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European Journal of Internal Medicine 21 (2010) 404–408

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European Journal of Internal Medicine


j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e j i m

Original article

Impact of exercise intensity and duration on insulin sensitivity in women with T2D
Åsa B. Segerström a,⁎, Forouzan Glans b, Karl-Fredrik Eriksson b, Anna Maria Holmbäck a, Leif Groop b,
Ola Thorsson c, Per Wollmer c
a
Department of Health Sciences, Division of Physiotherapy, Lund University, Box 157, 221 00 Lund, Sweden
b
Department of Clinical Sciences, Malmö, Diabetes and Endocrinology, Lund University, University Hopsital Malmö, Malmö, Sweden
c
Department of Clinical Sciences, Malmö, Clinical Physiology and Nuclear Medicine Unit, Lund University, 221 05 Malmö, Sweden

a r t i c l e i n f o a b s t r a c t

Article history: Background: Clinical guidelines seldom provide in depth information about the most suitable type and
Received 4 February 2010 intensity of exercise to obtain optimal benefit in different subgroups of T2D individuals.
Received in revised form 28 April 2010 The aim of this study was to examine the effect of group exercise training on exercise capacity, insulin
Accepted 10 May 2010 sensitivity and HbA1c in women with diabetes.
Available online 8 June 2010
Methods: Twenty-two women with T2D participated in a supervised group exercise program for six months.
The program combined endurance and resistance exercise. The duration and intensity of exercise for each
Keywords:
subject was recorded. The volume of exercise was calculated as the product of exercise duration and
Exercise
Exercise tolerance
intensity. Exercise capacity, insulin sensitivity and HbA1c were measured at baseline and after six months of
Exercise therapy training. The subjects were dichotomized with respect to training volume in a high training volume group
Insulin resistance and a low training volume group.
Results: Exercise capacity did not change significantly during the training period. Insulin sensitivity increased
significantly and HbA1c decreased significantly from baseline in the high volume group but not in the low
volume group. The increase in insulin sensitivity was explained with the intensity of exercise by 30%. The
reduction in HbA1c was explained with exercise by 25%.
Conclusion: Improvement in insulin sensitivity after six months combined supervised group training in
female diabetic subjects is related to exercise intensity, whereas the reduction in HbA1c is related mainly to
training volume. Metabolic effects of training may be seen in the absence of improved exercise capacity.
© 2010 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.

1. Introduction about the most suitable type and intensity of exercise to obtain
optimal benefit in different subgroups of T2D individuals [10].
Exercise is one of the cornerstones of treatment of type 2 diabetes Little is known about the impact of intensity and duration of
(T2D) [1]. Aerobic endurance exercise has traditionally been seen as training on improvements in exercise capacity, insulin sensitivity and
the most suitable exercise mode [1–3]. Resistance exercise has lately HbA1c. Boulé et al. [11], performed a meta-analysis of the effect of
been shown to be beneficial to glucose metabolism [1,4,5]. Combined structured exercise training on fitness in subjects with T2D. Of the
endurance and resistance exercise has been shown to contribute to seven controlled trials included in the analysis, none was primarily
both improved glucose control and fitness [6–8]. designed to investigate the impact of exercise intensity and volume. A
The current recommendation for endurance exercise of the wide range of modes of training was used. The meta-analysis showed
American College of Sports Medicine (ACSM) for patients with T2D that exercise intensity, but not volume, was associated with improved
is to exercise at an intensity of 50 to 80% of heart rate ratio (HRR) or VO2peak. Improvement in HbA1c was related to relative exercise
peak oxygen uptake (VO2peak) [9]. The duration of each session is intensity (expressed as % VO2peak) but not to absolute exercise
recommended to be 20 to 60 min and should be repeated about three intensity (expressed as metabolic equivalents) or exercise duration. In
to four times per week. Resistance exercise is recommended to engage a previous meta-analysis including 12 studies [12], neither exercise
large muscle groups. Ten to fifteen repetitions of each muscle group intensity nor volume was related to improvement in HbA1c.
are recommended. The exercise program should be performed at a A few studies have examined the effects of various combinations of
minimum of two days per week with at least 48 h between sessions exercise intensity and duration in healthy, normal [13] or overweight/
[9]. Generally, clinical guidelines do not provide in depth information obese [14,15] subjects. DiPietro found [13], in elderly women, that
high intensity exercise was more beneficial for insulin sensitivity than
moderate intensity exercise when energy expenditure was kept the
⁎ Corresponding author. Tel.: +46 46 222 66 97; fax: +46 46 222 18 08. same. In contrast, Houmard et al. [14] found that for two exercise
E-mail address: asa.segerstrom@med.lu.se (Å.B. Segerström). regimens with the same energy expenditure, longer duration of

