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Physical training in human obesity. III. Effects of long-term physical training on body composition
Physical Training in Human Obesity. III. Effects of Long-term Physical Training on Body Composition Per Bjtirntorp,
Kristina
de Jounge,
Lars Eight
severely
obese patients
tissue
hypercellularity,
mass,
and a juvenile
subjected without
dietary
program times ule
was
5 beats
5-min Body
fat showed
cell
decreased
after
ing blood
glucose
were
6 mo plasma
6 mo
creased.
three
a fixed
sched-
sults
ability
decrease
below of body
maximal each cell
no significant
or 6 mo of training.
working
the heart
Fasting
rate
during
training mass,
three session.
and
changes plasma
insulin
insulin
suggest
might
3
values
tolerance
the
the
the type of severe training
marked
body
without
severe
lack
of
also
The
re-
body
fat
a similar, decrease
period
subjects
studied,
procedure fat
de-
had
training for
obesity
study’
lighter,
values.
long
be characteristic
After
still
triglycerides
to lower
that
after
were
plasma
a trend
but fast-
not changed.
glucose
in a previous
body
after
showed
was
and
improved,
was
Sullivan,
3 mo of training,
Now
The
to the
training
Lars
Stenberg
duration
so that
periods weight,
during
Krotkiewski,
35-min
individualized
10-l
training
and followed
of each subject,
adipose body
of obesity
Marcin
and Jesper
restrictions. of
weekly
with
elevated onset
to physical
Si&trijm,
with
because although
produced in
a
patients
obesity.
S
TUDIES IN THE RAT shovv that physical training is followed by a body, weight decrease.’ Prolonged light exercise causes a slower gain in body, weight in growing rats. Apparently this is solely due to an increased caloric expenditure, because food intake is not decreased.j Shorter periods of heavier exercise, on the other hand, cause an increase in caloric expenditure as well as a decreased food intake, resulting also in a slower weight gain than in freely eating sedentary controls.3.4 Old fat rats lose weight after rather strenuous exercise, and the weight lost is mainly fat.’ In man physical training of young athletes causes a decrease in skin fold thickness in spite of an elevated intake of calories during the training periods.h Physical activity in man thus also seems to balance caloric intake so that a weight decrease occurs. These regulatory mechanisms are apparently working
Metabolism,
Vol
22,
No.
12 (December),
1973
1467
BJORNTORP
1468
ET Al.
not only in young subjects but also at higher ages than those where athletic activities are frequent.‘,7.8.9.‘0 Obese subjects also decrease in body fat when exercise is added to a controlled caloric intake.” However, in severely obese patients who were told not to restrict their diet during a rather strenuous physical training program lasting for 8 wk, there is no decrease but rather a slight increase in body fat.‘? This was surprising in view of the evidence that physical training causes a decrease in fat both in the normal and fat experimental animally’ as well as in young’*6 and middle-aged athletes, 9 in middle-aged sedentary men,‘,’ and in patients who have suffered a myocardial infarction, some of whom were slightly obese.” Therefore, the study referred tol2 was repeated and extended as will be reported in the present work. The group of severely obese subjects was selected to include only patients with a rather circumscribed obesity syndrome characterized by a hypercellular adipose tissue, an elevated body cell mass, and a juvenile onset of obesity. I3 Furthermore, the physical training procedures were rigidly standardized and prolonged in duration and followed a schedule previously applied on a group of middle-aged men who had suffered a myocardial infarction,” where it was found to effectively reduce body fat. MATERIALS I I severely obese patients
Originally continue
after
working
capacity
respectively. (30-47 work
a few weeks because
yr old). time
in comparison
Of the remaining Before
mass was above geographical
mean
region,
In seven patients histories.
against through
plus
All
program. pressure
part
all patients
were instructed any kind
were living
As
not
initial
in the knees.
life both
5 x IO”,
populations
during
and body
“.I4
from
cell
the same
yr) or before could be ascertained
photographs.
in previous
These
per’od. The patients were preselected
and pain
a sedentary
above
selected control
school, and/or
diet with
training,
too low
body cell mass was above mean plus 2 SDS of the controls.
not to change the’r
of reducing
the physical
exercise.
(21 37 yr old) and three were men
had a fat cell number
an onset of obesity at school age (7-14 was less certain.
but three of them could
during
of the group.
five were women
of randomly
In five patients
blood
the remaining
period
I SD
weight records during
documentation patients
with
leisure time.
METHODS
began the training
of elevated
eight patients
the training
and during
AND
investigations
dietary
habits
the justification
instructions
while
in the remaining from
this
that
they would
the
laboratory’2.‘5
but to eat freely.
were repeated
from
patient
They
not
occasionally
the
were advised
be able
dur’ng
to carry
the training
to ensure the best possible cooperation.
Plz?tsical Training The group was trained as in the preceding
in a gymnasium
reports. 12,15 The
the program.
The design for the training
had suffered
a myocardial
load was, however,
infarction.
The physical train’ng of rather
tient as described were inserted,
followed
strenuous below,
The exercise
The training
program
capacity,
tinuous ECG
a fixed schedule
exercise
of tixed
also frequently for a group
physically
was finished
with
took
part
of patients
thereafter.
I6 The
in
who work
I).
