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Clinical Science (1988)74,79-83
79
The strength, contractile properties and radiological density
of skeletal muscle before and 1 year after gastroplasty
D. J. NEWHAM, R. A. HARRISON*, A. M. TOMKINSt AND C. G. CLARK*
Department of Physiology, University College London, *Department of Surgery, University College London, The Rayne Institute, and
TDepartment of Human Nutrition, London School of Hygiene and Tropical Medicine, London
(Received 5 March/20 May 1987; accepted 7 July 1987)
SUMMARY
1. Skeletal muscle strength, contractile properties and
radiological composition have been studied in seven
morbidly obese adults (six female) before and 1year after
gastroplasty operations. The mean body weight fell from
138.3 k g ( s ~ 2 5 . 2to
) 99.7 kg(s~23.O)(P<0.001).
2. The strength and contractile properties (force/
frequency, relaxation rate and fatiguability) of both the
adductor pollicis and quadriceps muscles were unaffected
by the weight loss.
3. Computerized axial tomography scans obtained 1
year after surgery showed that the quadriceps contained
an abnormally high proportion of fat. The mean fat content was 10.8% (range 3.0-30.1%) compared with 1.6%
(range 0-5%) for normal muscle. Two individuals were
scanned before and after surgery and the fat content of
their quadriceps fell from 12.6% and 6.9% to 3.1% and
3.0%, respectively.
4. It is concluded that in obese individuals large
amounts of weight can be lost, from both subcutaneous
and intramuscular fat stores, without compromising either
the strength or contractile properties of skeletal muscles.
These results do not support the claim that skeletal
muscle contractility is a sensitive indicator of changes in
nutritional status.
Key words: computerized axial tomography, obesity,
skeletal muscle, surgery for obesity.
Abbreviations: BMI, body mass index; CT, computerized
axial tomography; HU, Hounsfield unit; MRR, maximal
relaxation rate; MVC, maximal voluntary contraction.
INTRODUCTION
Obese individuals are strongly encouraged to lose their
excess weight because of the significant health risks assoCorrewondence: Dr D. J. Newham, Department of Physiology, Ukversity College London, Gower Street, London
WClE 6BT.
ciated with obesity [l]and also by social pressures. Surgical intervention may be appropriate in cases of morbid
obesity, where the individual has a proven inability to lose
weight by voluntary dietary control despite strong
encouragement and support.
The surgical techniques used to reduce body weight are
principally aimed at reducing either the capacity of the
stomach or absorption from the gastrointestinal tract (i.e.
bypass surgery). In the past, the bypass procedure has
been associated with a large number of metabolic, nutritional and immunological complications, and reversal
operations are necessary in a significant proportion of
patients [2]. The gastroplasty procedure [3], in which a
proximal stomach pouch less than 50 ml in volume is
fashioned, has proved to be reliable and relatively free of
metabolic complications [4]. Whatever the actual procedure, surgery for obesity is intended to cause a considerable, relatively rapid and sustained weight loss. It is
obviously desirable to achieve and maintain the weight
loss without the patient becoming undernourished and
susceptible to the multiple consequences of protein
energy malnutrition.
In the last few years there have been a number of
reports stating that malnourished individuals have
abnormal skeletal muscle contractile properties [5-lo].
Furthermore, it has been claimed that tests of skeletal
muscle contractility are more sensitive indicators of small
changes in nutritional status than other currently available
techniques [ll,121.
The undernourished patient derives energy from
muscle tissue and thus the muscle bulk is reduced [13].
However, the hypothesis that skeletal muscle contractility
might be a sensitive and accurate indicator of changes in
nutritional status is relatively new and exciting, and if
correct would meet a real clinical need. While the detrimental consequences of malnutrition in both medical and
surgical conditions are well recognized, the detection of
early malnutrition is notoriously difficult by the conventionally used anthropometric, biochemical and immunological techniques [ 141.
80
D. J. Newham et al.
The aim of this study was to investigate whether the
strength or contractile properties of the quadriceps and
adductor pollicis muscles of obese individuals were
affected by the considerable reduction in both energy
intake and body weight that occurs in the first year after
gastroplasty. The density and cross-sectional area of the
quadriceps has been stfldied using computerized axial
tomography (CT ). This technique allows the measurement of the cross-sectional area of the whole limb, individual muscle groups and also subcutaneous fat depth
[ 151. The radiological density of each tissue compartment
can be measured and the proportion of fat within the
muscle calculated from the known density of fat and fatfree muscle [ 161.
