LOW-INTENSITY RESISTANCE EXERCISE REDUCES

HYPERGLYCEMIA AND ENHANCES GLUCOSE CONTROL

OVER A 24-HOUR PERIOD IN WOMEN WITH TYPE 2
DIABETES
LOUMAÍRA CARVALHO DA CRUZ,1,2 ALFREDO A. TEIXEIRA-ARAUJO,1,2,3
KAROLINE T. PASSOS ANDRADE,4 THAISE CAMILA O GOMES ROCHA,5 GUILHERME MORAIS PUGA,6
Downloaded from https://journals.lww.com/nsca-jscr by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3YiN3qTGLcvKow8YRCUhsgn+Yt2Jxk5uUiA/8dLbvwO0= on 09/24/2019

3,4,5
AND SÉRGIO R. MOREIRA
1
Physical Education Department, UNILEA˜O—University Center, Juazeiro do Norte, Ceara´, Brazil; 2Physical Education
Department, Regional University of Cariri, URCA, Iguatu, Ceara´, Brazil; 3Graduate Program of Physical Education, Federal
University of Sa˜o Francisco Valley, UNIVASF, PE, Petrolina, Brazil; 4Graduate Program of Health and Biological Sciences,
Federal University of Sa˜o Francisco Valley—UNIVASF, Petrolina, Pernambuco, Brazil; 5College of Physical Education, Federal
University of Sa˜o Francisco Valley—UNIVASF, Petrolina, Pernambuco, Brazil; and 6Physical Education Department, Federal
University of Uberlaˆndia, Uberlaˆndia, Minas Gerais, Brazil

ABSTRACT RE80%1RM (263.966 6 62.795 mg$dl21 3 1.380 min21).

Cruz, LC, Teixeira-Araujo, AA, Andrade, KTP, Rocha, TCOG,
Puga, GM, and Moreira, SR. Low intensity resistance exercise
reduces hyperglycemia and enhances glucose control over
a 24-hour period in women with type 2 diabetes. J Strength
Cond Res 33(10): 2826–2835, 2019—The study herein aimed
to compare glucose concentration and hyperglycemic re-
sponses of 24 hours after resistance exercise (RE) performed
in different intensities in patients with type 2 diabetes (T2D).
Twelve women with T2D (55.2 6 4.0 years; 70.1 6 11.4 kg;
and 155.7 6 3.3 cm) performed 4 experimental sessions
divided into 2 blocks separated by 7 days and in randomized
order: block-A (session-1: control-CONT40% and session-2:
RE40% of one repetition maximum [1RM] test) and block-B
(session-3: CONT80% and session-4: RE80%1RM). The RE
sessions were performed over 40 minutes with 3 circuits of 7
exercises each, with 40%1RM and 80%1RM with 16 and 8
repetitions for each set, respectively. Glucose was monitored
over 24 hours after each experimental session through contin-
uous glucose-monitoring system. One-way ANOVA for
repeated measures showed that area under the curve of glu-
Hyperglycemia (.160 mg$dl21) was less prevalent (p # 0.05)
during the total period after RE40%1RM (20.8 6 21.2%)
when compared with CONT40% (77.4 6 18.3%), CONT80%
(69.4 6 24.6%), and RE80%1RM (66.0 6 33.7%). There was
a lower hyperglycemic state in RE40%1RM (p # 0.05) vs.
CONT40%, CONT80%, and RE80%1RM after breakfast
(1:25 6 0:54 vs. 4:00 6 0:00, 3:40 6 0:53, and 3:25 6
1:09 hours, respectively), lunch (1:25 6 2:03 vs. 4:55 6
0:17, 4:25 6 1:26, and 3:40 6 2:06 hours, respectively),
and dinner (0:15 6 0:27 vs. 3:15 6 0:45, 3:25 6 0:47, and
2:50 6 1:31 hours, respectively). During the sleeping period,
there was a lower hyperglycemic state (p # 0.05) in RE40%
1RM (0:20 6 0:39 hours) vs. RE80%1RM (4:05 6 3:08
hours). A single low-intensity RE40%1RM decreases hypergly-
cemic prevalence over a 24-hour period and ameliorates glu-
cose control after meals and in sleeping periods in women with
T2D.
KEY WORDS intensity, exercise, diabetes, control
INTRODUCTION

cose concentration was reduced (p # 0.05) after RE40%1RM
(193.738 6 33.186 mg$dl21 3 1.380 min21) when compared
with CONT40% (263.937 6 26.665 mg$dl21 3 1.380 min21),
CONT80% (254.721 6 35.836 mg$dl21 3 1.380 min21), and
Address correspondence to Loumaı́ra Carvalho da Cruz,
loumairacarvalhoba@gmail.com.
33(10)/2826–2835
Journal of Strength and Conditioning Research
Ó 2018 National Strength and Conditioning Association
the
T
ype 2 diabetes (T2D) is a chronic disease charac-
terized by excessive increases in blood glucose
concentration, which causes hyperglycemia, espe-
cially in postprandial times (1,25). Postprandial
hyperglycemia is a major prediction factor of microvascular
and macrovascular chronic complications (6–8,25,40) and
has been associated with endothelial dysfunction (7), arte-
riosclerosis (8), and cardiovascular diseases (CVDs), espe-
cially in women (3,6,20), who are affected mostly by
hospitalizations and have a higher risk of mortality resulting
TM

2826 Journal of Strength and Conditioning Research

Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.

