Aging,Metabolism,

International Journal of Sport Nutrition and Exercise Exercise Training,

2004, 14,and Glucose Tolerance / 73
73-80
© 2004 Human Kinetics Publishers, Inc.

Metabolic Effects of the Addition

of Resistive to Aerobic Exercise in Older Men

Cynthia M. Ferrara, Susan H. McCrone, David Brendle,

Alice S. Ryan, and Andrew P. Goldberg

The metabolic changes associated with the addition of 4 months of resistive

exercise to an existing aerobic exercise program (AEX+RT, n = 7) were com-
pared to a maintenance aerobic exercise program (AEX, n = 8) in overweight,
older men. The subjects in this study had recently completed a 6-month aerobic
exercise program (treadmill walking, 45 min/d, 2 d/wk). The AEX+RT group
added 6 exercises on upper- and lower-body pneumatic-resistance machines (2
sets, 15 repetitions each, 2 d/wk) to an aerobic exercise program at ≥ 70% heart
rate reserve for 30–40 min, 2 d/wk on treadmill, while the AEX group continued
the same maintenance treadmill AEX program. There were no baseline differ-
ences in body weight, VO2max, or glucose metabolism between groups. The
AEX+RT group increased upper- and lower-extremity strength by 28 ± 4% and
46 ± 6%, respectively (p < .05), despite a 9% decrease in VO2max (p < .05).
VO2max did not change in the AEX group. There was no change in the fasting
glucose or insulin levels, or the 3-h glucose responses to an oral glucose load in
either group. The insulin responses decreased by 25 ± 4% in the AEX+RT
group (p < .01) but did not change in the AEX group. In conclusion, the addition
of resistive exercise training to an existing aerobic exercise program may im-
prove insulin sensitivity in overweight, older men, and thus prevent the devel-
opment of type 2 diabetes.

Key Words: aging, glucose tolerance, exercise training

Introduction
Aerobic (2, 7, 12) and resistive (11, 13) exercise training both improve glucose
metabolism in older individuals, potentially reducing their risk for type 2 diabetes.
The physiological mechanisms contributing to the improvements in insulin action
after aerobic (AEX) or resistive (RT) exercise training may involve changes in body
composition, skeletal muscle metabolism, and/or aerobic capacity. AEX increases
VO2max and is associated with reductions in central obesity and visceral fat (12),

C. Ferrara is currently with the Department of Physical Therapy at the University of

Massachusetts Lowell, Lowell, MA 01854-5124. S.H. McCrone is currently with the School
of Nursing at West Virginia University, Morgantown, WV 26506. D. Brendle, A.S. Ryan,
and A.P. Goldberg are with the School of Medicine at the University of Maryland, Baltimore,
MD 21201.

73
 74 / Ferrara et al.

potential mechanisms mediating improvements in insulin sensitivity (5). AEX also

increases skeletal muscle oxidative capacity and capillary density (1), total muscle
GLUT4 (7), and the activity of proteins involved in insulin signaling (8), all of
which may contribute to the improvements in insulin action. Resistive training, on
the other hand, increases muscle mass, fiber area, and the capillary-to–muscle fiber
ratio, but not VO2max (4). A combined program of AEX and RT would be expected to
increase VO2max, alter body composition, and improve muscle strength to the same
degree as either exercise program alone (9). Since the mechanisms contributing to
the improvements in insulin action after either type of exercise program may differ,
it is possible that the potential improvements in glucose tolerance and insulin sensi-
tivity resulting from a combined program may be greater than the improvements
observed with either program alone. This preliminary study was designed to deter-
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mine whether the addition of RT to an existing AEX program would result in greater
improvements in glucose metabolism than observed with a maintenance AEX pro-
gram alone.

