Mechanisms o f Ageing and Development, 49 (1989) 147-- 157 Elsevier Scientific Publishers Ireland Ltd.
147
T H E I N F L U E N C E OF H I G H - R E S I S T A N C E T R A I N I N G ON GLUCOSE T O L E R A N C E IN YOUNG AND E L D E R L Y SUBJECTS
B. W. CRAIG*, J. E V E R H A R T * * and R. BROWN*** Human Performance Laboratory, Ball State University, Muncie, I N 47306 (U.S.A.) (Received October 10th, 1988) (Revision received February 2nd, 1989)
SUMMARY
Aging is associated with a decrease in glucose tolerance. In younger subjects both high and low intensity forms of exercise have been shown to improve glucose tolerance. The purpose of this investigation was to determine whether or not strength training in elderly subjects would have a positive effect upon glucose and insulin responsiveness following a glucose feeding. The medical history of each subject and an exercise stress test were given prior to the establishment of the two age groups: those individuals with contra-indications for exercise were not tested further. An oral glucose tolerance test, 100 g, was administered to six young (23 _+ 1 year) and 9 elderly (63 _+ 1 year) male subjects before and after 12 weeks of a supervised progressive resistance weight lifting program, which employed Nautilus equipment. All the major muscle groups of the body were exercised and a three set, six--eight repetition, training protocol was followed. Blood samples were taken at 0, 30, 60, 120 and 180 min; after centrifugation (1169 g for 15 min) the serum was frozen for analysis o f glucose and insulin. Percent body fat was determined by skin calipers and the Lean Body Mass estimated. The 6 Rep max for the leg press, leg extension and bench press machines were used to determine the strength gains made for the 12 weeks of training. The results show that both the young and elderly subjects had a significant increase (P < 0.05) in LBM and a signifcant decrease (P < 0.05) in percent body fat with training. In the young these changes occurred without a significant change in body weight, whereas the elderly had a significant increase (P < 0.05) in body weight. In terms o f strength, both the young and elderly showed significant gains (P < 0.05) following training. The training protocol had little effect on the glucose response, but did significantly lower (P < 0.05) the plasma insulin
*To whom all correspondence should be addressed. **Present address: Wellness Program, Ball Hospital, Muncie IN, U.S.A. ***Present address: National Institute for Fitness and Sport Indianapolis IN, U.S.A. 0047-6374/89/$03.50 Printed and Published in Ireland
© 1989 Elsevier Scientific Publishers Ireland Ltd.
148
response to a glucose load. In response to a 100 g oral glucose load insulin declined regardless of age, with the insulin sum of the young and elderly being, 31.8e70 and 32.6°/o lower, respectively, after training. Although strength training improved glucose tolerance in both age groups, the response of the elderly subjects was well below that of the young. In conclusion, the data present here demonstrate that 12 weeks of high resistance strength training improved the overall physical fitness level of both the young and elderly participants of this study, but did not affect age related differences.
Key words: Strength training; Glucose tolerance; Aging INTRODUCTION
It has been shown that glucose tolerance deteriorates with age [1,6,10], and that endurance forms of training are an effective way to improve glucose tolerance in younger subjects by decreasing basal and glucose stimulated insulin levels, and increasing peripheral insulin sensitivity [2--5,23,28]. Recent evidence from young subjects has shown that high resistance forms of exercise training can also influence glucose uptake by improving peripheral insulin sensitivity [8,24]. Cuppers et al. [8] compared aerobically trained athletes and sedentary subjects to weight trained individuals, and found that the strength training significantly lowered the insulin response to an oral glucose load. In another study Miller et al. [24] examined the effects of 10 weeks of weight lifting upon the glucose tolerance of college age students, and found similar results. These two investigators theorized that the improvements could be the result of repeated bouts of hypoxic exercise [8] or due to increased lean body mass [24]. If either of these mechanisms are responsible for the increased insulin responsiveness shown in younger subjects this form of exercise could be an effective way to decrease the glucose intolerance prevalent in older populations. Seals [29] has shown that older subjects can maintain glucose tolerance at the same level as their young counterparts if they are well trained aerobically. With the increasing popularity of health spas and high resistance exercise machines it seemed prudent to examine this form of training in older individuals. To this end young (23 years) and elderly (63 years) groups of subjects were strength trained for 12 weeks, and their oral glucose tolerance and insulin responsiveness measured before and after training. The training protocol employed in this study significantly (P < 0.05) increased insulin responsiveness to a 100 g oral glucose load in both the young and elderly subjects. However, the older subjects had higher basal and insulin stimulated levels of glucose than the young, both before and after training. Whether or not these differences were due to a decrease in overall physiological function or involved some change in cellular mechanisms with age i5 unclear from the data presented here.
