.8 6 2.4 26.2 6 2.1
heterogeneous component that includes intestine, pancreas, Body weight, kg 62.8 6 9.5† 72.3 6 10.2
Body height, cm 169.6 6 6.2† 185.2 6 7.7
lung, skin, blood volume, endocrine glands, and connective BMI, kg/m2 22.14 6 2.47 22.53 6 1.82
tissue. It is evident that different calculation procedures Total body waterBIA , liters
result in different amounts of residual mass (see residuals (% body wt) 32.8 6 3.1 (52.2)† 42.2 6 5.0 (58.4)
1–3, Tables 1–3). These differences are in part explained by Fat free massBIA , kg
the methods used to assess skeletal muscle mass (e.g., (% body wt) 45.9 6 4.7 (73.1)† 63.1 6 6.9 (87.2)
skeletal muscle massDEXA measures appendicular instead of Organ masses, kg
whole body muscle mass). The close association between the (% body wt)
MuscleDEXA 17.9 6 2.5 (28.5)† 28.8 6 3.0 (39.8)
different measures of residual mass and 1) FFMBIA and thus MuscleANTHRO 21.5 6 4.1 (34.2)† 31.9 6 5.5 (44.2)
2) REE suggests that residual mass indirectly reflects meta- BrainMRI 1.5 6 0.1 (2.4) 1.6 6 0.2 (2.2)
bolic active tissues (Table 2–3). HeartMRI 0.3 6 0.0 (0.5)† 0.4 6 0.1 (0.6)
Data analyses. All data were recorded in a database system LiverMRI 1.5 6 0.2 (2.4) 1.7 6 0.3 (2.4)
with a personal computer; statistical analyses were per- SpleenMRI 0.2 6 0.0 (0.3)* 0.3 6 0.1 (0.4)
formed by SPSS for Windows 5.0.2. Data are presented as KidneysMRI 0.2 6 0.0 (0.3)† 0.2 6 0.1 (0.3)
means 6 SD. The Mann-Whitney U-test or Fisher’s Exact Bone mineralDEXA 2.4 6 0.3 (3.8)† 3.2 6 0.6 (4.4)
FatDEXA 19.2 6 6.0 (30.6)† 12.9 6 4.5 (17.8)
Test was used for comparisons between groups. Pearson’s Residual 1 (muscle mass-
correlation coefficients were calculated to test for relation- DEXA ), kg (% body wt) 19.7 6 2.1 (31.7)† 28.3 6 4.2 (36.6)
ships among different parameters. In addition, a multivariate Residual 2 (muscle
stepwise regression analysis was performed using REE as massANTHRO ), kg (%
dependent variable. A probability value of 0.05 was accepted body wt) 16.2 6 3.8 (26.2)† 25.1 6 4.0 (32.8)
as the limit of significance. The specific contributions of body Residual 3 (theoretical),
weight, FFM or muscle mass, and organ masses (i.e., slopes or kg (% body wt) 10.7 6 1.6 (17.0)† 13.1 6 1.7 (17.0)
REE, MJ/day 5.74 6 0.68† 7.28 6 0.85
k values) were calculated from the individual regression
RQ 0.84 6 0.05 0.85 6 0.05
lines. The model assumes that whole body REE is the sum of
respiration of the individual tissues. Then REE was predicted Values are means 6 SD. BMI, body mass index; BIA, bioelectrical
by different formulas impedance analysis; DEXA, dual-energy X-ray absorptiometry; MRI,
magnetic resonance imaging; ANTHRO, anthropometrics; REE, rest-
a 1 (k1 3 body wt.) (5) ing energy expenditure; RQ, respiratory quotient. Residual 3 (theo-
retical) is calculated from fixed organ weights as assumed by Elia (9).
b 1 (k2 3 kg FFMBIA ) (6) Significant differences between genders: * P , 0.05; † P , 0.01.