METHODS
Patients
Seven morbidly obese patients (six females, mean age
38.8 years, range 33-49 years) were studied before and 1
year after gastroplasty. All underwent a gastroplasty
operation after it had been established that they were
euthyroid and were capable of losing weight during a 2
week period of hospitalization with strictly supervised
dietary restriction (1883J/day). Estimation of food intake
by the 2 week dietary diary method indicated that the
average energy intake 1 year after the operation was 2757
(range 2 175-3766) J/day.
The study was approved by the Committee on the
Ethics of Clinical Investigation at University College
London.
Muscle strength and contractile properties
The force of voluntary and electrically stimulated
isometric contractions of the adductor pollicis and
quadriceps muscles were studied using previously
described techniques [ 171.
The adductor pollicis was stimulated through the ulnar
nerve at the wrist. The surface recorded electromyogram
was used to ensure that the stimulation was supramaximal. Only tests in which supramaximal stimulation
was maintained throughout have been included in the
results.
The quadriceps were stimulated through large damp
electrodes bandaged on to the anterolateral aspects of the
thigh. Voltages sufficient to activate 20-40% of the
maximal voluntary force (at 30 Hz) were used. It has been
shown that if more than 15% of the muscle is activated by
stimulation at 30 Hz, the force/frequency relationship and
maximal relaxation rate (MRR) are independent of
voltage [ 181. Three maximal voluntary contractions
(MVCs) were performed for approximately 2 s and the
best was taken as the maximal force and measured in
Newtons (N).
To define the force/frequency relationship the muscles
were stimulated percutaneously at 1 Hz (for 5 s ) and at
10, 20,50 and 100 Hz (each for 2 s). A rest period of 5 s
was used between stimulation at each frequency. The
force at each frequency was expressed as a percentage of
that developed at 100 Hz (1/100%, 10/lOOo/~,etc.). The
maximal relaxation rate (MRR) was determined from the
differentiated force signal [19] at the end of the 100 Hz
tetanus and expressed as the percentage of force lost in 10
ms.
Fatiguability in the adductor pollicis was measured
during intermittent stimulation at 40 Hz for 250 ms in
each second for 3 min [20]. The quadriceps were stimulated continuously at 30 Hz for 18 s.
These tests were carried out 1-2 days before and 12
months after gastroplasty.
Muscle density and cross-sectional area
CT scans were taken at a level which was 12% of the
body height above the lateral knee joint space. All scans
were performed on a Phillips Tomoscan 310 with a
scanning time of 4.8 s and a slice thickness of 9 mm.
CT pictures were analysed off-line on a locally
designed interactive system [ 151 to give measurements of
quadriceps and bone radiological density and also the area
of specific tissues. By specifying the Hounsfield unit
number (HU, the unit of radiological density) midway
between the structure and its surroundings, the computer
would then search in a given area for that density value
and produce a contour. If a clear contour between the
quadriceps and hamstrings could not be seen a tangential
line was drawn between the medial and lateral boundaries of the quadriceps.
The percentage of fat in the muscle was calculated
using the formula described by Jones et al. [16], which
assumes that normal muscle has a density of 60 HU and
fat a density of - 106 HU. Previous studies have shown
the reproducibility of area measurements to be about 4%
and density measurements to be in the order of 5 HU [ 161.
All patients had scans 1 year after surgery. Two
patients also had preoperative scans.
Statistics
The data are presented as means and SD. The results
obtained before and 1 year after surgery were compared
using a paired t-test. Statistical significance was set at
P < 0.05.
RESULTS
Weight loss
The mean body weight before surgery was 138.3 kg (SD
25.2) and 99.7 kg (SD 23.0) 1 year after, giving a mean
weight loss of 38.6 kg (SD 8.6) ( P < 0.001). The body mass
index (BMI, weight/height2) fell from 50.2 (SD 5.7) to 36.1
(SD 6.5) ( P < 0.001).One year after surgery all the patients
were still overweight, having BMI values of greater than
25.