149
METHODS
Subjects Subjects were recruited from Ball State University and Muncie, Indiana. All subjects were required to fill out a health history questionnaire and sign an informed consent form prior to testing. Two age groups were established: Elderly (62.8 __+ 0.7), which contained nine subjects, and Young (23.3 _+ 1.5), which contained six subjects. Originally each group contained 15 individuals, but several subjects dropped out of the study due to illness or injuries which were unrelated to the training protocol.
Testing Before treadmill testing, each subject was screened for contra-indications to exercise testing and the following measurements taken: 12-lead resting electrocardiogram, heart rate, blood pressure, skinfolds and girth. After pretesting, each subject was given a maximal graded exercise treadmill test using the Bruce protocol. The graded exercise test allowed us to establish a functional capacity for each subject, and was supervised by a physician. Functional capacity refers to the maximal amount of oxygen a subject can take in per minute o f exercise and will be termed the subjects VO 2 max. Basal blood samples were drawn from an anticubital vein in the morning after a 12-h fast both pre-training and post-training. The samples were centrifuged at 1169 g for 15 min and the serum removed and frozen for later analysis.
Training Upon completion of the testing procedures the subjects underwent 12 weeks of weight training. Each weight training session was preceded with 5 rain of static stretching o f the major muscle groups. The actual training session consisted of 45-60 min of isotonic weight-conditioning exercise on Nautilus equipment and involved the leg press, leg extension, leg curl, torso extension, bench press, pull down, pull over and horizontal arm adduction machines. Biceps and triceps exercises were not included in the training protocol because it was felt that they might be too intense for the elderly subjects. At the end of the weight training session the subjects performed modified situps, in which only the head and shoulders are raised. This type of situp has been termed stomach crunch and strengthens the abdominal muscles better than traditional situp exercises. Following the workout, the subjects underwent 5 min of static stretching and a 10-min cool-down period in which they walked around an indoor track associated with the weight facility. To familarize the subjects with the equipment and to instruct them in proper lifting procedures the first week of the study progressed from 1 to 3 sets. The first day of training the subjects only completed one set of ten repetitions per lift at each station. The second day another set of ten repetitions was added to each type of lift. The third day the subjects progressed to three sets and the weight was adjusted so
150 that only eight repetitions could be accomplished by the third set. The three set regimen was maintained for the duration of the 12-week training period and the subjects instructed to increase their weight by one plate (10 pounds) in each type of lift when they could successfully complete ten repetitions on the third set. The training sessions were supervised by trained personnel and were conducted in the morning (0600 --0800 h) 3 days/week. Only a few subjects were unable to train at this time.
Body composition The fat weight and percent of body fat was measured using Lang calipers and the sum of seven skinfolds equation for estimating body density. This method has been shown to be highly reliable [20]. Lean body mass was estimated by subtracting fat weight from body weight.
Strength improvement test After the first week of training a strength test was performed at the leg press, leg extension and bench press stations. Jackson et al. [19] have shown that the bench and leg press tests are valid measures of upper and lower body strength. Strength was measured as the maximal a m o u n t of weight that could be lifted with six repetitions. This test, as opposed to a single repetition max, was used to avoid undue stress in the elderly population. The same strength test was given to the subjects at the end of the 12-week training period.