from diabetes when compared with men (33). Furthermore,
maintenance of chronic hyperglycemia can cause cellular
apoptosis and lesions in organs and target tissues, such as
kidneys, retinas, and the heart (13).
Attenuating postprandial hyperglycemia can be a good
strategy to prevent CVDs, arteriosclerosis, and associated
complications (8). Thus, it is important to highlight the
importance of investigating the glycemic response of an indi-
vidual with T2D, especially over a 24-hour period, which
runs through the postprandial times. Such moments result
in up to one-third of the day spent in a hyperglycemic state
during control conditions without exercise performance for
the individual with T2D. This exposure could decrease sig-
nificantly up to 24 hours during the day with low-intensity
aerobic exercise (AE) performance (25).
Physical exercise has been defined as an efficient strategy for
blood glucose control in patients with T2D (10,23,37). This
strategy reduces blood glucose concentration and decreases
time spent in a hyperglycemic state (25,30,36,37). Although
the scientific community has shown that AE is an important
strategy in acute glycemic control (10,38), other authors such as
Church et al. (9) investigated the effects of chronic AE and
resistance exercise (RE) performed both alone and in combi-
nation, which resulted in better blood hemoglobin–glycated
levels. Evidence regarding acute (14,16,28) and chronic
(11,12,17) REs has been demonstrated in patients with T2D.
Little is known about the comparison among different
domains of intensities (low vs. high) in different days with
continuous blood glucose measurements over a period of
24 hours. An investigation of these characteristics was
reported with AE intervention where the authors found
that unlike a control session without exercise or with high-
intensity AE performance, a low-intensity session resulted in
significant glycemic control and also reduced the prevalence
of hyperglycemia in a subsequent 24-hour period (25). How-
ever, evidence of the effects of different RE intensity perfor-
mance could provide better support for exercise
recommendations regarding the optimal prescription for pa-
tients with T2D. It is well known that low-intensity RE was
effective in acute glycemic control (28). Analysis was per-
formed over a short time period (2 hours) and within a lab-
oratory environment without information of glycemic
response during lunch and dinner postprandial moments
and the sleeping period. Some studies have shown that
high-intensity RE can improve insulin sensitivity (17,22)
and increase muscle GLUT4 expression (17), which enhan-
ces the importance of investigating acute glycemic responses
during a period of 24 hours after RE sessions at different
intensities in patients with T2D.
Thus, the aim of this study was to compare blood glucose
responses and prevalence of hyperglycemia within 24 hours
after an RE session performed at low and high intensities in
women with T2D. Based on these theoretical assumptions,
low-intensity exercise results in better glycemic control
(25,28), and considering the possible increases in sympa-
Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
the TM
Journal of Strength and Conditioning Research | www.nsca.com
thetic nervous activation and higher adrenergic release dur-
ing high intensity (5), the hypothesis of this study was that
daily glycemic control can be modulated in a late acute
period after low RE performance in women with T2D.
METHODS
Experimental Approach to the Problem
To test the main hypothesis, the design of this study included 4
experimental sessions completed during 2 weeks of interven-
tion with 2 sessions each week. The intervention weeks were in
a randomized order. On day 1 of each week, a control session
(CONT40% one repetition maximum [1RM] or CONT80%
1RM) was performed, and on day 2, an RE session (40%1RM
or 80%1RM) was performed. In each session, the glycemic
responses were analyzed during a 24-hour period with
preintervention and postintervention measurements using
a continuous glucose-monitoring system (CGMS).
Subjects
Twelve postmenopausal women with T2D between 48 and
60 years old (55.2 6 4.0; Table 1) took part in the study with
a crossover randomized block design according to the CON-
SORT (Figure 1) (34). The inclusion criteria were (a) woman,
(b) diagnosed with T2D, (c) clinically stable, and (d) aged
between 40 and 60 years. Exclusion criteria considered were
(a) use of exogenous insulin, (b) morbid obesity (BMI .40
kg$m22), (c) decompensated blood glucose, (d) abnormalities
on an electrocardiogram (ECG) at rest with acute cardiac
ischemia, (e) heart disease, diabetic retinopathy, proliferative
retinopathy, or severe autonomic neuropathy, (f) upper or
lower limb amputation, (g) present uncontrolled hypertension
(systolic .160 mm Hg or diastolic blood pressure .100 mm
Hg), (h) presence of diabetic nephropathy (albuminuria $14
mg$L21 or .30 mg$24 h21), (i) chronic renal failure, (j)
exercise performance limitation because of joint/bone/skele-
tal muscle injury, and (k) smokers.
All participants were informed of risks, benefits, and
objectives of the study and gave written informed consent.
This study was approved by the local Ethics Committee of
Studies and Research from the Federal University of São
Francisco Valley (No. 0005/180814). This study is also reg-
istered at www.clinicaltrials.gov (NCT02645448). The
research was conducted according to the principles of the
Declaration of Helsinki. The general characteristics of all
participants are shown in Table 1.
Procedures
Initial Assessments and One Repetition Maximum Test. Initially,
the participants were subjected to a resting ECG, and after
a normal certificate of cardiac condition, women were
subjected to experimental study procedures. On the first
visit to the laboratory, all participants filled out an anamnesis
regarding health history and anthropometric measurements
such as waist circumference, height, and body mass for
subsequent calculation of body mass index (24) and body fat
percentage (31).
VOLUME 33 | NUMBER 10 | OCTOBER 2019 | 2827
 Resistance Exercise and Hyperglycemia
Figure 1. Consort flow diagram. RE = resistance exercise; 1RM = one repetition maximum.
Two weeks before the study intervention, all participants
underwent a familiarization with the exercise protocol during
3 alternate days. After 48 hours, 1RM test was performed (30)
in the following exercises: bench press on the machine (pecto-
ral, triceps, and anterior deltoid muscles), leg extension (quad-
riceps muscle), fly on the machine (pectoral muscle), leg curl
(biceps femoris, semitendinosus, and semimembranosus
muscles), lat pulldown (posterior muscles of the torso and
biceps), leg press (quadriceps and gluteus muscles), and seated
row (posterior muscles of the torso and biceps). All exercises
were performed on Evidence (Cachoeirinha/RS—Brazil) and
Physicus (Auriflama/SP—Brazil) equipment.
Standardization of Medication, Diet, and Physical Activity
Before and After the Interventions. After the 1RM test,
participants received instructions in relation to food intake
and the practice of daily physical activities. It was recom-
mended to avoid beverage consumption that contained
caffeine and alcohol within 48 hours before the first day of
the intervention, to fast during the days of the experimental
sessions, and to receive a standardized breakfast containing
285 kcal: 45 g (180 kcal) of carbohydrates, 6 g (24 kcal) of
proteins, and 9 g (81 kcal) of fat. Moreover, they were
instructed to maintain the same diet during the 2-week
period of the intervention and record their nutritional intake
the
2828 Journal of Strength and Conditioning Research
Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
in a food diary over a 24-hour period, which was later
analyzed and calculated by a trained nutritionist using
Microsoft Excel software and the Brazilian Table of Food
Composition (4). It was also recommended to take the main
meals at the same time each day, with the breakfast con-
trolled by the researcher (between 7:00 and 7:20 AM), lunch
between 12:00 and 2:00 PM, and dinner between 6:00 and
8:00 PM. One-way ANOVA showed no significant differences
in daily energy intake and consumption of macronutrients
between the experimental sessions (Table 1). During the
days of intervention, participants were instructed to refrain
from any exercise and strenuous physical work, except for
the scheduled experiment.
Continuous Glucose Monitoring System. After the manufac-
turer’s instructions for the CGMS Guardian REAL-Time
model (Minimed Medtronic, Inc., Northridge, CA, USA)
before the first day of the trial session, (CONT40%1RM
and CONT80%1RM) the glucose sensor (Sof-SensorTM)
was inserted into the participant. The CGMS consisted of
a sensor-transmitter inserted through a needle into the
abdominal subcutaneous tissue using a Sen-Seter device
and a display for reading by a wireless radio-frequency sen-
sor (Guardian real-time). This system has been validated by
studies regarding diabetes and its complications (26,35).
TM
 the TM