Muscle strength
There were no significant differences in the MVC of
either the adductor pollicis or quadriceps. The values for
Skeletal muscle and weight loss
the adductor pollicis before and after weight loss were
53.9 N (SD11.2) and 54.8 N (SD12.9) respectively. For the
quadriceps the values were 392.7 N (SD92.3) and 385.6 N
(SD92.0).
The maximal tetanic (100 Hz) force of the adductor
pollicis was similarly unaffected by the weight loss. This
was 47.2 N (SD 9.2) before surgery and 47.5 N (SD 11.9) 1
year later.
Contractile properties
No significant changes were seen in the force/frequency
relationship, relaxation rate or fatiguability of either
muscle. The data are presented in Table 1.
Muscle density
The quadriceps density 1 year after surgery was 43.7
HU (SD 14.7). This was significantly lower ( P < O . O O l ,
Student’s t-test) than the normal values of 60.3 HU (SD
4.0) [21], indicating an excess amount of fat (density of
- 106 HU) within the muscle.
One year after gastroplasty the patients had a mean fat
content of 10.8% (range 3.0-30.1%) in the quadriceps.
This is significantly greater ( P < 0.025) than the fat
content of 1.6% (range 0-5%) in the quadriceps of nonobese individuals [ 161.
The density of the quadriceps in the two patients who
had preoperative scans was 39 and 48.6 HU (12.6 and
6.9% fat), and 1 year later this had increased to 55 HU
(3.0% fat) in both cases. Fig. 1 shows the scans of one of
these patients and it can be seen that there was a decrease
in the area of both the subcutaneous fat and the muscle
compartment. The quadriceps cross-sectional area fell
from 75.6 to 66.3 cm2 and the density increased from
48.6 HU (6.9% fat) to 55 HU (3.0% fat). The crosssectional area of the muscle of the other patient decreased
from 91.7 cm2 to 83.9 cmz. The strength of the quadriceps muscle was unchanged (290 and 284 N in one case
and 376 N and 390 N in the other), indicating that the
decreased area within the muscle envelope was not due to
loss of contractile material.
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DISCUSSION
This study has shown that the considerable weight loss
that takes place in obese subjects after gastroplasty does
not change either the strength or contractile properties of
a distal and proximal skeletal muscle. CT measurements
of the quadriceps muscle showed a marked increase in the
radiological density and a reduction in size. However, the
muscle strength was unchanged, indicating that intramuscular fat had been mobilized with no loss of contractile tissue.
The relationship between the contractile properties of
skeletal muscle and nutritional status is an area which is
currently the subject of considerable activity and interest.
In 1982, Lopes et al. [5] reported that the adductor pollicis muscle of malnourished individuals had abnormal
contractile properties, and that the abnormalities were
rapidly reversed by 4 weeks of parenteral nutrition. Of
more relevance to the results presented here was a subsequent paper, in which the same abnormalities were
induced in obese individuals by 2 weeks on a hypocaloric
diet (1674 J/day) and reversed by oral refeeding [ 111. As
no change was detected by the conventional techniques of
nutritional assessment, the authors hypothesized that tests
of muscle contractility were more sensitive to changes in
nutritional status than other available techniques. Subsequent work has shown that clinically malnourished
patients do have abnormal contractile properties [5, 6, 8,
9, 121, but the claim that these techniques ate sensitive to
small changes in nutrition status which are undetectable
by conventional assessment has not been supported by
further work. Using techniques identical to those of
Jeejeebhoy and co-workers [5, 121, other workers [7, 8,
211 were not able to reproduce the results of this group on
the effects of dietary restriction. The individuals studied
in the work reported here were still obese a year after
gastroplasty, but might still have been malnourished due
to the prolonged restricted energy intake. However,
despite the considerable changes that had occurred in
their nutritional status, their skeletal muscle contractility
and strength was unchanged.