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Copyright © 2000 American Physiological Society. All rights reserved.
ORGAN-TISSUE MASS AND ENERGY EXPENDITURE E311

massANTHRO, and the different organs measured except

Residual 2
for brainMRI and liverMRI. The water content of LBMDEXA

0.57†
was calculated from TBWBIA and LBMDEXA to be 0.73 6
0.03 in females and 0.73 6 0.00 in males, respectively.
Residual mass accounted for 32 and 37% of body weight

Residual 1
in males and females, respectively (Table 1). Calculat-

0.87†
0.83†
ing residual mass based on the assumption of constant
contributions of blood volume, skin, intestine, connec-
tive tissue, and lungs gave residual masses of 13.1 6

Table 2. Pearson correlation coefficients among body compartment sizes in 26 healthy subjects as assessed by different methods
TBWBIA
1.7 kg (male) and 10.7 6 1.6 kg (female), respectively (5

0.95†

0.85†
0.78†
residual 3). There were significant and sex-independent
differences between residual mass 1 and 2 or 3, respec-
tively (P , 0.01 or , 0.05). We also found significant

20.28NS
20.26NS

0.22NS
FatDEXA

20.55†
differences between residual masses 2 and 3 (P , 0.01).
DEXA was used to assess the composition of different
regions of the body (i.e., trunk 5 t, legs 5 l, arms 5 a).

BoneDEXA

0.04NS
The different segments contributed to body masses by

0.84†
0.83†
0.57†
0.89†
44 and 45% (t), 39 and 36% (l), and 11 and 13% (a) in
females and males, respectively. Proportions of fat for
each region were greater in females than in males (t:

SpleenMRI

20.08NS
0.65†

0.70†
0.76†
0.47*
0.70†
23.7 6 6.7 and 15.0 6 5.2%, l: 38.1 6 4.5 and 17.6 6
4.7%, a: 36.1 6 7.3 and 15.7 6 4.0% segmental weight
for females and males, respectively; P , 0.01 for sex
differences). By contrast, the proportions of weight of

KidneysMRI

20.08NS
0.71†
0.61†

0.61†
0.69†
0.54†
0.63†
trunk, arms, and legs consisting of LBMDEXA were
increased in males (t: 74.0 6 6.6 and 82.8 6 5.0%;
l: 58.0 6 4.4 and 77.6 6 4.5; a: 59.1 6 7.0 and 79.3 6
3.9% segmental weight, in females and males, respectively, LiverMRI

0.21NS
0.44*
0.47*
0.67†

0.63†
0.68†
0.43*
0.77†
P , 0.01 for sex differences). Regional proportions of bones
were similar between sexes (data not shown).
The relationships between different body and tissue

20.34NS
HeartMRI

0.45*
0.69†
0.59†
0.71†

0.78†
0.82†
0.77†
0.68†
masses are given in Table 2. There were significant

FFM, fat-free mass; TBW, total body water. * P , 0.05; † P , 0.01; NS, not significant.
correlations between FFMBIA and all other organs
except the brain. Fat massDEXA did not reach significant
associations with body weight in normal-weight sub-
0.35NS
0.36NS
20.17NS
BrainMRI

0.40*
0.42*
0.41*

0.41*
0.54*
0.46*
0.42*
jects. Plotting the ratio of skeletal muscle massDEXA and
the sum of organ massesMRI against FFMBIA showed
significant and positive association (Fig. 1).
REE and body composition. Measured REE varied
MuscleDEXA

20.34NS
0.43*
0.81†
0.57†
0.59†
0.68†
0.83†

0.97†
0.94†
0.83†
0.83†
from 4.77 to 8.62 MJ/day. REE values were higher in
males than in females (127%; P , 0.001; Table 1).
Adjusting REE on the basis of group mean REE plus
the measured REE minus predicted REE (as predicted
20.21NS
FFMBIA

0.97†
0.40*
0.77†
0.66†
0.61†
0.72†
0.86†

0.99†
0.95†
0.76†
0.89†

from the individual FFMBIA in the linear regression


equation generated in our population) (see Fig. 2 and
Ref. 25 for details of the underlying assumptions) gave
similar values for both sexes [m, 6.45 6 0.51 vs. f,
0.21NS
0.17NS

0.22NS
0.37NS

0.10NS
0.47*
0.36†

0.63†

0.59†
0.63†
0.40*
0.40*

0.73†
BMI

6.58 6 0.30 MJ/day; not significant (NS)].