Methods
Fifteen older men (60–77 yrs) provided informed consent according to the guide-
lines of the University of Maryland Institutional Review Board for Human Re-
search. Prior to participation, all men completed 6 months of AEX (10; treadmill
walking, 2 d/wk, 45 min/d, intensity at >70% heart rate reserve), and attended an
hour-long session on nutrition and stress management once a week. The 6-month
program increased VO2max, reduced body weight, total and low density lipoprotein
cholesterol (LDL-C), and triglyceride concentrations (p < .05; 10) and reduced
insulin areas during an OGTT (p < .05), with no change in glucose areas (unpub-
lished results). The post-AEX training status was the baseline for the study. Seven of
the original 25 men volunteered to add 4 months of RT to their current aerobic
exercise program, while 8 men continued their current AEX program for 4 months.
All of the men were in good health, although 3 men (n = 2 in AEX+RT and n = 1 in
AEX) had impaired glucose tolerance. Both programs included 30–40 min of tread-
mill walking 2 d/wk at ≥ 70% heart rate reserve. The workload was evaluated each
week to maintain the exercising heart rate within the target range. The AEX+RT
program added 2 sets of six exercises on pneumatic-resistance machines, as previ-
ously described (13; 15 repetitions/set, leg press, chest press, leg curl, latissimus
pull down, leg extension, and military press). The resistance was set at 80% of the 1
repetition maximum (1 RM) for the first three to four repetitions. Starting with the
fourth repetition, the resistance was reduced just enough to permit the subject to
complete a total of 15 repetitions at a resistance requiring near maximal effort on
every repetition without interruption of the normal cadence of each repetition. The
resistance level was checked weekly and adjusted to accommodate strength gains
for each individual. Subjects alternated which exercise program (AEX or RT) they
performed first to minimize the possibility that fatigue might limit improvements in
either program. Blood pressures and heart rates were recorded before warm-up and
after completion of the exercise session.
Testing before and after the 4 months of exercise training included measures
of body composition, maximal oxygen consumption (VO2max), muscle strength (1
RM, AEX+RT only), and 3-h oral glucose tolerance tests (OGTT). Subjects were
 Aging, Exercise Training, and Glucose Tolerance / 75

encouraged not to change their current diet and to be weight stable during the
additional 4 months of exercise.
Measures of body composition included body mass index (BMI), calculated
by dividing the weight by the height squared (kg/m2), and waist-to-hip ratio (WHR),
an index of the pattern of regional body fat distribution, calculated by dividing the
waist measurement (the minimum circumference of the abdomen) by the circumfer-
ence of the buttocks at the maximal gluteal protuberance (hip measurement). Per-
cent body fat, fat-free mass (FFM, total body bone mineral content plus lean tissue
mass), and fat mass were determined by dual energy x-ray absorptiometry (DXA,
Model DPX-L, Lunar Radiation Corporation, Madison, WI, USA).
The treadmill VO2max test was performed on each subject, as previously de-
scribed (12). The test began at 0% grade and an initial treadmill speed set to elicit
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75% of the maximal heart rate measured during the screening treadmill exercise
test. A true VO2max was achieved if two of following three criteria were met: (a)
respiratory exchange ratio at maximal exercise > 1.10, (b) maximal heart rate > 90%
of age-predicted maximum (220 – age), and (c) a plateau in VO2 (<200 ml/min
change in VO2) during the last stages of exercise. Tests were repeated until all of the
subjects’ tests met these criteria for a true VO2max.
Strength testing was performed on Keiser K-300 equipment in the AEX+RT
group only, using a protocol previously described (13). Subjects were familiarized
with the equipment at least two times with low-intensity exercise sessions prior to
the initial strength evaluation. The strength testing determined a subject’s 1 RM,
defined as the maximum amount of weight that can be moved through the full range
of motion successfully one time. Strength was measured in both the upper and lower
body using the following exercise machines: leg press, leg extension, chest press,
latissimus pull down, and military press.
The OGTT was performed after a 12-h fast, 24–48 h after the last bout of
exercise. Blood samples were drawn before and at 30-min intervals for 3 h after the
ingestion of 75 g of glucose. Plasma glucose concentrations were measured using
the glucose oxidase method (Beckman Instruments, Fullerton, CA, USA). Plasma
insulin concentrations were measured by radioimmunoassay (Linco Research Inc.,
St. Charles, MO, USA). The areas under the curves for the glucose and insulin
responses during the 3-h OGTT were calculated using a trapezoidal model (14).
HOMA IR, an estimate of whole body insulin resistance, was also calculated (6):
[(Fasting insulin [uU/ml] ⫻ fasting glucose [mmol/L])/22.5].

