Research Department of Human Nutrition, Center for Food Research, The Royal Veterinary and Agricultural University, DK-1958 Frederiksberg, Denmark
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ABSTRACT |
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Muscle fiber
morphology and activities of four key enzymes, as well as energy
metabolism, were determined in nine normal-weight postobese women and
nine matched control subjects. No differences in fiber type
composition, but a smaller mean fiber area and area of fiber types I
and IIb, were found in postobese compared with control subjects
(P < 0.05). The activities of
-hydroxyacyl-CoA dehydrogenase (HADH) and citrate synthase (CS) were
20% lower in postobese than in control subjects
(P < 0.05). However, the activities
of lactate dehydrogenase and lipoprotein lipase were not significantly
different between postobese and control subjects. Basal metabolic rate
and respiratory exchange ratio were also similar, but maximal oxygen
uptake (
O2 max)
tended to be lower in postobese than in control subjects
(P = 0.06). When adjustments were made
for differences in
O2 max, HADH and CS
were not different between postobese and control subjects. In
conclusion, these data suggest that smaller fiber areas and lower
enzyme activities, i.e., markers of aerobic capacity of skeletal
muscle, but not fiber composition, may be factors predisposing to
obesity.
aerobic capacity; -hydroxyacyl-CoA dehydrogenase; citrate
synthase; lactate dehydrogenase; lipoprotein lipase; basal metabolic
rate; diet
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INTRODUCTION |
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A REDUCED CAPACITY FOR FAT OXIDATION, with a resulting
positive fat balance, is an important etiological factor of obesity (4,
36). This, among other factors, is evidenced by studies in
obesity-prone normal-weight subjects who have been found to have a
lower lipid oxidation than never-obese subjects when subjected to a
fat-rich diet (2, 32). The reasons for this lower fat oxidative
capacity are, however, still unclear. They may relate to abnormalities
in the adipose tissue (storage, release) and/or in skeletal
muscle (uptake, oxidation). With regard to the adipose tissue, we found
that fat was stored more efficiently and lipolysis was more suppressed
after a fat-rich meal in postobese subjects (32). In contrast, the
release of fat from adipose tissue for oxidation in skeletal muscle
postabsorptively or during exercise may be intact in postobese
subjects. Thus fat mobilization was found to be similar in postobese
and matched control subjects during and after 1 h of exercise at 50%
maximal oxygen uptake (O2 max) (35).
The lower fat oxidation observed in postobese subjects may, however,
also relate to a reduced capacity in skeletal muscle to take up
and/or oxidize the circulating lipids. Several studies have
been published on the relation between obesity and muscle fiber types
and biochemical characteristics, although with conflicting results (19,
20, 22, 37, 40, 44, 47). Some studies have reported that obesity is
related to a relative reduction in oxidative muscle fibers (type I)
(20, 22, 44) and/or a relative increase in glycolytic muscle
fibers (type IIb) (19, 20, 22). However, no such relations were found
in another study (41). As for enzyme activities, the activity of
citrate synthase, malate dehydrogenase, and oxoglutarate dehydrogenase, all oxidative key enzymes in the tricarboxylic acid cycle (i.e., markers of muscle aerobic-oxidative capacity), was found to be negatively related to body fat or weight gain (19, 37, 40). Also, a low
activity of -hydroxyacyl-CoA dehydrogenase (a key enzyme in fatty
acid oxidation) was found to correlate with a high 24-h respiratory
quotient (RQ) in Pima Indians and, thereby, to an increased risk of
weight gain (47).
Together these studies indicate that muscle morphology and oxidative capacity are important in the etiology of obesity. To our knowledge, data on muscle morphology and enzyme activities in normal-weight subjects [body mass index (BMI) <25.0 kg/m2] with the genetic predisposition to obesity have not yet been reported. The aim of the present study was therefore to measure muscle morphology and activities of selected key enzymes in normal-weight postobese subjects and compare these data with those of normal-weight, never-obese, matched control subjects.
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METHODS |
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Subjects.