Journal of Strength and Conditioning Research | www.nsca.com

TABLE 1. Mean 6 SD of descriptive characteristics of the participants and habitual energy intake (24 hours).

CONT40%1RM 40%1RM CONT80%1RM 80%1RM

General characteristics
N 12
Age (y) 55.2 6 4.0
Body mass (kg) 70.1 6 11.4
Height (cm) 155.7 6 3.3
Body mass index (kg$m2(21)) 29.0 6 5.4
Fat percentage (%) 30.4 6 5.9
Physical active level (min$wk21) 120.2 6 22.3
T2D diagnosis (y) 5.7 6 3.7
Medication (n)
Metformin 7 (mean 6 SD: 58.4%)
Sulfonylureas 1 (mean 6 SD: 8.3%)
Metformin and Sulfonylureas 3 (mean 6 SD: 25.0%)
Diet only 1 (mean 6 SD: 8.3%)
One repetition maximal test (1RM)
Chest press (kg) 26.7 6 6.6
Leg extension (kg) 51.3 6 15.1
Peck deck (kg) 19.8 6 5.3
Leg curl (kg) 49.2 6 11.7
Lat pulldown (kg) 33.3 6 7.5
Leg press (kg) 62.5 6 18.3
Seated row (kg) 37.7 6 8.3
Glucose concentration*
Fasting glucose (mg$dl21) 139.7 6 32.4 144.5 6 34.5 145.1 6 37.4 148.1 6 35.0
Rest glucose (mg$dl21) 237.3 6 8.7 232.1 6 14.8 228.8 6 13.0 234.5 6 9.8
Energy intake
Fat (g$d21) 35.3 6 12.8 39.1 6 16.4 37.7 6 15.4 36.5 6 13.8
% intake 21.3 6 7.3 22.1 6 8.2 22.4 6 7.7 22.2 6 7.6
Carbohydrate (g$d21) 218.6 6 40.9 236.2 6 63.0 210.9 6 35.7 209.1 6 38.9
% intake 58.1 6 4.2 59.1 6 8.0 56.4 6 6.1 56.8 6 5.9
Protein (g$d21) 59.9 6 14.1 67.3 6 21.4 68.0 6 27.0 65.3 6 24.6
% intake 15.9 6 2.5 16.7 6 2.9 17.6 6 4.6 17.4 6 4.6
Energy intake (kJ$d21) 6,283.3 6 1,014.3 6,688.7 6 1,565.2 6,308.9 6 1,178.0 6,184.0 6 1,094.6

*Mean glucose concentrations before the breakfast at 7:00 AM (fasting glucose) and preintervention after the breakfast between
8:00 and 8:20 AM (rest glucose).

Immediately after CGMS installation (laboratory envi-
ronment), the equipment calibrations were performed
according to factory instructions (Minimed Medtronic,
Inc., Northridge, CA, USA). Moreover, CGMS calibra-
tions were also done during experimental session mo-
ments (daily life of the participant). Such calibrations were
performed every 6 hours for 24 hours after the experi-
mental sessions (CONT40%1RM, 40%1RM, CONT80%
1RM, and 80%1RM). The researcher went to the partic-
ipant’s location (home or workplace) to obtain blood glu-
cose samples using a glucose monitor (Accu-Check
Performa; Roche Diagnostics, Mannheim, Germany) and
for immediate calibration of the CGMS. The participants
were blinded regarding CGMS measurements, which
occurred every 5 minutes during the 24-hour period of
each experimental session, as well as blood glucose during
the equipment calibration times.
Participants with T2D were instructed to keep their
regular routines of daily life while using the CGMS, which
has a capacity of glucose measurement for a period of up to
72 hours after installation. Thus, each equipment insertion
allowed the realization from 2 to 4 experimental sessions
proposed in this study. At the end of the 48 hours of glucose
measurements corresponding to 2 experimental sessions, the
CGMS was removed, and data were exported from the
portable monitor (Guardian REAL-Time) to an online
program (CareLink; MedTronic Inc., Northridge, CA,
USA), where it converted the signals measured in glucose
values according to the manufacturer’s instructions (35). The
glucose concentrations were analyzed on day 1 (2 weeks)
over 24 hours to observe the effect of the control sessions
(CONT40%1RM and CONT80%1RM) and on day 2 (2
weeks) for the next 24 hours to observe the effect of sessions
with RE (40%1RM and 80%1RM).