Statistical Analyses
Differences between the AEX and AEX+RT groups and pre- and post-intervention
within each group were determined by t tests, with p ≤ .05 statistically significant.
Data are means ± standard error (SEM).

Results
There were no differences in age, weight, BMI, % body fat, fat mass, fat-free mass,
WHR, and VO2max between groups at the beginning of the intervention. Weight,
BMI, % body fat, fat mass, fat-free mass, and WHR did not change after the inter-
vention (Table 1). VO2max decreased by 9% (2.7 ± 0.1 vs. 2.4 ± 0.1 L/min, p < .05) in
 76 / Ferrara et al.

Table 1 Body Composition and Aerobic Capacity Before and After 4 Months
of Aerobic and Resistive Exercise or an Aerobic Exercise Maintenance Pro-
gram

Aerobic and
Aerobic exercise resistive exercise
(n = 8) (n = 7)
Variable Pre Post Pre Post

Age (years) 67 ± 2 69 ± 1
± ± ± ±
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Weight (kg) 91 4 93 5 87 6 88 6
BMI (kg/m2) 30.7 ± 1.4 30.0 ± 1.3 28.9 ± 1.7 28.6 ± 1.5
% Body Fat 30 ± 3 32 ± 2 28 ± 3 28 ± 3
Fat mass (kg) 28 ± 3 30 ± 3 25 ± 4 25 ± 5
Fat-free mass (kg) 63 ± 1 62 ± 2 62 ± 2 63 ± 3
WHR 0.99 ± 0.03 0.98 ± 0.03 0.92 ± 0.02 0.96 ± 0.04
VO2max (L/min) 2.8 ± 0.2 2.6 ± 0.1 2.7 ± 0.1 2.4 ± 0.1*
VO2max (ml/kg/min) 31 ± 3 29 ± 2 31 ± 1 28 ± 1*

Note. Values are means ± SEM. *Pre vs. Post, p < .05. BMI = body mass index. WHR = waist-
to-hip ratio.

the AEX+RT group, but did not change in the AEX group (2.8 ± 0.2 vs. 2.6 ± 0.1 L/
min). One RM muscle strength increased in the AEX+RT group by 48 ± 8% in leg
press, 45 ± 9% in leg extension, 25 ± 4% in chest press, 25 ± 10% in the latissimus
pull down, and 32 ± 4% in the military press (ps < .05).
There were no differences in fasting plasma glucose and insulin concentra-
tions, or glucose and insulin OGTT areas between groups at baseline (Table 2).
There was no change in fasting plasma glucose or insulin concentrations or the
OGTT glucose areas following AEX+RT or AEX alone (Figure 1). There was a 25
± 4% decrease in the OGTT insulin area in the AEX+RT group (p < .01) but no
change in the AEX group. HOMA IR decreased in the AEX+RT (p < .05) but did not
change in the AEX group.

Discussion
The results of this study show that the addition of resistive exercise to an existing
aerobic exercise program significantly reduces insulin responses to an oral glucose
load to a greater extent than a continued maintenance aerobic exercise program in
overweight, older men. The significant decrease in insulin levels, with no change in
glucose response, suggests that the addition of RT to AEX improved tissue sensitiv-
ity to insulin.
Although we found large improvements in muscle strength after RT was
added to AEX, we failed to detect an increase in fat-free mass. This conflicts with
 Aging, Exercise Training, and Glucose Tolerance / 77
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Figure 1 — The 3-h OGTT glucose and insulin areas for subjects in the AEX+RT (1A)
and AEX (1B) groups. Values not connected by lines are means ± SEM for all subjects.
 78 / Ferrara et al.

Table 2 Glucose Metabolism Before and After 4 Months of Aerobic

and Resistive Exercise or an Aerobic Exercise Maintenance Program

Aerobic Aerobic and

exercise resistive exercise
Variable Pre Post Pre Post

Fasting glucose
(mmol/L) 5.4 ± 0.1 5.5 ± 0.2 5.4 ± 0.2 5.3 ± 0.2
Fasting insulin
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(pmol/L) 80 ± 11 87 ± 11 75 ± 10 58 ± 11
HOMA IR 3.0 ± 0.5 3.5 ± 0.6 2.7 ± 0.5 2.3 ± 0.6+
OGTT
glucose area
(mmol/min/L) 1203 ± 70 1335 ± 94 1285 ± 92 1313 ± 132
OGTT
insulin area
(pmol/min/L) 71378 ± 10522 77084 ± 13193 71345 ± 15777 52585 ± 10932*