Each
session lasted for 35 mm and
intensity,
determined
Between
a 5.min
Thereafter
these periods
period
followed
individually
for
two periods
of jogging
and
light
each
three pa-
of jogging gymnastics.
decreased in intensity down to walking.
was standardized and measurements
in Douglas
(Fig.
and light gymnastics.
for 5 min.
for each subject in relation
which was first determined
recording
air was collected
and who were trained
(KdJ)
of the same physiotherapist
of this report
was the same as described
up with jogging
each lasting
and the exercise was gradually working
authors
higher in the present patients.
started with 5 min of warming periods
under the leadership
other
by a work
of oxygen consumption
bags snd the ~01~1111:mrosurrd
to the individual
test on a bicycle during
ergometer
maximal
in :I dry gasmeter.
Ga\
work.
maximal with conExpired
samples vvcre
PHYSICAL TRAINING
IN HUMAN
1469
OBESITY
Work
load
lkpmhnl
1.
Fig. the
Schedule
physical
sions.
over
training
For details
ses-
see text.
5
analysed with a micro-Scholander available
analysis
were regarded as an indication A work
method
kit (Boehringer,
and blood
Mannheim.
of maximal
step of 29 cm height,
primarily
men 1200 kpm/min day, Wednesday.
enzymatically
35 Time IMinutes)
with
a commerclall!,
Concentrations
above
rate
IO- 15 beats/mm
on the ergometer
and the work
below
the maximal
bicycle or by climbing
and Friday
:t
session these pulse rates were checked
load corrected
as a rule 900 kpm/min.
at 5 p.m. for 6 mo. The patients
part in at least 70 of the 75 training
heart
up and do-n
upwards
when needed to obtain
The initial worh load during the 5-min periods of fixed work
and for the women
8 mhl
effort.
at a given pace. At each training
after 3 min on the load in question. the desired heart rate.
lactate
30
25
20
West Germany).
load was selected which gave a heart
rate. This work was performed
15
10
This program included
was for the
was repeated
Mon-
in the present report took
sessions.
After 3 and 6 mo of training the work test was repeated.
Determination
of Body Composition,
Plasma Metubolites.
Before and after 3 and 6 mo of physical training ing body weight,
total exchangeable
potassium.
mass and total body fat could be calculated adipose
tissue biopsies ”
were
performed.
and
and femoral
regions were determined
obtained
by dividing
total
body
fat
with
body composition
and total the
from
mean
fat
cell
sizes of
method.*’
fat cell weight
by meahur-
which
by Berg and Isaksson.”
by a microscopic
an average
was determlned
body water ““*
as described
dominal,
and Insulin body cell
Percutaneous
the
glutral,
ab-
Fat cell number
calculated
from
the
WB~ mean
fat cell weights of the three regions examined. .4 peroral
glucose tolerance
Patients were fasting
test was performed
overnight
before
and did not smoke.
After
training
and after
the training
formed on the fourth and on the seventh day after the last training
6 mo of tralnlng.
period
the test \*a:, per-
session. One hundred
pram,
ot
glucose were ingested dissolved in 200 ml water. Venous blood samples were tahen into hrparinilcd test tubes for determination and 120 min after Here determined Plasma
drinking also after
trlglycerides24
and
of blood
Statistical
traming
and
plasma
inaulin13
Fasting
blood
3 mo of training,
alloumg
cholesterol”
determlned
and serum uric acid26 before training loads after patient.
glucose”
of the glucose solution. were
4 days from in all
before, the
fastmg
30,
last training blood
and after 6 mu. One subject was infected
were to be performed,
and
glucose and plasma
and these tests therefore
samples
60,
90,
ln\;ulln bessmn. tshen.
when the glucose
had to be deleted
in rhih
method used was Student’s t test.
RESULTS
Table I shows the results mo after physical training. usually decreased. Maximal
of the individual work tests before, and at 3 and 6 The heart rate at a given submaximal work load oxygen consumption increased in all patients.
BJORNTORP
1470
Table
1.
Results
Physical
of Work
Training
Tests
in Eight
Before
and
Severely
Maximal Oxygen Consumption (literlmin)
Subjects
Sex
Before Training
HF
W
2.3
3 and
Obese
6 MO After Subjects
Heart Rote on Submaximal Work Loads (beats/min)
After 3 MO of Training
After 6 MO of Training
Work Load (kpm/min)
Before Training
3.5
2.5
600
171
After 6 MO. of Training 158
900 W
ML GP
2.4
2.8
3.1
178
600
123
119
900
144
136
600
152
152
2.7
2.8
W
171
900 BR
W
2.4
W
MP
2.8
1.9
2.9
2.3
2.2
ET AL.
600
145
132
900
163
152
600
169
138
600
137
117
900
170
143
600
130
105
900
160
129
600
140
159
900 M
TH KJ
2.8
M
3.3
M
SK
2.7
3.3
3.8
4.0
3.0
3.5
900 Mean
z&zSD*
Mean
difference
2.5
+ 0.5
3.0
0.45
% 0.6
i
3.0
0.42
0.43
f
168
0.6
+ 0.18
vs. before troininq *Calculated
i
SD
p < 0.001
p < 0.05
on subjects with complete
data
(n, 6).