VOLUME 33 | NUMBER 10 | OCTOBER 2019 | 2829

Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
 Resistance Exercise and Hyperglycemia

Figure 2. Schematic overview of the study design. CGMS = continuous glucose monitoring system; RE = resistance exercise; 1RM = one repetition maximum.

Study Design. Figure 2 presents the schematic overview of
the study design. The control sessions of the RE at 40%
1RM and 80%1RM (CONT40% and CONT80%, respec-
tively) were performed 24 hours before the respective RE
sessions. The glucose concentrations were analyzed for 4
experimental sessions, in which the same were divided into
2 blocks, separated into 7 days, and in a randomized order:
block-A (day 1: CONT40% and day 2: RE at 40%1RM)
and block-B (day 3: CONT80% and day 4: RE at 80%
1RM).
Preintervention (Rest). Before any intervention, the partic-
ipants remained seated in the laboratory for a period of
20 minutes (between 8:00 and 8:20 AM) in a quiet room with
no noise interference.
Intervention (Control and Resistance Exercise). The RE inten-
sities were established based on the American College of
Sports Medicine (ACSM) and American Diabetes Associa-
tion (ADA) for individuals with T2D recommendations (10)
and classified as 40%1RM as low exercise intensity and 80%
1RM as high exercise intensity. All interventions (RE or
control) lasted 40 minutes (between 8:20 and 9:00 AM) each
(Figure 2). The RE sessions were conducted with 3 circuits
of 7 exercises each in the same sequence as the 1RM test.
During the RE session at 40%1RM, 16 repetitions of each
exercise were performed with 60-second recovery intervals
and 120 seconds between circuits. During the RE session at
80%1RM, 8 repetitions of each exercise were performed
with a 90-second interval and 120 seconds between circuits.
The length of the repetition in each series of RE was 3 sec-
onds, with 1 second in the con-
centric phase and 2 seconds in
the eccentric phase. In control
sessions, participants remained
seated in a comfortable chair
and in the same environment
of the RE sessions.

Postintervention. At the end of

each intervention (between
9:00 and 8:00 AM), participants
were released to their routines
of everyday life and oriented to
record the daily nutritional
intake (day 1) and repeat the
same consumption in the next
day (day 2) in each of the 2
weeks of experiment. More-
over, the researcher told the
participants to avoid doing ex-
Figure 3. Mean glucose concentrations throughout the postintervention period. Vertical gray bar indicates rest ercises of any kind and to
(8:00–8:20 AM) and intervention with control or RE (8:20–9:00 AM). Vertical dashed lines indicate time of lunch
(12:00 AM), dinner (7:00 PM), and breakfast (7:00 AM). Horizontal dashed lines indicate hyperglycemic cutoff (160 maintain the use of recommen-
mg$dl21). 1RM = one repetition maximum. ded doses of medication
throughout the experiment.
the TM

2830 Journal of Strength and Conditioning Research

Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
 the TM

Journal of Strength and Conditioning Research | www.nsca.com

levels (Table 1). The use of

medication was maintained ac-
cording to the routine of each
volunteer during the experi-
ment. Analysis of food records
showed that the total daily
caloric intake was not statisti-
cally different (F[3,33] =
0.389, p = 0.765) between the
experimental sessions. More-
over, when analyzing daily car-
bohydrate (F[3,33] = 0.868;
p = 0.533), protein (F[3,33] =
0.320; p = 0.813), and lipid (F
[3,33] = 0.150; p = 0.929)
ingestion, similar values were
observed between the experi-
mental sessions (Table 1).
Finally, it is important to note
in Table 1 that the mean glu-
cose concentrations in the pre-
intervention of experimental
sessions showed no difference
in fasting glucose (F[3,33] =
0.117; p = 0.949) and resting
glucose (F[3,33] = 1.869; p =
0.148).
Figure 4. Area under the curve (AUC) of glucose concentrations (A). Prevalence of hyperglycemia (expressed as
percentage of the total time during which glucose concentrations exceeded 160 mg$dl21) within the 24-hour Glucose Concentration During
assessment period after performing sessions (B). *Significant difference 40%1RM vs. CONT40%1RM (p , Total Period
0.01); †significant difference 40%1RM vs. CONT80%1RM and 80%1RM (p , 0.01). 1RM = one repetition Figure 3 shows the kinetics of
maximum.
the blood glucose concentra-
tion during all periods of the
experimental sessions.
Statistical Analyses Figure 4A shows the AUC glucose concentration in the
Data were presented as mean and SD. The data normality was total period of different experimental sessions. It was possible
confirmed by the Shapiro-Wilk test. The glucose values were to observe an interaction between sessions (F[3,33] = 12.413;
used to determine the response throughout the postexperimen- p , 0.001) with a significant reduction in the 40%1RM ses-
tal session period and area under the curve (AUC) of glucose sion compared with other sessions (p # 0.05).
concentration. The prevalence of hyperglycemia, which corre-
sponded to blood glucose concentrations above 160 mg$dl21 Hyperglycemia Prevalence
(18), was calculated during the postmeal periods of each exper- Interaction between the experimental sessions was found in
imental session: breakfast (9:00–12:00 PM), lunch (1:00–7:00 PM), hyperglycemia (F[3,33] = 12.362; p , 0.001), which was
dinner (7:00–11:00 PM), and during sleep time (11:00 PM–6:00 prevalent in 77.4 6 18.3%, 20.8 6 21.2%, 69.4 6 24.6%,
AM). One-way ANOVA for repeated measures was performed and 66.0 6 33.7% for the 24-hour periods of CONT40%
to test the possible differences between the experimental con- 1RM, 40%1RM, CONT80%1RM, and 80%1RM sessions,
ditions (CONT40%1RM vs. 40%1RM vs. CONT80%1RM vs. respectively (Figure 4B). The 40%1RM session was found
80%1RM). The Tukey post hoc test was used when the value to be statistically different when compared with the other
of “F” was considered significant for the identification of pairs sessions (p # 0.05). The 80%1RM session showed no signif-
of differences. A p value # 0.05 was considered statistically icant difference when compared with the CONT80%1RM (p
significant. All analyses were performed using the STATISTI- = 0.986) and CONT40%1RM (p = 0.681) sessions for the
CA software for Windows v. 6.0 (StatSoft, Inc.). prevalence of hyperglycemia in the postintervention period
(Figure 4B).
RESULTS Regarding the hyperglycemia prevalence conditions after
Participants were diagnosed with T2D around 5.7 6 3.7 meals and during the sleeping times, there were significant
years and all were classified with irregular physically active interactions between the sessions in the 4 hours after