Glucose tolerance An oral glucose tolerance test (OGTT) was performed on each subject 1 week preand 3 days post-training. The morning of the O G T T the subjects reported to the laboratory after an overnight fast between 0530 and 0630 h. Each individual recorded their food intake for 3 days prior to the pre-training O G T T and were asked to duplicate this diet for the 3 days prior to post-training O G T T . They were instructed to eat a normal mixed diet consisting of at least 50°70 carbohydrate for the 3 days recorded. U p o n entering the facility, the subjects rested 30 min before a pre-OGTT blood sample was taken. They were then given a glucose solution, containing 100 g of glucose, and required to drink it as quickly as possible. Once the glucose load was consumed, blood samples were obtained at 30, 60, 120 and 180 min. The samples were centrifuged at 1169 g for 15 min and the serum portion of the blood frozen fo~ later analysis of insulin and glucose. The same O G T T procedures were employed 3 days following the last exercise session. Insulin was determined using radioimmunoassay kits for insulin from Radioassay Systems Laboratories, Carson CA. The glucose content of the blood was determined using a Yellow Springs glucose analyzer.
Statistical analysis The pre- to post-differences within each group for the basal glucose and insulin
151
levels, VO 2 max, strength test and body characteristics were calculated using a paired t-test. Between group differences were compared with an unpaired t-test and 2-way ANOVA. Any significant differences noted by the ANOVA were tested with a Newman-Keul post-hoc test. The statistical analysis was conducted on a Mclntosh Plus microcomputer using Stat View 512 + (Brainpower Inc., CA). RESULTS
Subject characteristics The elderly subjects o f this study were approximately 5 kg heavier than the younger group, and experienced a significant (P < 0.05) weight gain (Table I). The increase in weight can be attributed to a significant rise (P < 0.05) in lean body mass, and was accompanied by a significant drop (P < 0.05) in percent body fat. Body weight in the younger subjects was steady throughout training but they did show a significant rise (P < 0.05) in lean body mass and a significant decrease (P < 0.05) in percent fat. The VO 2 max o f the younger subjects was approximately 1.0 1/min higher than the elderly but the difference was not statistically significant. While the younger subjects showed no change in VO 2 max with training the older group did have a slight rise in their VO 2 max.
Strength improvements The maximal amount of weight that could be lifted with six repetitions was used as an estimate o f strength and both the young and elderly group showed significant (P < 0.05 or above) gains in each of the lifts measured (Table II). The starting weight of the elderly subjects was well below that of the young and the final weight they could lift after 12 weeks of training only reached the starting point of the younger lifters. However, even though the older individuals could not lift the same amount o f weight as the younger the percent increase for the two groups was nearly identical.