0953-6205/$ – see front matter © 2010 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.ejim.2010.05.003
Å.B. Segerström et al. / European Journal of Internal Medicine 21 (2010) 404–408 405

exercise at moderate intensity had better effects on insulin sensitivity were performed to music and led by certified instructors. During the
than shorter duration at high intensity. We are not aware of any study first three month the classes included a warm-up period (10 min),
specifically measuring the impact of exercise intensity and duration in rhythmic aerobic exercise training (15 min) including ergometric
diabetic subjects. The aim of this study was therefore to examine the cycling, resistance exercises modes for arm, leg, abdominal and back
impact of exercise intensity and duration on changes in exercise muscles (15 min), cool-down and stretching exercises (10 min).
capacity, insulin sensitivity and HbA1c in diabetic women taking part Resistance training was performed with the individuals own body
in a group training program. weight, rubber band and dumbbells as resistance, with modes such as
biceps/triceps curls, standing push-ups, crunches, sit ups and belly
2. Materials and methods backs. Each resistance exercise mode was performed 15–20 times.
During the last three month the classes included a warm-up period
2.1. Subjects (10 min), rhythmic aerobic exercise training (25 min) including step-
up, resistance exercises modes for arm, leg, abdominal and back
Twenty-two female patients with T2D living in Malmö, Sweden, muscles (10 min), cool-down and stretching exercises (10 min).
with a sedentary lifestyle, participated in the study. The patients were Resistance training was performed with the individuals own body
recruited from an endocrinology specialist clinic in Malmö for a study weight as resistance, with modes such as push-ups, crunches, sit ups
on ethnicities [16]. Approximately half of the patients were first and belly backs. Each resistance exercise mode was performed 15–20
generation immigrants from countries in the Middle East. No patient times. All subjects took part in all exercise modes but exercised at
took part in any organized physical activity before the study. different intensity.
Background data are presented in Table 1. Six of the patients had Heart rate was monitored continuously during each exercise
clinical signs of neuropathy and five patients were treated with beta session by a Polar belt (Polar Fitness F1, POLAR, Oulu, Finland). The
blockers for hypertension. Patient characteristics are fairly represen- certified instructor kept records of heart rate and exercise duration
tative for a specialist clinic treating T2D patients in Sweden. All throughout the training program. Exercise logs for each participant
subjects gave written informed consent prior to their inclusion. The were kept by the instructor. It proved to be impossible to monitor the
study was approved by the regional ethical review board at Lund individual walks in a reliable manner.
University, Sweden.
2.3. Exercise tests
2.2. Exercise protocol
An incremental exercise test was performed on an electrically
All patients were invited to take part in a six months exercise braked bicycle ergometer (Bosch EAG 551, Berlin, Germany) at baseline
training program, consisting of supervised combined group exercise and after 6 months of training. The subjects started to exercise at 30 W
training twice a week. The patients were also instructed to walk for and continued to exhaustion with the workload increasing by 15 W
1 h once a week at a level of 12–13 on Borg's 20 graded scale for rating every minute [18]. Pedalling rate was 60 rpm which was aided by both