VOLUME 33 | NUMBER 10 | OCTOBER 2019 | 2831

Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
 Resistance Exercise and Hyperglycemia

moments during the low-

intensity RE session that had
TABLE 2. Mean 6 SD of glucose concentrations throughout postintervention
period and prevalence of hyperglycemia expressed as the total amount of time significant decreases in glucose
after meals and during sleep.* concentration and in hypergly-
cemic prevalence in the 24-
CONT40%1RM 40%1RM CONT80%1RM 80%1RM hour period when compared
Day period 21
(mg$dl ) 21
(mg$dl ) (mg$dl )21 21
(mg$dl ) with other experimental ses-
sions (Table 2).
Total time 196.0 6 17.4 146.0 6 25.5† 188.1 6 25.7 192.0 6 41.6 Other studies find similar
Breakfast 245.3 6 13.5 163.2 6 23.2† 226.7 6 38 209.5 6 38.5 results in relation to 24-hour
Lunch 202.3 6 16.2 146.3 6 38.9† 208.9 6 39.0 212.2 6 68.7
blood glucose concentration
Dinner 182.3 6 20.4 137.9 6 9.5† 190.3 6 20.3 196.6 6 45.6
Sleep 160.8 6 30.3 130.5 6 14.5z 160.1 6 21.8 181.6 6 42.8 and hyperglycemia prevalence
(25,36,39). However, the inter-
CONT40%1RM 40%1RM CONT80%1RM 80%1RM vention used in these previous
studies was performed with AE
Day period (h:min) (h:min) (h:min) (h:min)
in men, which the literature
Total time 18:35 6 4:23 5:00 6 5:05† 16:40 6 5:54 15:50 6 8:04 has already documented as
Breakfast 4:00 6 0:00 1:25 6 0:54† 3:40 6 0:53 3:25 6 1:09 a method which provides good
Lunch 4:55 6 0:17 1:25 6 2:03† 4:25 6 1:26 3:40 6 2:06 glycemic control (19). How-
Dinner 3:15 6 0:45 0:15 6 0:27† 3:25 6 0:47 2:50 6 1:31
Sleep 3:00 6 3:04 0:20 6 0:39z 2:55 6 2:38 4:05 6 3:08 ever, this study focuses on the
investigation of RE performed
*Prevalence of hyperglycemia: total time during which glucose concentrations exceeded with different intensities in
160 mg$dl21. Postbreakfast period: 9:00 AM–12:00 PM; postlunch period: 1:00–7:00 PM;
postdinner period: 7:00–11:00 PM; and during sleep period: 11:00 PM–6:00 AM.
women with T2D. This popu-
†p , 0.01 regarding CONT40%1RM; CONT80%1RM; and 80%1RM. lation has a higher risk of mor-
zp , 0.01 regarding 80%1RM.
tality resulting from diabetes
when compared with the male
population (33) because of psy-
chosocial and biological fac-
breakfast (F[3,33] = 22.000; p , 0.001), the 5 hours after tors, such as higher androgen hormone concentration that
lunch (F[3,33] = 10.570; p , 0.001), and within 4 hours after leads to insulin release and hepatic glucose production (20).
dinner (F[3,33] = 28.105; p , 0.001). Although there was Resistance exercise has been investigated because it
significant interaction between sessions (F[3,33] = 4.540; p , reduced HbA1c levels (11), enhanced GLUT4 expression
0.01), a significant difference (p , 0.01) was found only (17), and improved insulin sensitivity (11,22). The investiga-
between the 40%1RM and 80%1RM sessions (Table 2) in tions found in the literature only compared the effect of AE
the sleeping period (11:00 PM–6:00 AM). with RE (2), AE with the combined exercise (15), only the
Table 2 also shows the absolute concentrations of post- combined exercise (30), and the order of combined exercise
meal glucose from primary meals (after breakfast, lunch, din- execution (41). In our laboratory, it was possible to analyze
ner, and sleeping) in different experimental sessions. There the acute effect of different intensities of RE (28) comparing
was a significant reduction in glucose concentration in the a super low (23%1RM) and low (43%1RM) exercise intensi-
40%1RM session compared with other sessions (p , 0.01) in ties. There was good glycemic control in both RE sessions,
the period of 4 hours after breakfast (F[3,33] = 14.068; p , possibly because they are in the same physiological domain of
0.0001), 5 hours after lunch (F[3,33] = 5.758, p , 0.01), and 4 intensity (low to moderate) as shown by Moreira et al. (28). In
hours after dinner (F[3,33] = 11.280; p , 0.0001). In sleeping addition, blood glucose was monitored only 2 hours after the
time, there was a significant difference only between sessions proposed interventions under controlled laboratory condi-
40%1RM and 80%1RM (F[3,33] = 6.190; p , 0.01). tions, leaving a lack of information in extended acute effects,
especially with higher intensities of RE and under real con-
DISCUSSION ditions of daily living patients with T2D. This study investi-
The main findings showed that RE performed with low gated different exercise domains of intensity (low vs. high
intensity (40%1RM) reduced the AUC glucose concentra- intensity) and used the CGMS during a long day period after
tion (Figure 3) and the prevalence of hyperglycemia in the the intervention. It was shown that on the days that the RE
24-hour period (Figure 4A, B), with 73.1 6 37.7% and 68.4 6 was not performed, there was a prevalence of hyperglycemic
51.1% when compared with CONT40%1RM and 80%1RM state (24 hours) in the CONT40%1RM and CONT80%1RM
(high intensity) sessions, respectively, during total time post- sessions, with mean values in 77.4 6 18.3% (18:35 6 4:23
interventions. Moreover, these results have an important hours) and 69.4 6 24.6% (16:40 6 5:54 hours) for each
clinical application for patients with T2D based on postmeal period, respectively (Figure 4B and Table 2).
the TM