Body weight did not change significantly after 6 mo on this training program (Table 2). The average values for body cell mass increased at 3 and 6 mo, while the average values for body fat decreased at 6 mo. None of these changes were, however, statistically significant. Fasting plasma insulin was lower at both 3 and 6 mo after training, while fasting blood glucose was lower only at 6 mo. Body
fat
(kg) + 60
HF RPp SK
40
I
Before
3months
> Bmonths
Fig. training
2.
Body in eight
fat
before
severely
and obese
after
3 ond
subjects.
6 mo
of
physical
training
PHYSICAL
TRAINING
IN
HUMAN
1471
OBESITY
Blood glucose (mg/lOOml~
7 days h days Fig. and
3.
after
test 7
days
physical Means
insulin
a peroral
erance and
Blood
plasma
values
glucose
tol-
performed after
training f
glucose
the
4
I : :
lost
session.
0
SW.
30
60
I 90
:> 120 Minutes
The sum of insulin and the sum of glucose values during glucose tolerance test were both significantly lower after 6 mo than before, and plasma triglycerides tended to be somewhat lower. Cholesterol and uric acid did not change. Figure 2 gives the individual body fat values for the obese patients. As compared with values before training all patients had less body fat after 6 mo of training except MP and SK whose body fat increased. The decrease was most pronounced between 3 and 6 mo in patients HF. ML, and TH. Figure 3 shows the results of glucose and insulin determinations during the glucose tolerance tests on the fourth and seventh day after the last training session. The blood glucose value at 30 min was lower on the fourth day than on the seventh day (p < 0.05). Otherwise no differences could be shown. Plasma triglyceride and cholesterol values were not different 4 and 7 days after the last exercise. DISCUSSION
After uninterrupted acute work of long duration performed by hyperinssulinemic obese subjects, insulin levels are frequently lowered during the Iirst few days afterwards but not after 5-6 days.27 In the present work the repeated glucose tolerance tests after the last training session indicate that, already on the fourth day, acute training effects on the insulin values were no longer detectable, because the insulin values were not different on the fourth and seventh day after the last exercise. In comparison with nonobese subjects of the same age and sex2’ the present obese subjects usually showed an increased maximal oxygen consumption (liter/min) before training as reported previously for severely obese subjects.” After training, this consumption increased further and reached values which are above those obtained in a material of well-trained, middle-aged men.’ When expressed per kilogram of body cell mass the maximal oxygen consumption before training (77 ml O2 x min ’ x kg-‘) is close to the corresponding value for randomly selected, mainly sedentary middle-aged men from the same region (71 ml O2 x min ’ x kg ‘; maximal oxygen consumption: 2.3 liter/min.” body cell mass 31 kg”). It is therefore reasonable to believe that the elevation of
3 mo
training
6 mo
of paired
1
7
fVolues
tn.
‘Glucose
p (diff
test.
~
8
8
8
8
O+ 4 days after
tolerance
diff. * S,, (before-6 mo)
Means
tralning
After
training
After
Before
n
10
9
“.S.
lr5
*
+ 9
*
lost training
113
112
112
i
f
8
5
7
session.
n.s.
w
t 9
9
Fat
rublect
-3+5
39 i
42
42 i
(kg)
Body
of Physical
Infected
rl.5.
216
36 *
36
34
(kg)
Cell Mass
(kg)
Weight
Effects
Body
2.
Body
Table
l
~6
excluded.
* 001
--12
6 *
12 i
18
(pU/ml)
Insulin
37
3
7
GTT*
-161
1301
i- 100
i
L 221
i 0.01
259
420
(flu/ml)
During
Values
of
PlCI~flICl
Sum
Patients
lnsulln
of Obese
Fasting
Training
t
7f
0.05
72
560
in 85
*
- 84 f
448
532
and
GTT‘
(mg/lOOml)
During
Valuer
GIUCOX
Sum of
Composition
8
9
c 0.001
-8zt3
68
75
76 *
(mg/lOOmll
GlUCC%
Blood
Fost,ng
on Body
i
0.26
f
0.53
0 47
0.42
+ 0.53:
J 0.10
1.14
16 2 *
1.45
(mW
Triglyceride
Plasm0
Metabolic
36 i 47T
I
*
“.S.
18 zk27
244
218
226
43
Cholesterol (mg/lOO
ml)
(beans
Plasma
Variables
-0
1
n.r
i
5 9 i
6.0
ml)
1.6
0.7
+ 2.0
Acid
Uric
SD)
(mg/lOO
k
0.7
Fat
-
-
= cl.2
k9)
Sire
Cell
e
1.1
lO_‘O)
Number
6.0
(x
Fat Cell
PHYSICAL
TRAINING
maximal
oxygen
in
tissue
IN HUMAN
these
body cell mass than adipose
consumption
obese
is associated
subjects
is probably
with
training
increase
in
mean body fat, none of which decreased
It would
of course
the training
program
large
mass
cell
mass.