of perceived exertion (RPE) [17]. visual feedback and verbal encouragement. Expired gas was sampled
The supervised combined group exercise training consisted of continuously via a mixing chamber and analysed for the concentration
aerobic exercise training and resistance exercise training. Aerobic of O2 and CO2 (Sensor medics 2900, Bilthoven, Netherlands). Measure-
exercise training includes rhythmic aerobic exercise modes involving ments were obtained every 20 s during 1 min at rest, continuously
large muscle groups to improve cardiovascular endurance. Resistance during exercise and for 1 min during recovery. VO2peak was determined
exercise training was performed with the individuals own body as the highest value recorded during the last minute of the exercise test.
weight, rubber band and dumbbells as resistance aimed to increase Heart rate was measured by means of electrocardiography. All patients
muscular strength and muscular endurance. Stretching routines were required to exercise until exhaustion, which was aided by verbal
aimed at improving flexibility were performed. The aerobics classes encouragement. A respiratory exchange ratio (RER) above 1.0 was
reached by all subjects. Work rate was determined as the peak value in
Table 1
Watt.
Subjects characteristics, exercise and metabolic variables at baseline and after six
months of training in the low volume (below 50th percentile of exercise volume) and
2.4. HbA1c
high volume groups. M-value and HbA1c were log-transformed before analysis due to
non-normal distribution.
HbA1c was measured by HPLC (mono S, Pharmica LKB No 17-
Low volume group High volume group
0547-01) and plasma glucose was analysed with hexokinase method
Baseline 6 months Baseline 6 months (Beckman Syncron CX System chemistry).
N 11 11 11 11
Age (years) 51.8 ± 6.5 49.8 ± 7.3
2.5. Insulin sensitivity
Height (cm) 156 ± 5 167 ± 5**
Body weight (kg) 78.7 ± 10.3 80.2 ± 10.3 93.5 ± 10.2** 91.5 ± 12.3*
BMI (kg m− 2) 32.1 ± 3.5 32.7 ± 3.5 33.5 ± 2.2 32.8 ± 3.2 A Hyperinsulinemic–euglycemic clamp was carried out at baseline
FFM (kg) 46.1 ± 4.0 45.9 ± 4.2 50.2 ± 3.9* 51.0 ± 4.6 and after 6 months of intervention. The clamp was performed after
Peak heart rate (min− 1) 173 ± 24 166 ± 19 158 ± 22 160 ± 18 10 h of overnight fast 24–72 h after the last supervised group exercise.
VO2 peak(l min− 1) 1.39 ± 0.30 1.26 ± 0.26 1.49 ± 0.27 1.49 ± 0.36
The subjects were requested not to smoke during the fast. An infusion
VO2/body weight 17.8 ± 3.6 15.6 ± 2.5 16.1 ± 3.4 16.6 ± 4.4
(ml min− 1 kg− 1) (infusion rate 45 mU/m2) of short acting human insulin (Actrapid,
Work rate (W) 102 ± 18 103 ± 17 121 ± 16* 127 ± 17* Novo Nordisk, Denmark) was started and continued for 120 min.
RER 1.11 ± 0.06 1.07 ± 0.03 1.20 ± 0.08 1.08 ± 0.08** Blood samples for the measurement of plasma glucose were obtained
HbA1c (%) 6.5 ± 1.4 6.8 ± 1.0 6.6 ± 1.2 6.1 ± 1.0†
at 5 min intervals throughout the clamp. A variable glucose infusion of
M-value 2.8 ± 1.6 2.7 ± 2.2 2.3 ± 1.5 3.1 ± 2.2†
(mg kg− 1 min− 1) 20% glucose was started to maintain plasma glucose concentration
unchanged at 5.5 mmol/l, with a coefficient of variance (CV) of 6%.
Values are means ± SD.
FFM = Fat free mass.
Insulin sensitivity was calculated from the glucose infusion rates
Significantly different between groups *p b 0.05, **p b 0.05. during the last 60 min of the euglycemic clamp (M-value) and
Significantly different within group †p b 0.05. expressed as glucose uptake per body weight [19].
406 Å.B. Segerström et al. / European Journal of Internal Medicine 21 (2010) 404–408