2832 Journal of Strength and Conditioning Research

Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.

The results of this study corroborate previous research
(25,36,40), where the standard oral-drug treatment does not
seem to promote sufficient protection against the hypergly-
cemic state. Thus, van Dijk et al. (40) reported that to
improve glycemic control in patients with T2D, the use of
pharmacological strategies must be associated with changes
in lifestyle, such as nutritional interventions and exercise. As
shown in the RE sessions, the low RE intensity session sig-
nificantly reduced the prevalence of hyperglycemia in the
total period (20.8 6 21.2%; 5:00 6 5:05 hours) in relation
to other sessions (Figure 4B and Table 2). Although it was
not the aim of this study, it is speculated that the possible
mechanism of this benefit found with the low intensity of RE
is associated with muscle contraction through the AMPK
pathway and subsequent translocation of GLUT4, where
the glucose uptake because of the cascade of intracellular
events occurs regardless of the insulin action (29,32). How-
ever, RE performed with high intensity showed no reduction
in the hyperglycemic state in the same 24-hour period (66.0
6 33.7%; 15:50 6 8:04 hours) when compared with the
lower intensity session (Figure 4B and Table 2). This result
can be explained by an exaggerated increase in the counter-
regulatory hormonal response (21) driven by a speed
increase of anaerobic glycolysis (27), which leads to higher
hepatic and muscle glycogenolysis, and higher gluconeogen-
esis because of higher sympathetic nervous activity after
high-intensity exercise (5).
One limitation of this study was not knowing the origin of
the measured glucose. Although we showed blood glucose
reduction in the 40%1RM session, these results should be
interpreted with caution because moderate to high-intensity
resistance exercise may also contribute to improvements in
insulin sensitivity within 24 hours after exercise (22). Further
studies with techniques for measuring glucose uptake and its
endogenous production alone are welcome to elucidate
future conclusions on this subject.
In addition, when using CGMS, it was possible to analyze
glucose concentration responses during sleeping and post-
meal times (breakfast, lunch, and dinner), which had similar
habitual energy intake during the 24 hours of experimental
sessions (Table 1). With the exception of the low-intensity
RE session, there was hyperglycemia in other sessions dur-
ing all postmeal times. The 40%1RM session showed less
prevalence of hyperglycemia at breakfast (264.6 6 22.5%
and 258.5 6 37.4%), lunch (271.2 6 41.1% and 261.4 6
58.3%), and dinner (292.3 6 32.1% and 291.2 6 61.1%)
when compared with CONT40%1RM and 80%1RM ses-
sions, respectively. These results show high clinical relevance
because postmeal hyperglycemia can be related more to
atherosclerosis development and progression and CVDs
(7,8) than the fasting glucose, which means a greater risk
for cardiovascular events, especially in women with T2D
(6). After postmeal times, the 40%1RM session also resulted
in a decrease in the prevalence of hyperglycemia during the
hours of sleeping compared with the 80%1RM session
Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
the TM
Journal of Strength and Conditioning Research | www.nsca.com
(Table 2). Previous studies (25) observed lower hyperglyce-
mia during sleep times both after exercise sessions and con-
trol sessions without exercise. It is speculated that there was
an increased sympathetic activation during the 24 hours
after the 80%1RM session (5), which may have provided
a higher production of glucose than glucose uptake in
women in this study (Table 2). Further studies are needed
to investigate the relationship of hyperglycemia after meals
and the sleep period with the autonomic nervous system
indicators in individuals with T2D.
This study only standardized the breakfast for the
participant with T2D during the experimental sessions,
suggesting another limitation and a lack of standardization
in food intake for the remainder of the day. However, there
is the external validity of our results because the participants
with T2D maintained their daily feeding routines, as shown
in statistical analysis of the participants’ food records among
the 4 experimental sessions (Table 1). Another limitation of
this study is that the results can only be extrapolated for
women with T2D. It was therefore concluded that a single
RE performed at low-intensity (40%1RM) improved glucose
concentration control and reduced the prevalence of hyper-
glycemia during 24 hours especially after meals and sleep
periods in women with T2D.
PRACTICAL APPLICATIONS
The practical application of these results may be useful in
exercise sessions designed for people with T2D. Therefore,
for individuals with a hyperglycemic state (24 hours),
a single RE session over 40 minutes with 3 circuits (16
repetitions in 7 exercises in each circuit) at 40% of 1RM
intensity is recommended. The recovery period between
exercises should be 60 seconds in which the participant
should change the exercise, and the targeted muscle groups
should be the larger ones, and the exercise should be
performed in an alternating fashion (preferably). As shown
in this study, this intervention may be effective in lowering
blood glucose and prevalence of hyperglycemia during
a 24-hour period (after meals and sleeping times) in women
with T2D. Despite those exercise intensities being consid-
ered low and thus secure in terms of cardiovascular and
endocrine stress, a previous medical screening, including an
orthopedic, cardiovascular, and metabolic evaluation, is
strongly recommended, especially to RE sessions at higher
intensity.
ACKNOWLEDGMENTS
The authors thank CAPES to fund scholarships and CNPq
proc. 470593/2013-0 (Research support foundation of the
Brazil). The authors state that the results of this study do not
constitute endorsement of the product by the authors or the
NSCA. The authors declare no conflict of interest. Trial
registration: This study is registered at www.clinicaltrials.gov
(No. NCT02645448).
VOLUME 33 | NUMBER 10 | OCTOBER 2019 | 2833
 Resistance Exercise and Hyperglycemia
REFERENCES
1. American Diabetes Association. Standards of medical care in
diabetes. Diabetes Care 37(Suppl 1): s14–s80, 2014.
2. Bacchi, E, Negri, C, Trombetta, M, Zanolin, ME, Lanza, M, Bonora,
E, and Moghetti, P. Differences in the acute effects of aerobic and
resistance exercise in subjects with T2D: Results from the RAED2
randomized trial. PLoS One 7: 1–8, 2012.
3. Barrett-Connor, EL, Cohn, BA, Wingard, DL, and Edelstein, SL.
Why is diabetes mellitus a stronger risk factor for fatal ischemic