REE was significantly associated with FFMBIA (r 5
0.92), muscle massDEXA (r 5 0.89), and the sum of
0.28NS

20.16NS

0.71†
Height

0.89†
0.90†
0.44*
0.81†
0.58†
0.69†
0.71†
0.80†

0.88†
0.90†

0.86†

organsMRI (r 5 0.90) (Fig. 2, Table 3). There were no


sex-dictated differences between the slopes of the REE
regression lines when FFMBIA, muscle massDEXA, or
Body Wt

organ massMRI was used as the variable. REE


0.22NS

0.57†
0.86†
0.73†
0.89†
0.83†
0.42*
0.68†
0.77†
0.63†
0.70†
0.89†

0.85†
0.87†

1.00†

(kJ · day21 · kg FFM21) was 126, 121, and 114 for sub-
jects with different FFM values, i.e., FFM ,50 kg (n 5
10), FFM 50–60 kg (n 5 9), and FFM .60 kg (n 5 7),
MuscleDEXA

KidneysMRI

Residual 2
Residual 1

Residual 3

respectively (P , 0.01 for the difference in REE/FFM


SpleenMRI
BoneDEXA
HeartMRI
BrainMRI
Body Wt

LiverMRI

TBWBIA
FatDEXA
FFMBIA

between subjects ,50 kg FFM vs. .60 kg FFM).


Height
BMI

Plotting REE on the ratio of skeletal muscle massDEXA


to the sum of organ massesNMR resulted in a positive

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Copyright © 2000 American Physiological Society. All rights reserved.
E312 ORGAN-TISSUE MASS AND ENERGY EXPENDITURE

Table 3. Pearson correlation coefficients


between REE and age, body, or organ sizes
Resting Energy Expenditure

Females Males All

Age 20.62* 0.14NS 0.07NS


Body wt 0.88† 0.75† 0.88†
Height 0.75† 0.49*NS 0.82†
BMI 0.75† 0.63* 0.55†
FFMBIA 0.95† 0.80† 0.92†
MuscleDEXA 0.94† 0.68† 0.89†
BrainMRI 0.27NS 0.49* 0.51†
HeartMRI 0.13NS 0.46NS 0.72†
LiverMRI 0.77† 0.82† 0.74†
KidneyMRI 0.58* 0.12NS 0.52†
SpleenMRI 0.53* 0.43NS 0.67†
BoneDEXA 0.86† 0.47NS 0.79†
FatDEXA 0.66† 0.35NS 20.09NS
TBWBIA 0.81† 0.80† 0.90†
Residual 1 0.76† 0.79† 0.89†
Residual 2 0.22NS 0.38NS 0.69†
Residual 3 0.88† 0.75† 0.88†
Significance between REE and individual variables: * P , 0.05;
† P , 0.01.

Prediction of REE. Predicting whole body REE from


FFMBIA 6 FMDEXA by use of formulas 1–4 (METHODS)
Fig. 1. Ratios of high energy (sum of organs 5 organ massMRI)- vs. resulted in a very close agreement between measured
low energy-requiring organs (5 skeletal muscleDEXA) plotted against
FFMBIA. BIA, bioelectrical impedance analysis; DEXA, dual-energy and predicted values (mean deviations between 1155
X-ray absorptiometry; MRI, magnetic resonance imaging; FFM, and 2485 kJ/day). There were no systematic errors in
fat-free mass. groups of subjects differing with respect to their body
mass index (BMI, ,21 vs. 21–23 vs. .23 kg/m2) or their
and significant association (data not shown). Plotting FFMBIA (,50 vs. 50–60 vs. .60 kg) (data not shown).
REE per kilogram FFMBIA on the ratio of skeletal Calculating REE (REEc) on the basis of measured
muscle massDEXA per sum of organsMRI gave a negative organ masses times constant organ tissue respiration
and significant correlation (Fig. 3). rates, as reported in the literature (formula 9), a mean
In a multiple stepwise regression analysis, FFMBIA prediction error of 96 kJ/day was observed. There was a
alone explained 85% of the variance in REE (SE of the very close correlation between theoretically calculated
estimate 423 kJ/day). Additionally, including the sum (according to formula 9) and measured REE (Fig. 4).
of internal organsMRI into the model increased the r2 to We found significant differences in REE and REEc
0.89 with a SE of 381 kJ/day. In a stepwise multiple (according to formula 9: FFMBIA ,50 kg, n 5 10, vs.
regression analysis, only skeletal muscleDEXA and liver FFMBIA 50–60 kg, n 5 9, vs. FFMBIA .60 kg, n 5 7;
massMRI significantly contributed to REE, as indicated REE, 5.4 6 0.4 vs. 6.7 6 0.5 vs. 7.8 6 0.7 MJ/day; REEc,
in the following regression equation 5.7 6 0.4 vs. 6.7 6 0.4 vs. 7.7 6 0.9 MJ/day; P , 0.01 vs.
FFMBIA 50–60 kg) between groups differing with re-
REE 5 359 1 29 3 skeletal muscle massDEXA spect to FFMBIA. A Bland-Altman plot showed no signifi-
(8a) cant trend (r 5 0.19; P 5 0.357) between measured and
1 319 3 liver massMRI calculated REE difference (i.e., the difference between