This
cellularity
the body
body
cell
also
of
respiring
elevation
in other
01
tissues
not able to work
with
healthy,
However,
IX.6
subjects
procedure
body
This
decrease
in
subjects
no
fat was constant
I.5
kg to i 1.6 i
I.5
time-consum-
These
with
weight
kg (p <: 0.01)
on
men were
healthy
in body
judged
to that applied
infarction.“,”
decreased
following
however.
to such a long.
obese subjects
infarction
group
It was,
was identical
a myocardial
as the present +
some
to have a nonobese
nonobese
had suffered
and yet the men with from
while
the obese subjects.
the training
as hard
was constant.
and a slight
subjects.
parallel
However,
weight
mass
significant.
have been desirable
of men who
was reduced
period
mean
were fully
in other
to motivate
ing procedure.
system
the
in body fat after 6 mo of training,
or had even increased
a group
with body
tissue.30
was due to a slight
impossible
elevated
due to an increased
In spite of the long-term
doubt
1473
OBESITY
circulatory and body
after
fat
3 6 mo of
training.’ Si_cniticant men
after
diminution physical
Furthermore, a 16-wk which
of body
training
middle-aged
training
period
Although
dietary
cardial
can of course
infarction
diflerent. regular,
that
It
rather
The
strenuous
initial
Evidence exercise Marc
from
does
not
physical
training
strenuous
work.
ture.
a decreased
type
of exercise
rat experiments. ing sessions ments.
The
crcising slower
on
a lower
juvenile
that
load
with
obesity
onset
hyperplastic
obese
cause
suggests
for
of a
the myosomewhat
program
d more
that
for
marked
directly
de-
in body
elevated
the
this
work
fat.
patients
with
the
Oscai that
in that
and Williams” it
is
elevated
in body primarily body
case.
esThe
obese subjects
infarction
None
experi-
infarction
appettte
myocardial
The in the
of the trsin-
in the rat
indeed
on their
obese men decreased possible
loads
myocardial was
expendi-
to that
fat in the severely
body
patients.
caloric
is performed.’
work
with
light
consumption,
comparable
strenuous
that
long-lasting.
caloric
to increased
that the hard
among
seems
or
pro-
sort
were also
increases
effect of exercise
moderately
some
controlled
the day the exercise
suggests
as the present
It therefore
the not
in the patients
moderately
middle-aged
training.
likely
that
sessions
of the training taking
the obese,
in addition is not
decrease
pronounced
be emphasized
a severe
physical
work
thus only
to the more
decrease
pronounced a less
there were some shown
rather
correspond
clear weight
It should
work
of the training
obese subjects.
at least during
in the present
kg during
instructions
did
but
gives,
for
that
animal
appetite.
but it seems
and less
severely
however,
appetite
should
then indicates
such
influence
4.5
the course
dietary
surprising
the experimental
walking.’
decreased
consciously
either
event
crease in body fat in the present
or
work.3’
during were
sedentary
running7
and frequency
be excluded
at any
in middle-aged of
obesity
of the present
histories
patients.”
seems
moderate
the patients
not
found
consisting
an intensity
to those
ordinary
gram did not reveal diet, this
men with
with
seem comparable
fat was also
programs
regulation. patients”’ group
had
have also weight the
cell mass”
after
severe. who
1474
BJijRNTORP
ET At
are characterized by a failure to decrease in weight after physical training. It seems quite likely that this kind of obese subject is particularly difficult to treat successfully also with dietary means.32,33 a As described previously ‘2~‘5fasting plasma insulin was lowered without significant decrease of body fat after 3 mo of training. Fasting blood glucose was not changed at that time. After 6 mo of training plasma insulin values were again decreased, and at this time glucose tolerance had increased. The improved glucose tolerance may indicate a primary effect of physical training on glucose removal mechanisms rather than on insulin secretion. It cannot be excluded that such mechanisms have played a role in previous reports’2l’5 in individual patients but that they have not been detectable as statistically significant changes after the shorter periods of training. The improved glucose tolerance may alternatively be due to the body fat decrease34 seen in some of the patients after 6 mo of training. REFERENCES I. Bjijrntorp Sjostriim
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Buskirk
striction
Beaton JR: Bouts of exercise and food intake
composttton:
Effects
JJ.
1954
JO, Shank
L:
P, Berchtold
B. Sanne H. Tibblin
tolerance.
FJ:
Exercise food intake and body wetght in normal 117:544.
Lindholm
body composition
Mashayekhi
rats and genetically
IO. Bjiirntorp
L.
L: Adipose
cortisone
and
subjects. Acta
long-
anabolic
Endocrinol
1967 lsaksson of school
palsy. Acta Paediatr
B: Body children
composition with
cerebral
Stand (Suppl) 204:41,
I970
PHYSICAL
TRAINING
20. Hirsch
IN HUMAN
J. Goldrick
the metabolism Lipogenesis
RB:
of human
and
free
Serial
studies
on
tissue.
I.
adipose
fatty
1475
OBESITY
acid
uptake
and
release in small aspirated samples of subcutaneous fat. J Clan Invest 43: 1776. 1964 71. Sjiistriim
L,
Bjarntorp
P. Vrana J:
in comparison
matic determinations J Lipld
Mi-
on frorenwith
of osmium-fixed
72. Lcvln
K,
auto-
Linde S: Determination
of glu-
tluid and urine with
a new gluc~w oxidase reagent. J Swedish Assoc SY:iOlh,
Med
I962
23. Hales C‘N, Randle insulin
with insulin
PJ: Immunoassay
antibody precipitate.
of
Lancet
1:200. 1963 21. Carlson
LA:
Determination
of
glycerides. Acta Sot Med Ups 64:20X. 7i.