heart disease in women than in men? The Rancho Bernardo Study.
JAMA 265: 627–631, 1991.
4. Brazilian Table of Food Composition—TACO. Center for Studies and
Research in Food (NEPA)—UNICAMP (4th ed.). Campinas, Brazil:
NEPAUNICAMP, 2011.
5. Brooks, GA, Faheym, TD, and White, TP. Exercise Physiology:
Human Bioenergetics and its Applications (2nd ed.). Berkeley,
California: Mayfield, 1995.
6. Cavalot, F, Petrelli, A, Traversa, M, Bonomo, K, Fiora, E, Conti, M,
and Trovati, M. Postprandial blood glucose is a stronger predictor of
cardiovascular events than fasting blood glucose in T2D mellitus,
particularly in women: Lessons from the San Luigi Gonzaga
Diabetes Study. J Clin Endocrinol Metab 91: 813–819, 2006.
7. Ceriello, A. Impaired glucose tolerance and cardiovascular disease:
The possible role of post-prandial hyperglicemia. Am Heart J 147:
803–807, 2004.
8. Ceriello, A. Postprandial hyperglycemia and diabetes complications:
Is it time to treat? Diabetes 54: 1–7, 2005.
9. Church, TS, Blair, SN, Cocreham, S, Johnson, W, Kramer, K, Mikus,
CR, and Earnest, CP. Effects of aerobic and resistance training on
hemoglobin A1c levels in patients with type 2 diabetes. JAMA 304:
2253–2262, 2011.
10. Colberg, SR, Sigal, RJ, Fernhall, B, Regensteiner, JG, Blissmer, BJ,
Rubin, RR, and Braun, B. Exercise and T2D: The American
College of Sports Medicine and the American Diabetes
Association: Joint position statement. Diabetes Care 33: 147–167,
2010.
11. Dunstan, DW, Daly, RM, Owen, N, Jolley, D, de Courten, M, Shaw,
J, and Zimett, P. High-intensity resistance training improves
glycemic control in older patients with type 2 diabetes. Diabetes Care
25: 1729–1736, 2002.
12. Dunstan, DW, Puddey, IB, Beilin, LJ, Burke, V, Morton, AR, and
Stanton, KG. Effects of a short-term circuit weight training program
on glycaemic control in NIDDM. Diabetes Res Clin Pract 40: 53–61,
1998.
13. Feng, B, Cao, Y, Chen, S, Ruiz, M, and Chakrabarti, S. Reprint of:
miRNA-1 regulates endothelin-1 in diabetes. Life Sci 118: 275–280,
2014.
14. Fenicchia, LM, Kanaley, JA, Azevedo, JL Jr, Miller, CS, Weinstock,
RS, Carhart, RL, and Ploutz-Snyder, LL. Influence of resistance
exercise training on glucose control in women with T2D. Metabolism
53: 284–289, 2004.
15. Figueira, FR, Umpierre, D, Casali, KR, Tetelbom, PS, Henn, NT,
Ribeiro, JP, and Schaan, BD. Aerobic and combined exercise
sessions reduce glucose variability in T2D: Crossover randomized
trial. PLoS One 8: 1–10, 2013.
16. Gordon, BA, Fraser, SF, Bird, SR, and Benson, AC. Insulin
sensitivity not modulated 24 to 78 h after acute resistance exercise in
T2D patients. Diabetes Obes Metab 15: 478–480, 2013.
17. Holten, MK, Zacho, M, Gaster, M, Juel, C, Wojtaszewski, JFP, and
Dela, F. Strength training increases insulin-mediated glucose uptake,
glut4 content, and insulin signaling in skeletal muscle in patients with
T2D. Diabetes 53: 294–305, 2004.
18. International Diabetes Federation. Clinical Guidelines Task Force:
Global Guideline for T2D. Brussels, Belgium: International Diabetes
Federation, 2012.
the TM
2834 Journal of Strength and Conditioning Research
Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
19. Karstoft, K, Winding, K, Knudsen, SH, Nielsen, JS, Thomsen, C,
Pedersen, BK, and Solomon, TP. The effects of free-living interval-
walking training on glycemic control, body composition, and
physical fitness in type-2 diabetic patients: A randomized,
controlled trial. Diabetes Care 36: 228–236, 2013.
20. Kautzky-Willer, A, Harreiter, J, and Pacini, G. Sex and gender
differences in risk, pathophysiology and complications of type 2
diabetes mellitus. Endocr Rev 37: 278–316, 2016.
21. Kjaer, M, Hollenbeck, CB, Frey-Hewitt, B, Galbo, H, Haskell, W,
and Reaven, GM. Glucoregulation and hormonal responses to
maximal exercise in noninsulin-dependent diabetes. J Appl Physiol
68: 2067–2074, 1990.
22. Koopman, R, Manders, RJ, Zorenc, AH, Hul, GB, Kuipers, H,
Keizer, HA, and van Loon, LJ. A single session of resistance exercise
enhances insulin sensitivity for at least 24 h in healthy men. Eur J
Appl Physiol 94: 180–187, 2005.
23. Leenders, M, Verdijk, LB, van der Hoeven, L, Adam, JJ, van
Kranenburg, J, Nilwik, R, and van Loon, LJ. Patients with T2D
show a greater decline in muscle mass, muscle strength, and
functional capacity with aging. J Am Med Dir Assoc 14: 585–592,
2013.
24. Lohman, TG. Anthropometry and body composition. In: Lohman
TG, Roche AF, Martorell R, eds. Anthropometric Standardization
Reference Manual. Champaign, IL: Human Kinetics, 1988. pp. 120–
138.
25. Manders, RJF, van Dijk, JWM, and van Loon, LJC. Low-intensity
exercise reduces the prevalence of hyperglycemia in T2D. Med Sci
Sports Exerc 42: 219–225, 2010.
26. Meade, LT. The use of continuous glucose monitoring in patients
with T2D. Diab Tech Therap 14: 190–195, 2012.
27. Moreira, SR, Arsa, G, Oliveira, HB, Lima, LC, Campbell, CS, and
Simões, HG. Methods to identify the lactate and glucose thresholds
during resistance exercise for individuals with T2D. J Strength Cond
Res 22: 1108–1115, 2008.
28. Moreira, SR, Simões, GC, Moraes, JF, Motta, DF, Campbell, CS,
and Simões, HG. Blood glucose control for individuals with type-2
diabetes: Acute effects of resistance exercise of lower cardiovascular-
metabolic stress. J Strength Cond Res 26: 2806–2811, 2012.
29. Musi, N, Fujii, N, Hirshman, MF, Ekberg, I, Fröberg, S, Ljungqvist,
O, Thorell, A, and Goodyear, LJ. AMP-activated protein kinase
(AMPK) is activated in muscle of subjects with T2D during exercise.
Diabetes 50: 921–927, 2001.
30. Praet, SF, Manders, RJ, Lieverse, AG, Kuipers, H, Stehouwer, CD,
Keizer, HA, and van Loon, LJ. Influence of acute exercise on
hyperglycemia in insulin-treated T2D. Med Sci Sports Exerc 38:
2037–2044, 2006.
31. Rech, CR, Santos, DL, and Silva, JCN. Development and validation
of anthropometric equations for predicting body fat in women
between 50 and 75 years old. Rev Bras Cineantropom Desempenho
Hum 8: 5–13, 2006.
32. Richter, EA and Hargreaves, M. Exercise, glut4, and skeletal muscle
glucose uptake. Phyinussiol Rev 93: 993–1017, 2013.
33. Roche, MM and Wang, PP. Sex differences in all-cause and
cardiovascular mortality, hospitalization for individuals with and
without diabetes, and patients with diabetes diagnosed early
and late. Diabetes Care 36: 2582–2590, 2013.
34. Schulz, KF, Altman, DG, and Moher, D. CONSORT 2010
statement: Updated guidelines for reporting parallel group
randomised trials. Int J Surg 9: 672–677, 2011.
35. Terada, T, Loehr, S, Guigard, E, McCargar, LJ, Bell, GJ, Senior, P,
and Boulé, NG. Test–retest reliability of a continuous glucose
monitoring system in individuals with T2D. Diab Tech Therap 16:
491–498, 2014.