2.6. Fat free mass Table 2


Training characteristics in the low volume (below 50th percentile of exercise volume)
and high volume groups.
The fat free mass (FFM) was measured using bioelectric imped-
ance analysis (Akern Srl, Florence, Italy) according to Segal et al. [20]. Below 50th percentile Above 50th percentile

Duration (min/week) 167 ± 16 198 ± 9**


2.7. Calculations Intensity (HRR%) 65 ± 4 72 ± 6**
Volume (HRR% min/week) 10861 ± 1500 14278 ± 1135**
2.7.1. Exercise intensity Values are means ± SD.
The exercise intensity was expressed as a percentage of the heart Significantly different between groups **p b 0.005.
rate reserve (HHR%) calculated as
long duration and vice versa as supported by a lack of correlation
HRexercise −HRrest between exercise intensity and duration (r = 0.39, p = 0.07) (Table 2).
HRR% = × 100 There were no significant changes in VO2peak, VO2peak/body weight,
HRpeak −HRrest
or WR in either group after the training period. HbA1c decreased and
insulin sensitivity increased significantly after six months of training in
where HRexercise is the mean heart rate during the exercise session and the high volume group (Table 1).
HRrest is the heart rate recorded before the exercise test at baseline We correlated exercise intensity, duration and volume with insulin
[21]. sensitivity and HbA1c measured at six months and also with changes
in insulin sensitivity and HbA1c during the training period (Table 3).
2.7.2. Exercise duration The change in insulin sensitivity during training showed a significant
The exercise duration was defined has the mean duration (min/ correlation to training intensity and volume but not to duration.
week) of supervised group session attended during the six months. HbA1c at the end of the training period as well as change in HbA1c
One hour of walking per week was included for all subjects. showed significant negative correlations to duration and volume of
training, even if there was no correlation to intensity.
2.7.3. Exercise volume
Exercise volume (HRR% min/week) was calculated as the exercise
4. Discussion
intensity (expressed as HRR%) multiplied with the exercise duration.
The main findings of this study were that insulin sensitivity
2.7.4. Group dividing process
increased and HbA1c decreased significantly after six months of
When data were analysed in this study the participants were
combined supervised group training in subjects achieving a relatively
retrospectively divided into two groups. One group had exercised
high exercise volume, whereas no significant changes were seen in
above the 50th percentile of the exercise volume (high volume group)
subjects achieving a lower volume. Improved insulin sensitivity
and one group had exercised below the 50th percentile of the exercise
appeared to be related to training intensity, whereas improved
volume (low volume group). There were four subjects with neuro-
HbA1c appeared to be related to training volume. Almost no cardio-
pathy in the high volume group, two of whom were also treated with
respiratory exercise effects were achieved independent of exercise
betablockers. The low volume group contained three subjects treated
volume in this group of T2D women.
with betablockers, two of whom also had neuropathy.
Increased physical activity is considered an important life-style
modification in subjects with T2D. Supervised group training is often
2.7.5. Statistics
advocated as a means of maintaining adherence [22]. A meta-analysis
A paired Student's t-test was used when comparing changes with-
has shown that the effect of exercise on fitness is greater if exercise is
in groups. Unpaired Student's t-test was used when comparing
prescribed, supervised and performed in groups [23]. The training
groups. Pearson's correlation was used to analyse interaction between
program used in this study was designed so as to be varied and
variables. SPSS (version 13.0, SPSS Inc, Chicago, Illinois, USA) was used
promote adherence. It was not our intention to use a strictly
for the statistical analyses. HbA1c and M-value before and after
standardised program. As could be expected from this design, we
training as well as the changes in HbA1c and M-value after training
got a spectrum of training duration and intensity in the group. The
showed skewed distributions. They were therefore log-transformed
study should thus reflect a real life situation of supervised group
before statistical analysis. The p b 0.05 criterion was used for establishing
training, combining aerobic and resistance training.
statistical significance.
The duration of exercise during the supervised sessions was
calculated from the records kept by the supervising instructor. The
3. Results
subjects were also instructed to walk once a week during the
intervention. The adherence to this recommendation could not be
Twenty-two subjects completed six months of supervised group
monitored in a reliable manner, which gives uncertainty about the
training. Height and weight were significantly higher in the high
estimation of exercise duration. The intensity of exercise during the
volume group, though there was no significant difference in BMI. In
the low volume group were three subjects treated with beta blocker of
whom two also had clinical signs of neuropathy. In the high volume Table 3
group had four subjects clinical signs of neuropathy of whom two also Pearson's correlation coefficients between exercise variables and insulin sensitivity and
were treated with beta blocker. There was no significant difference HbA1c measured after the training period as well as the changes during the training
in VO2peak between groups but WR was significantly higher in the period (ΔM-value and ΔHbA1c). M-value and HbA1c were log-transformed before
analysis due to non-normal distribution.
high volume group both at baseline and after training. There were no
significant differences in HbA1c or insulin sensitivity at baseline Exercise M-value HbA1c ΔM-value ΔHbA1c
(Table 1). (mg kg− 1 min− 1) (%) (mg kg− 1 min− 1) (%)
Information about the training performed is shown in Table 2. Intensity 0.15 − 0.33 0.54* − 0.37
When the material was dichotomized according to exercise volume, Duration 0.16 − 0.60** 0.19 − 0.46*
there was approximately 50% difference between the two groups. Volume 0.16 − 0.56** 0.53* − 0.50*