C rambr K.
the ‘Theorell
Isukcwn
I I-213, 20.
strum
lY5Y
B. An e\:iluatlon
of
method for the determmcition
of
total serum cholesterol
Sand
J Clin
Lab Invest
Praetorlus
photometry.
E: Enzymatic
method
of uric acid by ultraviolet Sand
J Clin
Lab
for despcctrO-
Invest
I:212.
27.
FahlPn
M,
secretion
Diahetologla
Stenberg in
obesity
X:131. IY72
J.
(suppl) 49: 169. 1960 G.
Bjiirntorp after
P:
exercise.
Wilhelmsen
M, Bjure
L.
tkstriim-
J. Tibblln
G
Aerohlc
power and related factors in a population of men aged 54. Sand
\tudk
J Clin Lab Inveqt 26.2~7.
1970 30. Naeve RL.
Roode P: The specs and nurn-
bers of cells in vIsceraI organs In human ohaIr>. Am J Clin Pathol 54:251, 31. Oscai LB, on
Williams
over-weight
Gerlatr
Sot 4.
Krotkieubki
lY70. BT:
16:794.
P. S.jiistriim
I-ahlGn M.
male<.
M.
Larsson
L.
hral
1971
33.
Bjiirntorp
B.
Nutritionists 34. kalkhoff‘
RK.
J.
Somlodrr
Med. (Praxi\)
and weight rcduclns
of the Group
Diets.
I_.
Vrana
at SaltsjGbaden.
1971. Bibl Nutr
t’.
Sulli\:ln
und Behandlung
P: O&sit)
Meeting
,2m
Berchtold
J.
SchweiL Rundschau.
60:69X.
J
1068
Sziics L, Enzi G. Diqnose Adipositas.
EH‘ect 111’excrc~w
middle-aged
37. Bjiirntorp Jvnbwn
Ferron
I Y4Y Insulin
Sand
79. Grimby
regimen.
195’)
termlnatlon
Physiol
fat cells.
Res 11:521, I971
case In blood. cerebrospinal
I: Aerobic work capacity in men
Jodal B Aurell
croscopic fat cell size measurements cut adipose tissue
28. Astrand
and women with special reference to :~ge. ,Acta
of
Eur~>pcan
Sweden.
June
vol. 19, IY73 Kim
HJ.
Cerlrttk
J.
C.4: Metabolic effects of weight lo\\ 111
obese subjects. levels. insulin
Changes and growth
Diabetes 20,X?. 1971
In
plasma
hormone
sub\tratc responw,
Kristina
de Jounge,
Lars Eight
severely
obese patients
tissue
hypercellularity,
mass,
and a juvenile
subjected without
dietary
program times ule
was
5 beats
5-min Body
fat showed
cell
decreased
after
ing blood
glucose
were
6 mo plasma
6 mo
creased.
three
a fixed
sched-
sults
ability
decrease
below of body
maximal each cell
no significant
or 6 mo of training.
working
the heart
Fasting
rate
during
training mass,
three session.
and
changes plasma
insulin
insulin
suggest
might
3
values
tolerance
the
the
the type of severe training
marked
body
without
severe
lack
of
also
The
re-
body
fat
a similar, decrease
period
subjects
studied,
procedure fat
de-
had
training for
obesity
study’
lighter,
values.
long
be characteristic
After
still
triglycerides
to lower
that
after
were
plasma
a trend
but fast-
not changed.
glucose
in a previous
body
after
showed
was
and
improved,
was
Sullivan,
3 mo of training,
Now
The
to the
training
Lars
Stenberg
duration
so that
periods weight,
during
Krotkiewski,
35-min
individualized
10-l
training
and followed
of each subject,
adipose body
of obesity
Marcin
and Jesper
restrictions. of
weekly
with
elevated onset
to physical
Si&trijm,
with
because although
produced in
a
patients
obesity.
S
TUDIES IN THE RAT shovv that physical training is followed by a body, weight decrease.’ Prolonged light exercise causes a slower gain in body, weight in growing rats. Apparently this is solely due to an increased caloric expenditure, because food intake is not decreased.j Shorter periods of heavier exercise, on the other hand, cause an increase in caloric expenditure as well as a decreased food intake, resulting also in a slower weight gain than in freely eating sedentary controls.3.4 Old fat rats lose weight after rather strenuous exercise, and the weight lost is mainly fat.’ In man physical training of young athletes causes a decrease in skin fold thickness in spite of an elevated intake of calories during the training periods.h Physical activity in man thus also seems to balance caloric intake so that a weight decrease occurs. These regulatory mechanisms are apparently working
Metabolism,
Vol
22,
No.