Fig. 2. Metabolically active compo-


nents of FFM plotted against resting
energy expenditure (REE) by BIA,
DEXA, and MRI-DEXA.

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ORGAN-TISSUE MASS AND ENERGY EXPENDITURE E313

Fig. 3. REE per kg FFMBIA plotted against different ratios of high- Fig. 4. REE plotted against REE calculated according to formula 9
vs. low energy-requiring organs. (REEc). REEc was calculated from organ masses times constant
tissue respiration rates as reported from the literature (see METHODS
for details of underlying assumptions).
REE measured and REE calculated according to formula 9
vs. the average of REE measured and REE calculated;
Fig. 5), suggesting that there is no systematic error. REE. This is close to our data, as well as to the recent
results of others (12, 27), which were all based on direct
DISCUSSION and concomitant in vivo assessments of organ masses
and REE. By contrast, Deriaz et al. (6) and McNeill et
REE varies among individuals. Body size, body com-
position, age, sex, hormones, and genetic factors ex-
plain most of its variability (1, 24, 28). It has been
speculated that the relative proportion of high and low
metabolically active tissues independent of differences
in FFM significantly adds to the residual variance in
REE (24, 28, 29).
Our present knowledge regarding the contribution of
individual organs to REE in humans is mainly based on
1) in vitro measurements of tissue respiration (5, 9, 19)
and 2) postmortem analysis of body composition (10, 14,
15). These studies suggest that 1) V̇O2 per gram tissue
is relatively constant and 2) organ size is a major
determinant of REE. Tissue V̇O2 can be directly esti-
mated in vivo by measurements of the arteriovenous
(a-v) differences of O2 together with blood flow measure-
ments. Methodological problems may limit the in vivo
assessment as well as the interpretation of organ-
tissue metabolic rates (11). However, the in vivo data
suggest that the sum of regional V̇O2 exceeds whole
body REE (3, 5). The comparison of in vivo with in vitro
data is inconclusive (5). Thus our knowledge on energy
expenditure-body composition relationships in humans
is limited.
On the basis of data obtained from 1,598 autopsies
and with the assumption of a constant mass-specific
energy expenditure, Garby and co-workers (14, 15) Fig. 5. Bland-Altman Plot exploring the agreement between calcu-
calculated that the composition of FFM may explain 5% lated (according to formula 9) and measured REE. Dotted lines are
of the variation in the between-subjects variation in given for the first SE values.