There was a spectrum of subjects training at low intensity and with Significant correlation coefficients between variables *p b 0.05, **p b 0.005.
Å.B. Segerström et al. / European Journal of Internal Medicine 21 (2010) 404–408 407

sessions was estimated from the heart rate recorded during each studies with similar training volume (11600–18900 HRR% min/week)
session. Heart rate reserve has been shown to be an accurate method as in our high volume group [8,29,31,32,39]. Other studies with lower
to monitor exercise intensity in T2D patients with or without auto- training volume (4800–9750 HRR% min/week) showed no effect on
nomic neuropathy [24]. There were no substantial differences in the HbA1c [5,28,30,36,38]. Our results are thus in agreement with
number of subjects with neuropathy or treatment with betablockers previous studies.
between the two groups, and these factors are unlikely to have The reason why reduction in HbA1c is related to training volume is
affected the results. probably that moderate as well as intense exercise causes a short-
lasting reduction in plasma glucose [50,51]. Regular exercise, even if
4.1. Exercise effects of moderate intensity, may therefore reduce HbA1c over time.

The subjects in the high volume group were training at an intensity 4.4. Limitations
of 72%, which is within the limits recommended for this group of
patients [1,11,23,25]. They also complied with more than 80% of the One limitation of the present study is the relatively small number
exercise sessions which is generally considered satisfactory [9]. An of subjects. Exercise training studies with long duration are difficult to
increase in exercise capacity might therefore have been expected in perform, especially in sedentary subjects. The number of subjects in
these subjects. The subjects in the low volume group have, on the our groups is similar to many previous studies. A further limitation is
other hand, exercised at an intensity lower than recommended [1,9]. that the analysis was done retrospectively. The findings therefore
Studies of fitness training in T2D have primarily been performed need to be confirmed in prospective studies. Ideally, the spontaneous
with endurance exercise [5,26–40] but also with combined exercise physical activity of the subjects should also be monitored, e.g. by
[8,41]. In studies where an increase in VO2peak has been demonstrated, accelerometry. We selected not to include a non-diabetic control
exercise has amounted to 90–280 min per week [5,8,27,29–36,38– group in the study. There are several problems associated with a
41]. In studies where no increase in VO2peak was achieved, exercise control group in this type of study, e.g. matching with respect to body
amounted to 60–240 min weekly [26,28,37]. Most studies were weight. Furthermore, there is evidence suggesting that diabetic
conducted at training intensities above 60% of VO2peak [5,8,27,29– subjects respond less to exercise training than non-diabetic subjects
34,41]. Burns et al. [26] suggested that subjects with T2D respond less [52]. The optimal training program may therefore be quite different in
to training than healthy subjects, but this has not been a consistent diabetic and non-diabetic subjects.
finding [33,42,43]. In conclusion, this study suggests that the improvement in insulin
sensitivity after six months combined supervised group training in
4.2. Insulin sensitivity female diabetic subjects is related to exercise intensity, whereas the
reduction in HbA1c is related mainly to training volume. Metabolic
Most previous studies of exercise effects on insulin sensitivity in effects of training may be seen in the absence of improved exercise
T2D have used primarily endurance exercise e.g. [5,26,27,29– capacity. Further prospective studies are required to determine the
32,34,44,45]. Fewer studies have been performed on resistance appropriate type, intensity, frequency and duration of training in
exercise [5,46,47] and combined exercise [7,8]. While most studies subjects with T2D.