Eighteen healthy, normal-weight women [9 postobese (PO) and 9 matched control (C) subjects] participated in the study (Table 1). The PO women had a family history of
obesity (1 obese parent or sibling), had been >20% overweight
[means ± SE = 47 ± 6.4% (29)], and had been weight
stable (±3 kg) for
2 mo. All had dieted, and some also exercised,
but none had undergone surgical operations to become of normal weight.
The weight loss had taken place gradually. Two PO and two C subjects
smoked regularly, and one C subject smoked only on social occasions.
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Matching measurements.
Body weight was measured by a digital scale to the nearest 0.1 kg (Seca
model 708, Seca me- und Wiegetechnik, Bogel & Halke, Hamburg,
Germany) with subjects wearing underwear. Body composition for the
matching procedure was measured by electrical bioimpedance using an
animeter (HTS Engineering, Odense, Denmark).
FMimp and FFMimp values were calculated
using the equations by Heitmann (16). Height was determined to the
nearest 0.1 cm. Waist and hip circumferences were measured with a tape
measure, also to the nearest 0.1 cm. Waist was measured as the smallest
circumference above the navel (midtorso) and hip as the largest
circumference around the hip (between trochanter major and the iliac
crest). Sagittal height was measured to the nearest 0.5 cm at the
maximal height of the stomach with subjects lying down, resting, and
after a normal exhalation. Blood pressure was measured using an
automatically inflating cuff (UA-743, A & D, Tokyo, Japan), with the
subjects relaxed and lying down.
Muscle fiber and enzyme analyses.
Subjects arrived at the Copenhagen Muscle Research Center,
Rigshospitalet, Copenhagen, Denmark, in the morning after 10 h of
fasting; they rested in the supine position. Twenty to fifty milligrams
of muscle tissue were taken by needle biopsy technique (5) from the
vastus lateralis, 12-16 cm above the knee. A bundle of muscle
fibers was dissected out, mounted for histochemical studies in a
plastic material (Tissue-Tec), and frozen in nitrogen-cooled isopentane
(
130°C). The remaining portion of the muscle piece was
carefully freed from visible fat, connective tissue, and blood and was
frozen in liquid nitrogen. An additional piece of muscle was quickly
washed in saline, dried on filter paper, and frozen in liquid nitrogen.
This piece was used for determination of lipoprotein lipase activity.
All samples were stored at
80°C until analyzed. Water
content of the muscle samples was obtained by a weighing-drying procedure (26). Water content was in the normal range, i.e., 76.7 ± 0.4% (SE) for PO and 76.7 ± 1.0% for C subjects
(P = 0.98).
BMR.
BMR and respiratory exchange ratio (RER) were measured by indirect
calorimetry with an open-circuit, computerized ventilated hood system
(12). The measurements were performed in the morning on
days 7-10 of the menstrual cycle
after 10 h of fasting. Subjects arrived at the department by car,
train, or bus; they voided and rested for 30 min in the supine
position. BMR and RER were measured during the subsequent 30 min.
Carbon dioxide was measured with an infrared analyzer (Uras 10P,
Hartmann & Braun, Frankfurt, Germany) and oxygen with a paramagnetic
analyzer (model 1100A, Servomex, Sussex, UK). Ventilation
through the hood was determined by a Hastings mass flowmeter (type HFM
201-100; Teledyne Hastings-Raydist, Hampton, VA). BMR was
calculated by the Weir formula (45). RER was calculated as the ratio
between CO2 excretion and
O2 uptake. There was no correction
for urinary nitrogen, but this would introduce an error of <2% (28).
Training status.
The subjects' O2 max
was determined on an exercise bike. Subjects initially warmed up for 3 min at 70 rpm and 0.5 kg, corresponding to a workload of 35 W. The
workload was increased by 0.5 kg (35 W) every 3 min until exhaustion,
i.e., when the subjects could no longer continue exercising (~210 W).
Gas exchange was continuously monitored by an on-line system (Medical
Graphics). Heart rate was simultaneously monitored by a telemetric
system (Polar Sport Tester). The highest oxygen uptake measured during
the test was considered to be the subject's
O2 max.