36. Van Dijk, JW, Manders, RJ, Canfora, EE, Mechelen, WV, Hartgens,
F, Stehouwer, CD, and van Loon, LJ. Exercise and 24-h glycemic
control: Equal effects for all T2D patients? Med Sci Sports Exerc 45:
628–635, 2013.
37. Van Dijk, JW, Manders, RJ, Tummers, K, Bonomi, AG, Stehouwer,
CD, Hartgens, F, and van Loon, LJ. Both resistance- and endurance-
type exercise reduce the prevalence of hyperglycaemia in individuals
with impaired glucose tolerance and in insulin-treated and non-
insulin-treated type-2 diabetic patients. Diabetologia 55: 1273–1282,
2012.
38. Van Dijk, JW, Tummers, K, Stehouwer, CD, Hartgens, F, and van
Loon, LJ. Exercise therapy in T2D: Is daily exercise required to
optimize glycemic control? Diabetes Care 35: 948–954, 2012.
Copyright © 2018 National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
the TM
Journal of Strength and Conditioning Research | www.nsca.com
39. Van Dijk, JW, Venema, M, Mechelen, WV, Stehouwer, CDA,
Hartgens, F, and van Loon, LJC. Effect of moderate-intensity
exercise versus activities of daily living on 24-hour blood glucose
homeostasis in male patients with T2D. Diabetes 36: 3448–3453,
2013.
40. Van Dijk, JWM, Manders, RJF, Hartgens, F, Stehouwer, CD, Praet,
SFE, and van Loon, LJC. Postprandial hyperglycemia is highly
prevalent throughout the day in T2D patients. Diabetes Res Clin
Pract 93: 31–37, 2011.
41. Yardley, JE, Kenny, GP, Perkins, BA, Riddell, MC, Malcolm, J,
Boulay, P, and Sigal, RJ. Effects of performing resistance exercise
before versus after aerobic exercise on glycemia in type-1 diabetes.
Diabetes Care 35: 669–675, 2012.
VOLUME 33 | NUMBER 10 | OCTOBER 2019 | 2835