using endurance exercise show increased insulin sensitivity, there are
exceptions [5,26,44]. The studies on resistance and combined exercise 5. Learning points
show consistently an increase in insulin sensitivity [5,7,8,46,47]. Sigal
et al. [7] suggested that combined exercise results in greater increase
• Increase in insulin sensitivity is related to exercise intensity in
in insulin sensitivity than endurance or resistance exercise alone. It
women with type 2 diabetes.
has been suggested that a certain total energy expenditure is required
• Reduction in HbA1c is mainly related to training volume women
to enhance insulin sensitivity [27,48]. The impact of training intensity
with type 2 diabetes.
and duration has, however, not previously been addressed in diabetic
subjects. The limited information available in non-diabetic subjects is,
as indicated above, conflicting [13,14]. Our finding that insulin References
sensitivity increased only in the high volume group supports the
[1] Pedersen BK, Saltin B. Evidence for prescribing exercise as therapy in chronic
concept that a certain energy expenditure is required for this effect to disease. Scand J Med Sci Sports 2006;16(Suppl 1):3–63.
occur. The correlations analysis indicates that, for a given training [2] Eriksson JG. Exercise and the treatment of type 2 diabetes mellitus. An update.
volume, intensity rather than duration is related to improved insulin Sports Med 1999;27:381–91.
[3] Peirce NS. Diabetes and exercise. Br J Sports Med 1999;33:161–72 quiz 72-3, 222.
sensitivity. [4] Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C, White RD. Physical
activity/exercise and type 2 diabetes: a consensus statement from the American
4.3. HbA1c Diabetes Association. Diabetes Care 2006;29:1433–8.
[5] Cauza E, Hanusch-Enserer U, Strasser B, Ludvik B, Metz-Schimmerl S, Pacini G,
et al. The relative benefits of endurance and strength training on the metabolic
It is well known that training can reduce HbA1c in subjects with factors and muscle function of people with type 2 diabetes mellitus. Arch Phys
T2D [12,49]. A meta-analysis [12] including 14 trials showed that Med Rehabil 2005;86:1527–33.
[6] Loimaala A, Groundstroem K, Rinne M, Nenonen A, Huhtala H, Vuori I. Exercise
HbA1c is reduced also in the absence of weight loss. The meta-analysis training does not improve myocardial diastolic tissue velocities in Type 2 diabetes.
did not find any relation between the effect on HbA1c and intensity Cardiovasc Ultrasound 2007;5:32.
and duration of exercise. A larger meta-analysis including 103 studies [7] Sigal RJ, Kenny GP, Boule NG, Wells GA, Prud'homme D, Fortier M, et al. Effects of
aerobic training, resistance training, or both on glycemic control in type 2
of interventions [49] aimed to modify self-management of T2D and diabetes: a randomized trial. Ann Intern Med 2007;147:357–69.
including exercise also showed reduction in HbA1c. In this meta- [8] Maiorana A, O'Driscoll G, Goodman C, Taylor R, Green D. Combined aerobic and
analysis, the effect was weakly related to the duration of the resistance exercise improves glycemic control and fitness in type 2 diabetes.
Diabetes Res Clin Pract 2002;56:115–23.
intervention, but inversely related to the duration of the exercise
[9] ACSM's guidelines for exercise testing and prescription. 7 ed. New York: Lippincott
session. It should be emphasised, however, that this analysis refers to Williams & Wilkins; 2006.
the duration of exercise recommended rather than to that accom- [10] Praet SF, van Loon LJ. Exercise therapy in type 2 diabetes. Acta Diabetol 2009;46:
plished. We found a reduction in the high volume group only and that 263–78.
[11] Boule NG, Kenny GP, Haddad E, Wells GA, Sigal RJ. Meta-analysis of the effect of
the reduction in HbA1c was best correlated with training volume. structured exercise training on cardiorespiratory fitness in Type 2 diabetes
Significant reduction in HbA1c was also found in some previous mellitus. Diabetologia 2003;46:1071–81.
408 Å.B. Segerström et al. / European Journal of Internal Medicine 21 (2010) 404–408