Oral glucose tolerance test Glucose response (Table III). The resting glucose values, prior to ingestion of the oral glucose load, were significantly (P < 0.05) higher in the elderly subjects, both before and after training. In the younger subjects the serum glucose response to a 100 g glucose load was the same before and after training, with a peak at 30 rain and a return to pre-load level by 120 min. The only pre- to post-training difference occurred at 120 min., with the post-glucose value being significantly lower (P < 0.05) than the pre-glucose level. Although not statistically significant, the glucose sum (glucose concentration o f all time points added) o f the young group was lower after training. The glucose response o f the elderly followed the same general pattern as the young, but the levels o f glucose reached were higher. The pre-training serum glucose concentration of the elderly peaked at 30 min and remained at that level for 60 min
Post
N=
Pre
Posl
N=
77.3 _+ 2.@
76.1 _+ 1.8 61,1 4- 1.4 .,
~Young significantly higher than elderly I P < 0.05 or a b o v e )
*Values represent .~c + S E M "Post significantly higher t h a n Pre ( P < 0 0 5 or a b o v e l
(Age 62.8 ± 0 7 N = 9
Elderl.v
6 Pre Pov
Post
N=
115.0-± 6.1 1 5 6 0 ± 8.0"
198.0 ± 11.0""
148.0 4- " 5"
Pre
( A g e 2 3 3 -+ 1.5)
Young
L eg press
118.0 _+ 6.7 ~'
123.8 + 6.5 ~
71.6 _+ 5,68'
85.3 _+ 5.1
Sum 7 SkFd ~ram)
124.0 _+_ 4.9 164.0 4- 7.0
209.0 +- I0,8 ~='
t59.0 _+ 1().4 ~
Leg Extension
59.7 _+ 1.3
16.2 _+ 0.9 ~,~'
64.5 ~ 0.9 ~
63.5 + 0.9
Lean body mass (kg~
16.5 4- 0.8 ~
~.3 +_ 0.8 ~
8.6 + 0.7
Fat wt {kg)
SIX R E P E T I T I O N S T R E N C , T H -Ft!ST D A T A F O R Y O U N G A N D E L D E R I . Y S U B J E C T S
20.8 ___ 0.8 ~'
21.6 ___ 0.8 ~
10.1 +_ 0.89 ~
11.9 4-_ 0.8
07o body f a t
Groups
MAXIMAl
T A B L E 11
~Significant d i f f e r e n c e b e t w e e n y o u n g and elderly a,~ P ,~ 0 0 5
*Values represent t h e 2 _+ S . E . M . "Pre to Post differences significant at P < 0 . 0 5
9
( A g e 6 2 . 7 _+ 1.0)
Elderly
6
72.1 _+ 1,6
72.2 _ 1,31"
Pre
( A g e 2 2 . 7 +_ 1.5)
Young
Body wt (kg]
Group
BODY C H A R A C T E R I S T I C S F O R Y O U N G A N D E L D E R L Y W E I G H T T R A I N E D S U B J E C T S
TABLE I
82.0 _+ 5.9 I05.0 _~ 6 . 5
103.0 4- 9.2' 135.0 +_ 7.8"
Bench press
2 8 7 ± 0.1X'
2.82 _+ 0.15 ~
3.96 _+ 0.18
3.95 +_ 0.19
VO 2 max (I/rain)
'Ji
96.3 ± 2 . 0 97.7 ± 2.12
8 8 . 9 ± 2.4"," 8 7 . 4 ± 2.25 b
0
Time (min)
159.8 ± 8.01 172.1 ± 8.2
135.3 ± 6.0" 142.3 ± 7.2 b
30
Pre Post
Pre Post 17.6 ± 1.7" 15.3 ± 2.1
13.9 ___ 1.9"," 7 . 9 __. 1.0 b
0
Time (rain)
"Pre to P o s t d i f f e r e n c e s a r e s i g n i f i c a n t ( P < 0.05). bSignificant d i f f e r e n c e b e t w e e n y o u n g a n d e l d e r l y ( P < 0.05).
*Values r e p r e s e n t t h e x _ S . E . M .
( A g e 6 2 . 7 ± 1.0) N = 9
Elderly
( A g e 2 2 . 7 ± 1.5 N = 6
Young
Groups
107.2 ± 9.91 109.7 __. 8.4
89.9 ± 6.01 7 8 . 0 ± 4.6 b
120
78.2 ± 5.7 74.3 ± 6.21
72.1 ± 9 . 9 6 6 8 . 6 ± 5.8
180
605.2 ± 29.05 5 9 6 . 4 ± 24.8
5 0 4 . 0 ± 15.9" 4 9 1 . 6 ± 11.5 b
Sum
77.1 ± 6.9" 6 4 . 0 ± 7.0
9 7 . 9 ± 15.6 a 79.1 ± 10.0
74.0 _ 5.02 61.5 _ 6.4 b
60
85.3 ± 18.3 61.6 ± 6.9
67.2 __. 10.8" 32.6 ± 3.9-
120
53.3 ± 8.8" 32.3 ± 9.7
2 7 . 7 ± 7.3 18.2 ± 4.7 b
180
381.18 _ 56.1" 2 5 7 . 0 __. 32.3
2 7 1 . 3 ± 38.7 a 185.0 __. 2 0 . 9 b,*
Sum
T E S T (100 g L O A D ) F O R Y O U N G A N D E L D E R L Y S U B J E C T S B E F O R E A N D A F T E R A
6 4 . 9 _ 9.5 5 8 . 0 _ 4.4
30
INSULIN RESPONSE TO AN ORAL GLUCOSE TOLERANCE 12-WEEK STRENGTH TRAINING PROGRAM
T A B L E IV
163.8 ± 15.01 142.7 ± 12.3
117.9 ± 12.2 a 115.3 ± 3.7 b
60
T E S T (100 g L O A D ) F O R Y O U N G A N D E L D E R L Y S U B J E C T S B E F O R E A N D A F T E R
•S i g n i f i c a n t ( P < 0 . 0 5 ) d i f f e r e n c e b e t w e e n y o u n g a n d e l d e r l y f o r this p a r a m e t e r . bSignificant ( P < 0.05) d i f f e r e n c e b e t w e e n y o u n g a n d elderly f o r this p a r a m e t e r .