DXA scanning. Fat mass (FMDXA), fat-free mass (FFMDXA), and bone mineral content were determined once by a Hologic 1000/W DXA scanner (Hologic, Waltham, MA). For analysis, software version 5.61 was used. Subjects were nonfasting, wearing underwear and a cotton T-shirt. These data on body composition are used in the correlation analyses.
Habitual diet. The subjects recorded their habitual diet using a 7-day weighed-food record after having received careful oral and written instructions by a dietician. The energy intake was compared with the subjects' calculated energy needs (see above), and the percentage of under- or overreporting was calculated. Energy and macronutrient intake was calculated by the computer database of foods Dankost 2.0 from the National Food Agency of Denmark (Søborg, Denmark) (30).
Statistical analysis. Data are expressed as means ± SE. An unpaired t-test was used to test for differences between PO and C subjects. The significance level was set at P < 0.05. Simple correlation analyses were performed between the different measures. All significant correlations were plotted and, in case of extreme outliers (>95% confidence limits), reanalyzed and reported without this/these value(s). Forward stepwise selection analyses were performed for the four enzymes. The variables included were selected from the simple correlation analyses (P < 0.20), and an F value of 4.00 was the limit for a variable to enter the model. The adjusted R2 values are given (the adjustment compensates for the expected chance prediction when the null hypothesis is true). Statgraphics Software version 4.2 (Graphic Software Systems, Rockville, MD) was used in the statistical calculations.
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RESULTS |
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Muscle fibers and capillaries. The percentage of the different fiber types was similar in PO and C subjects (PO vs. C, type I: 53.4 ± 3.9% vs. 52.0 ± 4.7%; type IIa: 20.4 ± 1.6% vs. 19.7 ± 3.2%; type IIb: 9.3 ± 3.1% vs. 9.3 ± 2.7%; intermediary: 16.8 ± 2.0% vs. 19.1 ± 3.0%; P > 0.50) (Fig. 1). However, the area of fiber types I and IIb and mean fiber area were significantly smaller in PO than in C (PO vs. C, area I: 4,450 ± 200 vs. 5,429 ± 366 µm2 ; area IIb: 2,118 ± 467 vs. 4,121 ± 576 µm2; mean area: 3,910 ± 203 vs. 4,909 ± 372 µm2; P < 0.05) (Fig. 2). No significant differences were observed in the area of fiber type IIa (3,686 ± 246 vs. 4,297 ± 702 µm2, P = 0.42) or intermediary fiber area (3,210 ± 349 vs. 4,246 ± 447 µm2, P = 0.09). There were no differences in number of capillaries around each fiber type (Table 2), but fiber area per capillary was significantly smaller in PO than in C subjects (1,222 ± 64 vs. 1,555 ± 107 µm2, P < 0.05) (Fig. 2).
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Muscle enzyme activities.
The activities of HADH and CS were about 20% lower in PO than in C
subjects (P < 0.05) (Fig.
4). These differences still remained after
inclusion of smoking as a covariate in the analyses (HADH: P < 0.05, CS:
P = 0.058). The HADH-to-CS ratio, a
proposed expression for the ratio between fat oxidation and total
oxidation (17), was not different between the groups (Table 2). The
activity of LDH was 30% lower in PO, but the difference was not
significant (P = 0.08). Without one
extreme value in C (972 µmol · g1 · min
1),
this difference diminished (344 in PO vs. 429 µmol · g
1 · min
1 in C,
P = 0.12). All correlations with LDH
are reported without this outlier (n = 17). LPL activity was similar in the two groups (P = 0.85) (Fig. 4).
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BMR and training status.
BMR, RER, and O2 max
were not different between the two groups (Table
3). However,
O2 max expressed per
kilogram body weight tended to be lower in PO than in C subjects
(P = 0.06; Table 3).
O2 max
correlated negatively with age (r =
0.59, P < 0.01).
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DXA scanning. There was a tendency for kilograms of FMDXA and %FMDXA to be greater in PO than in C subjects (P < 0.06; Table 3). Kilograms of FFMDXA were, however, similar in the two groups, as was total bone mineral content (Table 3).