[12] Boule NG, Haddad E, Kenny GP, Wells GA, Sigal RJ. Effects of exercise on glycemic [33] Brandenburg SL, Reusch JE, Bauer TA, Jeffers BW, Hiatt WR, Regensteiner JG.
control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled Effects of exercise training on oxygen uptake kinetic responses in women with
clinical trials. JAMA 2001;286:1218–27. type 2 diabetes. Diabetes Care 1999;22:1640–6.
[13] DiPietro L, Dziura J, Yeckel CW, Neufer PD. Exercise and improved insulin [34] Braun B, Zimmermann MB, Kretchmer N. Effects of exercise intensity on insulin
sensitivity in older women: evidence of the enduring benefits of higher intensity sensitivity in women with non-insulin-dependent diabetes mellitus. J Appl
training. J Appl Physiol 2006;100:142–9. Physiol 1995;78:300–6.
[14] Houmard JA, Tanner CJ, Slentz CA, Duscha BD, McCartney JS, Kraus WE. Effect of [35] Yeater RA, Ullrich IH, Maxwell LP, Goetsch VL. Coronary risk factors in type II
the volume and intensity of exercise training on insulin sensitivity. J Appl Physiol diabetes: response to low-intensity aerobic exercise. W V Med J 1990;86:287–90.
2004;96:101–6. [36] Dunstan DW, Mori TA, Puddey IB, Beilin LJ, Burke V, Morton AR, et al. The
[15] Bajpeyi S, Tanner CJ, Slentz CA, Duscha BD, McCartney JS, Hickner RC, et al. Effect of independent and combined effects of aerobic exercise and dietary fish intake on
exercise intensity and volume on persistence of insulin sensitivity during training serum lipids and glycemic control in NIDDM. A randomized controlled study.
cessation. J Appl Physiol 2009;106:1079–85. Diabetes Care 1997;20:913–21.
[16] Glans F, Eriksson KF, Segerstrom A, Thorsson O, Wollmer P, Groop L. Evaluation of [37] Vanninen E, Uusitupa M, Siitonen O, Laitinen J, Lansimies E. Habitual physical
the effects of exercise on insulin sensitivity in Arabian and Swedish women with activity, aerobic capacity and metabolic control in patients with newly-diagnosed
type 2 diabetes. Diabetes Res Clin Pract 2009;85:69–74. type 2 (non-insulin-dependent) diabetes mellitus: effect of 1-year diet and
[17] Borg G. An introduction to Borg's RPE-scale. Ithaca: Monement Publications; 1985. exercise intervention. Diabetologia 1992;35:340–6.
[18] Fletcher GF, Balady GJ, Amsterdam EA, Chaitman B, Eckel R, Fleg J, et al. Exercise [38] Raz I, Hauser E, Bursztyn M. Moderate exercise improves glucose metabolism in
standards for testing and training: a statement for healthcare professionals from uncontrolled elderly patients with non-insulin-dependent diabetes mellitus. Isr J
the American Heart Association. Circulation 2001;104:1694–740. Med Sci 1994;30:766–70.
[19] DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for [39] Ronnemaa T, Mattila K, Lehtonen A, Kallio V. A controlled randomized study on the
quantifying insulin secretion and resistance. Am J Physiol 1979;237:E214–23. effect of long-term physical exercise on the metabolic control in type 2 diabetic
[20] Segal KR, Van Loan M, Fitzgerald PI, Hodgdon JA, Van Itallie TB. Lean body mass patients. Acta Med Scand 1986;220:219–24.
estimation by bioelectrical impedance analysis: a four-site cross-validation study. [40] Mourier A, Gautier JF, De Kerviler E, Bigard AX, Villette JM, Garnier JP, et al.
Am J Clin Nutr 1988;47:7–14. Mobilization of visceral adipose tissue related to the improvement in insulin
[21] Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate; a sensitivity in response to physical training in NIDDM. Effects of branched-chain
longitudinal study. Ann Med Exp Biol Fenn 1957;35:307–15. amino acid supplements. Diabetes Care 1997;20:385–91.
[22] Praet SF, van Loon LJ. Exercise: the brittle cornerstone of type 2 diabetes [41] Tessier D, Menard J, Fulop T, Ardilouze J, Roy M, Dubuc N, et al. Effects of aerobic
treatment. Diabetologia 2008;51:398–401. physical exercise in the elderly with type 2 diabetes mellitus. Arch Gerontol
[23] Nielsen PJ, Hafdahl AR, Conn VS, Lemaster JW, Brown SA. Meta-analysis of the Geriatr 2000;31:121–32.
effect of exercise interventions on fitness outcomes among adults with type 1 and [42] Segal KR, Edano A, Abalos A, Albu J, Blando L, Tomas MB, et al. Effect of exercise
type 2 diabetes. Diabetes Res Clin Pract 2006;74:111–20. training on insulin sensitivity and glucose metabolism in lean, obese, and diabetic