Note. Values are means ± SEM. *p < .01, Pre vs. Post. +p < .05, Pre vs. Post.

previous studies from this laboratory that have shown significant increases in fat-
free mass with RT for 3 d/wk for 4 months or longer (11, 13, 15). However, the
training protocol in the present study was only of 4 months duration, and the exercise
frequency was reduced from 3 to 2 d/wk. These differences in the training protocol
may not have been sufficient to increase fat-free mass in these men.
The AEX+RT program reduced the OGTT insulin area with no change in the
glucose area, while AEX had no effect on the glucose or insulin responses. This
suggests that the addition of RT to AEX reduced hyperinsulinemia in these obese
men without worsening their glucose tolerance. We previously showed that the
OGTT insulin area is positively correlated with the glucose infusion rate during a
euglycemic-hyperinsulinemic clamp in older men, and may be one of the best
predictors of insulin resistance in this population (3). Thus, the reduction in the
insulin response during the OGTT in the AEX+RT group is consistent with previous
reports of increased insulin sensitivity with RT (11, 13). In addition, the decrease in
HOMA IR in the AEX+RT group, appears to be a result of a nonsignificant reduc-
tion in insulin concentrations (p = .07), since glucose levels did not change with
AEX+RT. Although HOMA IR may not accurately predict insulin action in older
men with impaired glucose tolerance (3) and only estimates insulin resistance in the
fasting state, the decrease in HOMA IR in the AEX+RT group is consistent with
previous reports of increased insulin sensitivity with RT (11, 13). HOMA IR did not
decrease significantly in the AEX+RT group when the subjects with impaired glu-
cose tolerance were not included in the analysis, although it decreased in 4 out of the
5 remaining subjects after the 4-month exercise program.
 Aging, Exercise Training, and Glucose Tolerance / 79

There are several limitations of the present study. As this was a preliminary
study, the OGTT was used to assess changes in glucose and insulin responses to
exercise, not the more labor intensive euglycemic-hyperinsulinemic clamp, the
gold standard for measuring insulin action. Second, the small number of subjects in
both groups may have limited the ability to detect statistically significant changes in
glucose metabolism. Finally, the significant decrease in VO2max that occurred in the
AEX+RT group during the 4-month intervention was not anticipated, and probably
blunted the metabolic and cardiovascular effects of the combined AEX+RT pro-
gram. The reduction in time allotted to the aerobic exercise portion (30–40 vs. 45
min) and the muscle fatigue after completing the RT program may have affected the
subjects’ ability to perform the AEX component at the same workload, thereby
negatively affecting VO2max. Despite the decline in VO2max, the AEX+RT program
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reduced the insulin response to a glucose load. In contrast, the AEX maintenance
program maintained the benefits of the previous 6 months of aerobic exercise train-
ing. It will be important to maintain VO2max in future studies examining the meta-
bolic effects of combined resistive and aerobic exercise programs.
In conclusion, in spite of a reduction in VO2max, the addition of a resistive
exercise program to an existing aerobic exercise program appears to reduce
insulinemia and increase insulin sensitivity in older, overweight men beyond that
achieved by continuing in a maintenance AEX program. Future research is needed
to compare the cellular mechanisms by which RT and AEX improve insulin action
and glucose tolerance, and determine whether the effects of these programs are
additive or synergistic. This information could contribute to our understanding of
the potential metabolic benefits of exercise training in the treatment and prevention
of type 2 diabetes in older individuals.

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Acknowledgments
We thank all the subjects who volunteered, the nursing, dietary, laboratory staff, and
the exercise physiologists at the GRECC, Baltimore VAMC for assistance with research
studies. This work was supported by a T32 AG00219 training grant, a NIA K01-AG00747
grant (ASR), a V.A. Merit Review Entry Program grant (CMF), a V.A. Postdoctoral Nurse
Research Fellowship (SHM), and the Department of Veterans Affairs Baltimore Geriatric
Research, Education, and Clinical Center and Medical Research Service.