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Copyright © 2000 American Physiological Society. All rights reserved.
E314 ORGAN-TISSUE MASS AND ENERGY EXPENDITURE

al. (21) provided no evidence that the composition of only limited in vivo data on organ-tissue V̇O2. Suitable
FFM explains any of the variance in whole body REE. methods (e.g., 150 or positron emission tomography, Ref.
Regarding the role of metabolically very active organs 26) for the in vivo assessment of regional V̇O2 should be
(i.e., muscle, brain, liver) contributing to REE, the applied in future studies. These techniques will contrib-
different authors also came out with different results. ute to the development of new energy expenditure-body
We found that skeletal muscle and liver are the major composition estimation models.
determinants of REE in young, healthy, and nonobese Body size-related variations in REE are explained by
subjects (RESULTS). By contrast, Gallagher et al. (12) 1) the proportional contributions of different organs to
found that brain and skeletal muscle were the major FFM, as well as 2) tissue O2 consumption. In a stepwise
determinants of REE. The discrepancy between the multiple regression analysis, FFM alone explains 85%
results of these two studies may be explained by of the variance in REE, leaving an SE of the estimate of
differences in the database (e.g., the number and age of 423 kJ/day (RESULTS). Calculating REE as the sum of
the subjects differ between the two studies). In the two individual organ-tissue masses times a constant organ-
other studies, only skeletal muscle mass (6) or muscle tissue respiration rate, on the basis of data published in
plus fat plus heart mass (27) significantly contributed the literature (10), reduces the variance in REE and
to the prediction of REE. However, in their multiple results in small differences between measured and
regression analysis, Deriaz et al. used only skeletal calculated REE of 83 (12) or 96 kJ/day (this paper),
muscle mass and nonmuscular LBM (which is the sum respectively. However, it should be mentioned that the
of internal organs). Thus these authors could not use of standard formulas for the prediction of REE also
differentiate among individual organs. In addition, in reaches a very high precision in our homogeneous
the study by Deriaz et al., only a limited number of CT group of young, healthy, and nonobese subjects. It is
scans at nine selected sites were performed, and the tempting to speculate that the accuracy of prediction
relationship between REE and FFM was poor (i.e., r 5 may differ in a more heterogeneous sample of subjects
0.56 for REE vs. LBMCT, or r 5 0.49 for REE vs. FFM, (e.g., in patients with chronic diseases or obese patients).
as determined by densiometry; Ref. 6). Compared with In conclusion, the proportions of metabolically active
Deriaz et al., Sparti et al. measured liver but not brain components of REE contribute to the variance in REE
by serial CT images (27). In addition, appendicular and also explain the relation between REE and FFM.
skeletal muscle mass was measured by DEXA. With The essential findings of the present study are that 1)
use of simple correlation coefficients, muscle and liver the contribution of the mass of the metabolically more
showed significant associations with REE (r 5 0.84 and active internal organs to the variance in REE is ,5%;
0.75, respectively), which is very close to our data (r 5 only skeletal muscleDEXA and liverMRI significantly con-
0.94 and 0.77, respectively; see Table 3). Because a tribute to REE; 2) the decrease in REE per kilogram
homogeneous and comparable group of subjects was FFM with increasing FFM is explained by the changing
studied in both studies (27, this study) and similar proportions of metabolically active compounds of FFM;
methods have been used (CT, echocardiography, DEXA and 3) predictions of REE on the basis of individual
in Ref. 27; MRI, DEXA, BIA in this study), it is unclear organ masses were very close to measured REE. Our
why muscle but not liver reached statistical signifi- data support the assumptions (3, 24, 28, 29) and the
cance in Sparti’s regression analysis. It should be data of some authors (12) but are contrary to the results
mentioned that both studies (Ref. 27 and this study), of others (6, 21, 27).
although very similar with respect to the physical A preliminary report of this work was presented in abstract form
variables of the subjects, differ with respect to the at the 16th International Congress of Nutrition, Montreal, 1997 (PW
14.3).
magnitude of some internal organs (i.e., kidney mass Address for reprint requests and other correspondence: M. J.
was higher but left ventricular mass was lower in Ref. Müller, Institut für Humanernährung und Lebensmittelkunde, Chris-
27 compared with our data). Some of the differences in tian-Albrechts-Universität zu Kiel, Düsternbroker Weg 17, D-24105
organ masses given in the different studies (12, 27, this Kiel, Germany (E-mail: mmueller@nutrfoodsc.uni-kiel.de).
study) are due to methodological problems. For ex- Received 4 January 1999; accepted in final form 20 September 1999.
ample, Sparti et al. (27) as well as Gallagher et al. (12)
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