12 (December),
1973
1467
BJORNTORP
1468
ET Al.
not only in young subjects but also at higher ages than those where athletic activities are frequent.‘,7.8.9.‘0 Obese subjects also decrease in body fat when exercise is added to a controlled caloric intake.” However, in severely obese patients who were told not to restrict their diet during a rather strenuous physical training program lasting for 8 wk, there is no decrease but rather a slight increase in body fat.‘? This was surprising in view of the evidence that physical training causes a decrease in fat both in the normal and fat experimental animally’ as well as in young’*6 and middle-aged athletes, 9 in middle-aged sedentary men,‘,’ and in patients who have suffered a myocardial infarction, some of whom were slightly obese.” Therefore, the study referred tol2 was repeated and extended as will be reported in the present work. The group of severely obese subjects was selected to include only patients with a rather circumscribed obesity syndrome characterized by a hypercellular adipose tissue, an elevated body cell mass, and a juvenile onset of obesity. I3 Furthermore, the physical training procedures were rigidly standardized and prolonged in duration and followed a schedule previously applied on a group of middle-aged men who had suffered a myocardial infarction,” where it was found to effectively reduce body fat. MATERIALS I I severely obese patients
Originally continue
after
working
capacity
respectively. (30-47 work
a few weeks because
yr old). time
in comparison
Of the remaining Before
mass was above geographical
mean
region,
In seven patients histories.
against through
plus
All
program. pressure
part
all patients
were instructed any kind
were living
As
not
initial
in the knees.
life both
5 x IO”,
populations
during
and body
“.I4
from
cell
the same
yr) or before could be ascertained
photographs.
in previous
These
per’od. The patients were preselected
and pain
a sedentary
above
selected control
school, and/or
diet with
training,
too low
body cell mass was above mean plus 2 SDS of the controls.
not to change the’r
of reducing
the physical
exercise.
(21 37 yr old) and three were men
had a fat cell number
an onset of obesity at school age (7-14 was less certain.
but three of them could
during
of the group.
five were women
of randomly
In five patients
blood
the remaining
period
I SD
weight records during
documentation patients
with
leisure time.
METHODS
began the training
of elevated
eight patients
the training
and during
AND
investigations
dietary
habits
the justification
instructions
while
in the remaining from
this
that
they would
the
laboratory’2.‘5
but to eat freely.
were repeated
from
patient
They
not
occasionally
the
were advised
be able
dur’ng
to carry
the training
to ensure the best possible cooperation.
Plz?tsical Training The group was trained as in the preceding
in a gymnasium
reports. 12,15 The
the program.
The design for the training
had suffered
a myocardial
load was, however,
infarction.
The physical train’ng of rather
tient as described were inserted,
followed
strenuous below,
The exercise
The training
program
capacity,
tinuous ECG
a fixed schedule
exercise
of tixed
also frequently for a group
physically
was finished
with
took
part
of patients
thereafter.
I6 The
in
who work
I).
Each
session lasted for 35 mm and
intensity,
determined
Between
a 5.min
Thereafter
these periods
period
followed
individually
for
two periods
of jogging
and
light
each
three pa-
of jogging gymnastics.
decreased in intensity down to walking.
was standardized and measurements
in Douglas
(Fig.
and light gymnastics.
for 5 min.
for each subject in relation
which was first determined
recording
air was collected
and who were trained
(KdJ)
of the same physiotherapist
of this report
was the same as described
up with jogging
each lasting
and the exercise was gradually working
authors
higher in the present patients.
started with 5 min of warming periods
under the leadership
other
by a work
of oxygen consumption
bags snd the ~01~1111:mrosurrd
to the individual
test on a bicycle during
ergometer
maximal
in :I dry gasmeter.
Ga\
work.
maximal with conExpired
samples vvcre
PHYSICAL TRAINING
IN HUMAN
1469
OBESITY
Work
load
lkpmhnl
1.
Fig. the
Schedule
physical
sions.
over
training
For details
ses-
see text.
5
analysed with a micro-Scholander available
analysis
were regarded as an indication A work
method
kit (Boehringer,
and blood
Mannheim.
of maximal
step of 29 cm height,
primarily
men 1200 kpm/min day, Wednesday.
enzymatically
35 Time IMinutes)
with
a commerclall!,
Concentrations
above
rate
IO- 15 beats/mm
on the ergometer
and the work
below
the maximal
bicycle or by climbing
and Friday
:t
session these pulse rates were checked
load corrected
as a rule 900 kpm/min.
at 5 p.m. for 6 mo. The patients
part in at least 70 of the 75 training
heart
up and do-n
upwards
when needed to obtain
The initial worh load during the 5-min periods of fixed work
and for the women
8 mhl
effort.
at a given pace. At each training
after 3 min on the load in question. the desired heart rate.
lactate
30
25
20
West Germany).
load was selected which gave a heart
rate. This work was performed
15
10
This program included
was for the
was repeated
Mon-
in the present report took
sessions.
After 3 and 6 mo of training the work test was repeated.
Determination
of Body Composition,
Plasma Metubolites.
Before and after 3 and 6 mo of physical training ing body weight,
total exchangeable
potassium.
mass and total body fat could be calculated adipose
tissue biopsies ”
were
performed.
and
and femoral
regions were determined
obtained
by dividing
total
body
fat
with
body composition
and total the
from
mean
fat
cell
sizes of
method.*’
fat cell weight
by meahur-
which
by Berg and Isaksson.”
by a microscopic
an average
was determlned
body water ““*
as described
dominal,
and Insulin body cell
Percutaneous
the
glutral,
ab-
Fat cell number
calculated
from
the
WB~ mean
fat cell weights of the three regions examined. .4 peroral
glucose tolerance
Patients were fasting
test was performed
overnight
before
and did not smoke.