Habitual diet. Reported habitual energy intake was 22% lower in PO than in C subjects (P < 0.05) (Table 4). No significant differences in macronutrient intake were found between the groups. Compared with energy needs calculated from the BMR measurements, PO underreported by 6 ± 9% and C subjects overreported by 17 ± 8% (groups differ, P = 0.06).
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DISCUSSION |
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The present study discloses several interesting and potentially
important findings in muscle tissue of PO subjects. First, a 20% lower
activity of both HADH and CS was observed in the PO compared with the C
subjects. HADH is a key enzyme in -oxidation of fatty acids in the
muscle, and a reduced activity of this enzyme therefore points toward
reduced lipid-oxidizing capacity in the PO subjects. This finding
supports previous reports of reduced fat-oxidizing capacity of PO
subjects when on a fat-rich diet (2, 32). In line with this are also
the negative correlation between HADH and fat mass (%) found here and
the previously reported negative correlation between 24-h RQ and HADH
activity (low fat oxidation at a low HADH activity) (47). CS is the
first enzyme in the tricarboxylic acid cycle and is rate limiting for
the cycle. The reduced activity of CS found here is therefore a sign of
reduced capacity for oxidative disposal of glucose in the PO subjects. In the present study we saw no significant differences in the activity
of LDH between PO and C subjects. This indicates that nonoxidative
disposal of glucose is not different in the two groups. Controversies
exist, however, when the literature is examined. Thus a lower activity
of HADH and CS was found in the quadriceps femoris muscle of obese men,
but not of obese women, compared with lean subjects (43). No
differences in HADH were found between obese and lean men or women in
the study by Simoneau and Bouchard (37) after a match was made for
O2 max, although malate
dehydrogenase, a marker enzyme for the tricarboxylic acid cycle, was
still lower in obese men. One should bear in mind, however, that
studies in obese and PO humans cannot be readily compared because of
the substantial metabolic changes following the obese state.
A second major finding in the present study was the lack of differences in LPL activity between PO and C subjects. This was surprising, because a low LPL activity has been suggested to be a risk factor for obesity. Accordingly, LPL was found to correlate inversely with %body fat, here and previously (46), and with a low ratio of fat to carbohydrate oxidation (high 24-h RQ) in Pima males (13). Our findings, however, indicate that skeletal muscle LPL activity may not be a rate-limiting step for muscle fat oxidation in this group of PO subjects. As pointed out by Ferraro et al. (13), the flux of fatty acids into skeletal muscle might instead depend on mitochondrial oxidative metabolism, which is the key determinant of the intracellular lipid pool turnover rate. This is also supported by recent findings of reduced cellular capacity for fat oxidation rather than reduced fatty acid uptake or intracellular fat availability in obese compared with lean subjects (18).
A third interesting finding was the identical fiber type composition in PO and C subjects. This was also not entirely expected from the significant positive relations between obesity and type I fibers and the negative relations between obesity and type IIb fibers previously reported (19, 20, 22, 44). However, the finding is in agreement with the aforementioned larger study of Simoneau and Bouchard (37). They also agree with a recent study by Geerling et al. (14), which refutes the proposal by Wade et al. (44) that the proportion of oxidative type I muscle fibers relates to body fatness. If a certain fiber type composition is a predisposing, genetically determined risk factor for obesity, we should have observed differences in fiber types in our two study groups; for example, the PO group should have had relatively less of fiber type I and more of fiber type IIb. We also found no correlations between fiber type and fat mass, waist, or waist-to-hip ratio as found before (19, 20, 22, 44). The reason for this may be 1) that there is no important relationship or 2) the different methodology, i.e., a great variation in number and types of subjects (Caucasians or Pima Indians, lean or obese, predisposed to obesity or not, children or adults, young or old) used in the different studies.