*Values r e p r e s e n t ~ ± S . E . M .
( A g e 62.7 ± 1.0) N = 9
Pre Post
Post
N = 6
Elderly
Pre
A g e 2 2 . 7 ± 1.5)
Young
Group
GLUCOSE RESPONSE TO AN ORAL GLUCOSE TOLERANCE A 12-WEEK STRENGTH TRAINING PROGRAM
T A B L E III
154
before dropping to the pre-glucose load concentration at 120 min. After training the glucose peak also occurred at 30 min but had begun to decrease by 60 rain, although the decline was not as great as that seen in the young. The glucose sum of the young and elderly remained relatively stable with training, with the glucose levels of the elderly being approximately 18o70 higher than the young subjects both before and after the 12 weeks of exercise. Insulin response (Table IV). There was no statistical difference between the initial insulin levels of the two groups but the elderly values were higher at the onset of training. After 12 weeks of strength training both age groups had significantly lower (P < 0.05) insulin concentrations, which represented a 31% drop in the young and a 20% decrease in the elderly. In response to the 100 g glucose load, insulin peaked al 60 min both before and after training regardless of age. The insulin response of the elderly subjects was much higher than the young before training, and mirrored the initial response of the young after 12 weeks of training. If the data is expressed as the sum of all the insulin values the differences between the young and elderly can be seen more clearly. Prior to training, the overall response of the elderly was 66% higher than the young, 386.5/aunits/ml vs. 232.3 /aunits/ml, respectively. After 12 weeks of exercise training both groups significantly lowered (P < 0.05) the insulin response but the difference between them was maintained, with the insulin sum of the elderly being 57% higher than the younger subjects. DISCUSSION
Although the resting or basal glucose levels of the elderly subjects of this study were significantly higher (P < 0.05) than the young, both before and after training, 12 weeks of strength training had little influence on basal glucose levels or glucose tolerance within each group. However, the basal concentrations of insulin were were significantly lower ( P < 0.05) following training in both the young and elderly subjects, and represented a 43% drop in the young and a 13% decline in the elderly. In response to a 100 g glucose load, the elderly demonstrated a far greater improvement in insulin responsiveness than the young, with post-training insulin levels of the elderly being significantly below (P < 0.05) pre-training values. A reduction in insulin response with little or no change in glucose tolerance has been cited as evidence ot improved peripheral insulin sensitivity [2--5]. Insulin sensitivity has been linked to changes in insulin receptor number [26] with increased sensitivity requiring higher numbers of receptors. Receptor number was not measured in this study but prior work [7] has shown that increases in insulin receptor number in adipocytes ol endurance trained rats could not entirely account for the dramatic change in insulin responsiveness of those cells. Insulin responsiveness refers to the ability of a tissue to respond to insulin, and involves glucose uptake or some other post-insulin receptor mechanism [26], and therefore is a more likely explanation for the changes in insulin observed in this investigation.