After
training
and after
the training
formed on the fourth and on the seventh day after the last training
6 mo of tralnlng.
period
the test \*a:, per-
session. One hundred
pram,
ot
glucose were ingested dissolved in 200 ml water. Venous blood samples were tahen into hrparinilcd test tubes for determination and 120 min after Here determined Plasma
drinking also after
trlglycerides24
and
of blood
Statistical
traming
and
plasma
inaulin13
Fasting
blood
3 mo of training,
alloumg
cholesterol”
determlned
and serum uric acid26 before training loads after patient.
glucose”
of the glucose solution. were
4 days from in all
before, the
fastmg
30,
last training blood
and after 6 mu. One subject was infected
were to be performed,
and
glucose and plasma
and these tests therefore
samples
60,
90,
ln\;ulln bessmn. tshen.
when the glucose
had to be deleted
in rhih
method used was Student’s t test.
RESULTS
Table I shows the results mo after physical training. usually decreased. Maximal
of the individual work tests before, and at 3 and 6 The heart rate at a given submaximal work load oxygen consumption increased in all patients.
BJORNTORP
1470
Table
1.
Results
Physical
of Work
Training
Tests
in Eight
Before
and
Severely
Maximal Oxygen Consumption (literlmin)
Subjects
Sex
Before Training
HF
W
2.3
3 and
Obese
6 MO After Subjects
Heart Rote on Submaximal Work Loads (beats/min)
After 3 MO of Training
After 6 MO of Training
Work Load (kpm/min)
Before Training
3.5
2.5
600
171
After 6 MO. of Training 158
900 W
ML GP
2.4
2.8
3.1
178
600
123
119
900
144
136
600
152
152
2.7
2.8
W
171
900 BR
W
2.4
W
MP
2.8
1.9
2.9
2.3
2.2
ET AL.
600
145
132
900
163
152
600
169
138
600
137
117
900
170
143
600
130
105
900
160
129
600
140
159
900 M
TH KJ
2.8
M
3.3
M
SK
2.7
3.3
3.8
4.0
3.0
3.5
900 Mean
z&zSD*
Mean
difference
2.5
+ 0.5
3.0
0.45
% 0.6
i
3.0
0.42
0.43
f
168
0.6
+ 0.18
vs. before troininq *Calculated
i
SD
p < 0.001
p < 0.05
on subjects with complete
data
(n, 6).
Body weight did not change significantly after 6 mo on this training program (Table 2). The average values for body cell mass increased at 3 and 6 mo, while the average values for body fat decreased at 6 mo. None of these changes were, however, statistically significant. Fasting plasma insulin was lower at both 3 and 6 mo after training, while fasting blood glucose was lower only at 6 mo. Body
fat
(kg) + 60
HF RPp SK
40
I
Before
3months
> Bmonths
Fig. training
2.
Body in eight
fat
before
severely
and obese
after
3 ond
subjects.
6 mo
of
physical
training
PHYSICAL
TRAINING
IN
HUMAN
1471
OBESITY
Blood glucose (mg/lOOml~
7 days h days Fig. and
3.
after
test 7
days
physical Means
insulin
a peroral
erance and
Blood
plasma
values
glucose
tol-
performed after
training f
glucose
the
4
I : :
lost
session.
0
SW.
30
60
I 90
:> 120 Minutes
The sum of insulin and the sum of glucose values during glucose tolerance test were both significantly lower after 6 mo than before, and plasma triglycerides tended to be somewhat lower. Cholesterol and uric acid did not change. Figure 2 gives the individual body fat values for the obese patients. As compared with values before training all patients had less body fat after 6 mo of training except MP and SK whose body fat increased. The decrease was most pronounced between 3 and 6 mo in patients HF. ML, and TH. Figure 3 shows the results of glucose and insulin determinations during the glucose tolerance tests on the fourth and seventh day after the last training session. The blood glucose value at 30 min was lower on the fourth day than on the seventh day (p < 0.05). Otherwise no differences could be shown. Plasma triglyceride and cholesterol values were not different 4 and 7 days after the last exercise. DISCUSSION
After uninterrupted acute work of long duration performed by hyperinssulinemic obese subjects, insulin levels are frequently lowered during the Iirst few days afterwards but not after 5-6 days.27 In the present work the repeated glucose tolerance tests after the last training session indicate that, already on the fourth day, acute training effects on the insulin values were no longer detectable, because the insulin values were not different on the fourth and seventh day after the last exercise. In comparison with nonobese subjects of the same age and sex2’ the present obese subjects usually showed an increased maximal oxygen consumption (liter/min) before training as reported previously for severely obese subjects.” After training, this consumption increased further and reached values which are above those obtained in a material of well-trained, middle-aged men.’ When expressed per kilogram of body cell mass the maximal oxygen consumption before training (77 ml O2 x min ’ x kg-‘) is close to the corresponding value for randomly selected, mainly sedentary middle-aged men from the same region (71 ml O2 x min ’ x kg ‘; maximal oxygen consumption: 2.3 liter/min.” body cell mass 31 kg”). It is therefore reasonable to believe that the elevation of
3 mo
training
6 mo
of paired
1
7
fVolues
tn.
‘Glucose
p (diff
test.