The combined effects of reduced body weight and
unchanged force act to increase the strength/weight ratio,
Table 1. Contractile properties of the adductor pollicis and quadriceps before and 1 year after gastroplasty
For the force/frequency data, the force generated by stimulation at each frequency is expressed as a percentage of that at
100 Hz. The MRR values show the percentage of force loss in 10 ms. Fatiguability values refer to the force loss (percentage of initial) for the quadriceps after 18 s stimulation and for the adductor pollicis at 1 min intervals during 3 min of
intermittent stimulation. Results are shown as means k SD.
Force/frequency
Quadriceps
Beforesurgery
1 year after
Adductor pollicis
Beforesurgery
1 year after
1/100%
10/100%
20/100%
50/100%
MRR
Fatiguability
30.3f13.1
26.5f7.0
52.3f11.5
51.5f10.6
81.2f4.5
81.0f2.3
96.9f1.0
95.4f2.4
10.8f1.5
11.3f1.2
19.3f3.6
17.2f3.0
12.9f2.5
12.8f3.3
36.8f7.5
32.7f12.2
77.2f5.4
67.9f9.2
94.4f6.4
92.4f3.6
11.4f1.8
10.5f1.3
1 min
2 min
3 min
17.1f7.0
15.8f2.9
25.8f5.7
29.0f9.6
32.0f7.9
38.8f13.9
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D. J. Newham et al.
Fig. 1. CT scans of one patient before ( a ) and 1 year after ( b )gastroplasty. The cross-sectional
area of both subcutaneous fat and the quadriceps muscle decreased. However, the muscle density
increased and strength remained constant, indicating that fat rather than muscle had been lost.
which presumably contributes to the improved functional
ability which was reported by all the patients. The predicted normal values for the quadriceps MVC in nonobese subjects are related to the body weight [17]. The
initial MVC values were 49% (SD 16.3) of the lower limit
of normal (mean minus 2 s ~and
) after 1 year's weight loss
had improved to 73% (SD 28.9). It is interesting that, in
adults, an increase in body weight does not seem to be
accompanied by the increase in strength that occurs in
growing children [22]. The differences in the relationship
between muscle strength and body weight in normal
subjects and the obese patients is emphasized when the
predicted strength is calculated for the ideal body weight
according to height [23]. When this is done (Fig. 2) the
obese patients no longer appear weak and are all within
the normal range. An increase in body weight might be
expected to act as a stimulus for hypertrophy of the
weight-bearing muscles by being a form of 'internal'
weight training. However, the absence of strength changes
coincidental to weight changes shows that this is not the
case and presumably reflects the more sedentary life style
that accompanies progressive obesity.
These results are compatible with those of a previous
study which investigated the effect of dietary restriction
on two obese young boys (age 12 and 15 years) using
metabolic nitrogen balance, urinary creatinine, body
composition (water and potassium) and strength measurement techniques [24].The boys, lost 38 and 17 kg over 11
and 6 weeks respectively, yet there was no indication of
any loss of lean body mass.
The amount of fat remaining in the quadriceps after 1
year's weight loss was considerable: 10.8% compared
with 1.6% in normal non-obese quadriceps [16,25]. This
is a reflection of the fact that the subjects were still obese,
as shown by the BMI. The fat content of the muscles,
particularly before surgery, was remarkably large, but our
values, based on CT data, are comparable with those of
Lennmarken et al. [26], which were taken from biopsy
samples of the quadriceps of obese women. The period of
weight reduction caused a large loss of muscle stored fat
550
-
0
-z 500
Y
M
&
450,
0
400'
0
0
350'
6
300
250
40
60
80
100
120
140
160
180
Body weight (kg)
-
Fig. 2. The quadriceps MVC values of the patients related
to actual (0)and ideal (+) body weight. The normal range
for the MVC related to body weight is from Edwards et al.
[17]. When strength is related to actual body weight the
obese patients fall below the normal range, but have a
normal strength for their ideal body weight.
in the obese patients, and so it would seem that this fat is
lost along with that stored subcutaneously.
These results show that obese individuals can lose large
amounts of weight in a relatively short period of time
without compromising either their muscle strength or
function. They do not support the contention that tests of
muscle contractility are sensitive to changes in nutritional
status in individuals who are not grossly malnourished.
ACKNOWLEDGMENTS
We thank Mrs B. Rook Ley for typing the manuscript, and
the North East Thames Regional Health Authority for
financial support.
Skeletal muscle and weight loss
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