155
Several investigators have demonstrated that glucose uptake in adipocytes [9,14,21,22,30] and the diaphram of the rat [31] is regulated by the translocation of glucose carriers from intracellular pools to the cell membrane. Presumably, the same mechanism works in skeletal muscle and is responsible for the enhanced glucose uptake that occurs both during and following exercise [ 1 l, 12,15-- 18,25]. If this system does operate within the muscle then it is highly probable that strength training, as well as other forms o f exercise, may effect the number o f glucose carriers available for sugar uptake. While the data support this line of reasoning no direct evidence is given, and clearly additional experimentation is needed to substantiate possible training effects upon the glucose carrier system of muscle. An alternative explanation comes from recent work [12,17,18] showing that the last bout of exercise may be more important than training in increasing insulin responsiveness in the muscle. The primary mechanism responsible for the increase seems to be the creation o f glucose storage space within the muscle, due to the breakdown of glycogen [15]. High intensity exercise, such as weight training, relies on glycogenolysis for energy, and the improved insulin responsiveness of the young and old subjects of this study may be due to an increase in the muscle's ability to store glucose following exercise. Glucose uptake during muscular contraction has been shown to occur in the absence of insulin with increased responsiveness persisting for several hours following intense exercise [12,18,27]. Therefore, continued physical activity o f this nature could decrease the demand for insulin by increasing this non-insulin stimulated source of glucose. Regardless of what caused the increased responsiveness with training, the higher insulin levels of the older subjects, both pre- and post-training, indicates that their tissues could not respond as well as those of the young. In a previous study dealing with endurance training in rats [13] it was shown that exercise decreases the age related loss in muscle protein but cannot prevent it. This would imply that while the exercise training employed here can improve glucose tolerance in the elderly it cannot override the effects of the aging process. On the other hand, the lower insulin response to a glucose load o f the elderly may reflect differences in body composition a n d / o r physical fitness level between the subjects. The 12 week exercise program did significantly reduce (P < 0.05) body fat and increase (P < 0.05) Lean Body Mass (LBM) in both groups, but the elderly subjects had approximately twice the body fat of the young before and after training. In addition the maximal oxygen carrying capacity (VO 2 max) of the elderly was significantly lower than the young pre- and post-training. In a study by Seals et al. [29] it was shown that endurance training and the percent body fat can affect glucose tolerance. They preformed a O G T T on master (62 years) and young (28 years) athletes, and found the same blunted insulin response in both groups. Two older groups of untrained subjects, at 13.4070 and 20.8°70 body fat, were also tested by Seals et al. [29], and the individuals with the greater amount of fat had the lowest VO 2 max and were the least glucose tolerant. Another explanation for the lower insulin responsiveness of the elderly, and their inability to gain the same training benefits as the young, might involve differences in
tS#~
activity levels or dietary habits of the two age groups. Daily activity of the lwo subjects groups was not monitored but the higher VO: max values of the younger participants indicates a much more active lifestyle. Another factor that was not totally controlled in this study was the diet. The subjects kept a 3- day dietary record prior to the pre-training OGTT, and were asked to duplicate this diet 3 days prior to the post-training OGTT. In addition they were instructed to eat a normal mixed diet+ which was to consist of 50°70 carbohydrates, for the pre- and post-test periods However, the diet was not strictly controlled and variations in the dietary habit or young v s . elderly may have affected the ability of the body to respond to a glucose load they received. In conclusion, the data from this study demonstrate that 12 weeks of high resi~,tance strength training will decrease body fat and increase t+BM regardless ot +the subjects age. Training of this nature significantly (P < 0.05) improved insulin responsiveness to a 100 g glucose load in both young and old subjects. However, the older subjects were unable to attain the same training benefits as the young. Fhis may be related to differences in cellular mechanisms, a decline in physiological function, or variations in body composition. Additional research is needed to clarit~ how high-resistance exercise such as weight training, can influence glucose tolerance in older individuals. ACKNOWLEDGEMENTS
This research was supported by research grants from the Gerontological Institute of Notre Dame, South Bend, 1N and Ball State University, Muncie, IN. REFERENCES 1 2 3 4
5 6 7
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9
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