[24] Colberg SR, Swain DP, Vinik AI. Use of heart rate reserve and rating of perceived men. J Appl Physiol 1991;71:2402–11.
exertion to prescribe exercise intensity in diabetic autonomic neuropathy. [43] Schneider SH, Amorosa LF, Khachadurian AK, Ruderman NB. Studies on the
Diabetes Care 2003;26:986–90. mechanism of improved glucose control during regular exercise in type 2 (non-
[25] Sato Y, Nagasaki M, Kubota M, Uno T, Nakai N. Clinical aspects of physical exercise insulin-dependent) diabetes. Diabetologia 1984;26:355–60.
for diabetes/metabolic syndrome. Diabetes Res Clin Pract 2007;77(Suppl 1): [44] Araiza P, Hewes H, Gashetewa C, Vella CA, Burge MR. Efficacy of a pedometer-
S87–91. based physical activity program on parameters of diabetes control in type 2
[26] Burns N, Finucane FM, Hatunic M, Gilman M, Murphy M, Gasparro D, et al. Early- diabetes mellitus. Metabolism 2006;55:1382–7.
onset type 2 diabetes in obese white subjects is characterised by a marked defect [45] O'Gorman DJ, Karlsson HK, McQuaid S, Yousif O, Rahman Y, Gasparro D, et al. Exercise
in beta cell insulin secretion, severe insulin resistance and a lack of response to training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein
aerobic exercise training. Diabetologia 2007;50:1500–8. content in patients with type 2 diabetes. Diabetologia 2006;49:2983–92.
[27] Eriksen L, Dahl-Petersen I, Haugaard SB, Dela F. Comparison of the effect of [46] Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JF, Dela F. Strength training
multiple short-duration with single long-duration exercise sessions on glucose increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling
homeostasis in type 2 diabetes mellitus. Diabetologia 2007;50:2245–53. in skeletal muscle in patients with type 2 diabetes. Diabetes 2004;53:294–305.
[28] Middlebrooke AR, Elston LM, Macleod KM, Mawson DM, Ball CI, Shore AC, et al. Six [47] Ishii T, Yamakita T, Sato T, Tanaka S, Fujii S. Resistance training improves insulin
months of aerobic exercise does not improve microvascular function in type 2 sensitivity in NIDDM subjects without altering maximal oxygen uptake. Diabetes
diabetes mellitus. Diabetologia 2006;49:2263–71. Care 1998;21:1353–5.
[29] Toledo FG, Menshikova EV, Ritov VB, Azuma K, Radikova Z, DeLany J, et al. Effects [48] Praet SF, van Loon LJ. Optimizing the therapeutic benefits of exercise in Type 2
of physical activity and weight loss on skeletal muscle mitochondria and diabetes. J Appl Physiol 2007;103:1113–20.
relationship with glucose control in type 2 diabetes. Diabetes 2007;56:2142–7. [49] Conn VS, Hafdahl AR, Mehr DR, LeMaster JW, Brown SA, Nielsen PJ. Metabolic
[30] De Filippis E, Cusi K, Ocampo G, Berria R, Buck S, Consoli A, et al. Exercise-induced effects of interventions to increase exercise in adults with type 2 diabetes.
improvement in vasodilatory function accompanies increased insulin sensitivity Diabetologia 2007;50:913–21.
in obesity and type 2 diabetes mellitus. J Clin Endocrinol Metab 2006;91:4903–10. [50] Larsen JJ, Dela F, Kjaer M, Galbo H. The effect of moderate exercise on postprandial
[31] Alam S, Stolinski M, Pentecost C, Boroujerdi MA, Jones RH, Sonksen PH, et al. The glucose homeostasis in NIDDM patients. Diabetologia 1997;40:447–53.
effect of a six-month exercise program on very low-density lipoprotein [51] Larsen JJ, Dela F, Madsbad S, Galbo H. The effect of intense exercise on postprandial
apolipoprotein B secretion in type 2 diabetes. J Clin Endocrinol Metab 2004;89: glucose homeostasis in type II diabetic patients. Diabetologia 1999;42:1282–92.
688–94. [52] Burns N, Finucane FM, Hatunic M, Gilman M, Murphy M, Gasparro D, et al. Early-
[32] Christ-Roberts CY, Pratipanawatr T, Pratipanawatr W, Berria R, Belfort R, Kashyap onset type 2 diabetes in obese white subjects is characterised by a marked defect
S, et al. Exercise training increases glycogen synthase activity and GLUT4 in beta cell insulin secretion, severe insulin resistance and a lack of response to
expression but not insulin signaling in overweight nondiabetic and type 2 aerobic exercise training. Diabetologia 2007;50:1500–8.
diabetic subjects. Metabolism 2004;53:1233–42.

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