A fourth finding of interest here was the smaller mean fiber area, area of muscle fibers I and IIb, and fiber area per capillary in PO compared with C subjects. Area of fiber type I and mean fiber area have been found to correlate positively with relative body weight and %body fat, i.e., the larger the body weight or fat mass, the greater the fiber area (22, 25, 44). In the present study we saw a negative relation between mean fiber area and %fat massDXA. Thus the smaller the fiber area, the greater the fat mass. This would therefore indicate that a small fiber area predisposes to obesity and corresponds to our PO subjects being more predisposed to weight gain than our C subjects. The smaller fiber area and area per capillary also imply that the PO should have a better insulin action than C subjects (25). This was not measured in the present study. We have reported earlier that insulin sensitivity in PO subjects was similar to that in C subjects as measured by the euglycemic hyperinsulinemic glucose clamp technique (41). In another study, however, we observed lower postprandial glucose and insulin responses after 2 wk on three different ad libitum diets in PO subjects, indicating higher insulin sensitivity in this group (34). The latter would therefore be in line with the present findings. Furthermore, it would correspond to data fram Pima Indians showing that increased insulin sensitivity was a risk factor for weight gain (36).
The reasons for the lower fiber area in PO subjects can be several.
Thus the previous weight reduction (23), a lower
O2 max, or different
genes may be involved (15, 39). Training has been shown to influence
oxidative enzyme activity, LPL activity, muscle fiber areas, and
sometimes also fiber composition (15, 38, 42). We cannot know whether
the PO subjects here were less physically fit (lower
O2 max) because of
different genes or different training levels, although the activity
diaries indicated no differences in the latter. In twin studies, the
response to both endurance training
(
O2 max and
endurance performance) and high-intensity intermittent training
(several enzyme activities) was shown to be genotype dependent (15,
39). Furthermore, a recent study in obesity-prone, sedentary women
suggested that skeletal muscle maximal oxidative capacity (measured by
ATP production from oxidative phosphorylation) is an inherent
characteristic of skeletal muscle within the individual (21). Genetic
factors may also be involved in the variation of regulatory enzymes of the glycolytic and citric acid cycles, reaching 25-50% of the total phenotypic variation (after adjustment for age and sex
differences) (6). Because of the cross-sectional design of the present
study, however, we cannot conclude whether the differences observed
here are causes (genetic make-up or low physical activity level) or consequences of obesity and the foregoing weight loss.
There were no differences in BMR (total or per kg FFM) or fasting RER between our groups of PO and C women. This corresponds to some but not all previous studies of PO and C subjects (8, 32). The lack of difference may, however, be due to the relatively small sample size used here and before and, therefore, to a lack of statistical power. Thus Astrup et al. (3) showed that, when pooling data from different studies (n = 28), BMR was in fact 8% lower in PO than in C subjects (P < 0.05).
Dietary records showed that our PO subjects consumed 22% less energy than C subjects. This corresponds to our previous study of dietary intake in PO women and C subjects (33). The lower intake is most likely not due to lower energy needs but rather to underreporting, because both BMR and calculated energy needs were similar in our two groups. This assumption is supported by the negative correlation between energy intake and BMI or FM found here. It is also supported by our previous study, in which measured 24-h energy expenditure was similar in PO and C subjects but PO subjects were still reported to consume 21% less energy than C subjects (33).
Smoking may influence some of the measurements in the present study (e.g., enzyme activities). There were two regular smokers in each study group, but analyses of the data with smoking as a covariate did not alter our findings.
In conclusion, we found reduced activities of HADH and CS and smaller fiber areas in PO compared with C subjects. This suggests a reduced aerobic capacity of skeletal muscle in this group of subjects and implies that this may be an important factor predisposing to obesity. Conversely, the present data do not support the contention that muscle fiber composition is important for the development of obesity.
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ACKNOWLEDGEMENTS |
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We thank John Lind, Ingelise Kring, and Bengt Saltin for expert technical assistance.
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FOOTNOTES |
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This study was supported by the Danish Research and Development Program for Food Technology 1990-1994, Danisco Sugar, and the Danish Medical Research Council Grants 12-9537-3 and 12-1610.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: A. Raben, Research Dept. of Human Nutrition, Center for Food Research, The Royal Veterinary and Agricultural Univ., 30 Rolighedsvej, DK-1958 Frederiksberg C., Denmark.
Received 17 February 1998; accepted in final form 4 June 1998.
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