~
8
8
8
8
O+ 4 days after
tolerance
diff. * S,, (before-6 mo)
Means
tralning
After
training
After
Before
n
10
9
“.S.
lr5
*
+ 9
*
lost training
113
112
112
i
f
8
5
7
session.
n.s.
w
t 9
9
Fat
rublect
-3+5
39 i
42
42 i
(kg)
Body
of Physical
Infected
rl.5.
216
36 *
36
34
(kg)
Cell Mass
(kg)
Weight
Effects
Body
2.
Body
Table
l
~6
excluded.
* 001
--12
6 *
12 i
18
(pU/ml)
Insulin
37
3
7
GTT*
-161
1301
i- 100
i
L 221
i 0.01
259
420
(flu/ml)
During
Values
of
PlCI~flICl
Sum
Patients
lnsulln
of Obese
Fasting
Training
t
7f
0.05
72
560
in 85
*
- 84 f
448
532
and
GTT‘
(mg/lOOml)
During
Valuer
GIUCOX
Sum of
Composition
8
9
c 0.001
-8zt3
68
75
76 *
(mg/lOOmll
GlUCC%
Blood
Fost,ng
on Body
i
0.26
f
0.53
0 47
0.42
+ 0.53:
J 0.10
1.14
16 2 *
1.45
(mW
Triglyceride
Plasm0
Metabolic
36 i 47T
I
*
“.S.
18 zk27
244
218
226
43
Cholesterol (mg/lOO
ml)
(beans
Plasma
Variables
-0
1
n.r
i
5 9 i
6.0
ml)
1.6
0.7
+ 2.0
Acid
Uric
SD)
(mg/lOO
k
0.7
Fat
-
-
= cl.2
k9)
Sire
Cell
e
1.1
lO_‘O)
Number
6.0
(x
Fat Cell
PHYSICAL
TRAINING
maximal
oxygen
in
tissue
IN HUMAN
these
body cell mass than adipose
consumption
obese
is associated
subjects
is probably
with
training
increase
in
mean body fat, none of which decreased
It would
of course
the training
program
large
mass
cell
mass.
This
cellularity
the body
body
cell
also
of
respiring
elevation
in other
01
tissues
not able to work
with
healthy,
However,
IX.6
subjects
procedure
body
This
decrease
in
subjects
no
fat was constant
I.5
kg to i 1.6 i
I.5
time-consum-
These
with
weight
kg (p <: 0.01)
on
men were
healthy
in body
judged
to that applied
infarction.“,”
decreased
following
however.
to such a long.
obese subjects
infarction
group
It was,
was identical
a myocardial
as the present +
some
to have a nonobese
nonobese
had suffered
and yet the men with from
while
the obese subjects.
the training
as hard
was constant.
and a slight
subjects.
parallel
However,
weight
mass
significant.
have been desirable
of men who
was reduced
period
mean
were fully
in other
to motivate
ing procedure.
system
the
in body fat after 6 mo of training,
or had even increased
a group
with body
tissue.30
was due to a slight
impossible
elevated
due to an increased
In spite of the long-term
doubt
1473
OBESITY
circulatory and body
after
fat
3 6 mo of
training.’ Si_cniticant men
after
diminution physical
Furthermore, a 16-wk which
of body
training
middle-aged
training
period
Although
dietary
cardial
can of course
infarction
diflerent. regular,
that
It
rather
The
strenuous
initial
Evidence exercise Marc
from
does
not
physical
training
strenuous
work.
ture.
a decreased
type
of exercise
rat experiments. ing sessions ments.
The
crcising slower
on
a lower
juvenile
that
load
with
obesity
onset
hyperplastic
obese
cause
suggests
for
of a
the myosomewhat
program
d more
that
for
marked
directly
de-
in body
elevated
the
this
work
fat.
patients
with
the
Oscai that
in that
and Williams” it
is
elevated
in body primarily body
case.
esThe
obese subjects
infarction
None
experi-
infarction
appettte
myocardial
The in the
of the trsin-
in the rat
indeed
on their
obese men decreased possible
loads
myocardial was
expendi-
to that
fat in the severely
body
patients.
caloric
is performed.’
work
with
light
consumption,
comparable
strenuous
that
long-lasting.
caloric
to increased
that the hard
among
seems
or
pro-
sort
were also
increases
effect of exercise
moderately
some
controlled
the day the exercise
suggests
as the present
It therefore
the not
in the patients
moderately
middle-aged
training.
likely
that
sessions
of the training taking
the obese,
in addition is not
decrease
pronounced
be emphasized
a severe
physical
work
thus only
to the more
decrease
pronounced a less
there were some shown
rather
correspond
clear weight
It should
work
of the training
obese subjects.
at least during
in the present
kg during
instructions
did
but
gives,
for
that
animal
appetite.
but it seems
and less
severely
however,
appetite
should
then indicates
such
influence
4.5
the course
dietary
surprising
the experimental
walking.’
decreased
consciously
either
event
crease in body fat in the present
or
work.3’
during were
sedentary
running7
and frequency
be excluded
at any
in middle-aged of
obesity
of the present
histories
patients.”
seems
moderate
the patients
not
found
consisting
an intensity
to those
ordinary
gram did not reveal diet, this
men with
with
seem comparable
fat was also
programs
regulation. patients”’ group
had
have also weight the
cell mass”
after
severe. who
1474
BJijRNTORP
ET At
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