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Title: Effect of Moderate and High Resistance Training Intensity on Indices of Inflammatory and Oxidative Stress
Author: Kamal Azizbeigi

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This article was downloaded by: [Selcuk Universitesi]
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Research in Sports Medicine: An
International Journal
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http://www.tandfonline.com/loi/gspm20

Effect of Moderate and High Resistance
Training Intensity on Indices of
Inflammatory and Oxidative Stress
a

b

c

Kamal Azizbeigi , Mohammad Ali Azarbayjani , Sirvan Atashak &
Stephen R. Stannard

d

a

Exercise Physiology Department, Faculty of Physical Education,
Islamic Azad University, Sannadaj Branch, Iran
b

Exercise Physiology Departments, Faculty of Physical Education,
Islamic Azad University, Central Tehran Branch, Iran
c

Click for updates

Exercise Physiology Departments, Faculty of Physical Education,
Islamic Azad University, Mahabad Branch, Iran
d

Schools of Sport and Exercise, Massey University, New Zealand
Published online: 29 Jan 2015.

To cite this article: Kamal Azizbeigi, Mohammad Ali Azarbayjani, Sirvan Atashak & Stephen R.
Stannard (2015) Effect of Moderate and High Resistance Training Intensity on Indices of Inflammatory
and Oxidative Stress, Research in Sports Medicine: An International Journal, 23:1, 73-87, DOI:
10.1080/15438627.2014.975807
To link to this article: http://dx.doi.org/10.1080/15438627.2014.975807

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Research in Sports Medicine, 23:73–87, 2015
© 2014 Taylor & Francis
ISSN: 1543-8627 print/1543-8635 online
DOI: 10.1080/15438627.2014.975807

Effect of Moderate and High Resistance
Training Intensity on Indices of Inflammatory
and Oxidative Stress
KAMAL AZIZBEIGI

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Exercise Physiology Department, Faculty of Physical Education, Islamic Azad University,
Sannadaj Branch, Iran

MOHAMMAD ALI AZARBAYJANI
Exercise Physiology Departments, Faculty of Physical Education, Islamic Azad University,
Central Tehran Branch, Iran

SIRVAN ATASHAK
Exercise Physiology Departments, Faculty of Physical Education, Islamic Azad University,
Mahabad Branch, Iran

STEPHEN R. STANNARD
Schools of Sport and Exercise, Massey University, New Zealand

This study was designed to examine the effect of moderate (MR)
and high resistance (HR) training on systemic inflammation and
circulating enzymatic antioxidant activity. Thirty males were
assigned to HR (n = 10), MR (n = 10), or control (C; n = 10)
groups. Resistance training was performed for eight weeks.
Activities of superoxide dismutase (SOD), glutathione peroxidase
(GPX), creatine kinase (CK), and concentrations of malondialdehyde (MDA), interleukin-6 (IL-6), and tumor necrosis factor-alpha
(TNF-α) were measured before and after training in plasma. The
results show increased SOD activity in MR (p = 0.026) and HR (p =
0.044) groups. GPX activity in HR (p = 0.012) and MR (p = 0.037)
increased significantly more than in C. Whilst a significant reduction in MDA in MR (p = 0.013) and HR (p = 0.023) was observed
Received 29 May 2013; accepted 17 May 2014.
We would like to thank our participants in our study. Finally, we would like to thank the
Vice President of Research, Islamic Azad University, Sanandaj Branch, for providing financial
support for the present study.
Address correspondence to Mohammad Ali Azarbayjani, Iranzamin St, Shahrake Gharb SQ,
Tehran, Iran. E-mail: m_azarbayjani@iauctb.ac.ir, m.a.azarbayjani@gmail.com
73

74

K. Azizbeigi et al.

compared with C, no significant difference in IL-6, TNF-α and CK
occurred between groups. We conclude that changes in enzymatic
antioxidant defense and inflammatory markers following resistance training are independent of training intensity.
KEYWORDS resistance training, antioxidant defense, inflammation

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INTRODUCTION
During strenuous exercise the metabolic rate in the working skeletal muscle is
raised in excess of 100 times that of resting levels. The associated increase in
oxygen consumption leads to elevations in the rate of reactive oxygen species
(ROS) production (Davies, Quintanilha, Brooks, & Packer, 1982). It has been
reported that ROS can affect metabolic processes such as transcription and
expression of genes, cellular differentiation, and inflammatory response
(Kosmidou et al., 2002). ROS are not only released from muscle, but also
endothelial and immune cells to stimulate further changes during intense
physical exercise. This includes the synthesis of cytokines such as tumor
necrosis factor alpha (TNF-α) and interleukin-6 (IL-6) (Kosmidou et al.,
2002). TNF-α, and IL-6 are expressed in human skeletal muscle in strict fiber
type specific fashion, so the level of spatial recruitment, and thus intensity of
muscle contraction, will affect production of these cytokines. Additionally,
about 30% of circulating IL-6 comes from adipose tissue (Mohamed-Ali,
Pinkney, & Coppack, 1998). Regardless of cytokine circulating source,
among many markers of systemic inflammation, TNF-α and IL-6 are the
most frequently measured (Donges, Duffield, & Drinkwater, 2010). High
levels of these cytokines are strong predictors of mortality risk in middle-age
and elderly people (Arsenault et al., 2009), being associated with the risk
factor of other diseases such as diabetes and some cancers (Penninx et al.,
2004; Petersen & Pedersen, 2005).
Regular exercise training promotes antioxidant defense and has antiinflammatory effects in skeletal tissue and plasma (Cakir-Atabek, Demir,
Pinarbasili, & Gunduz, 2010; Petersen & Pedersen, 2005), and can thus be
used as a therapeutic and preventive modality to mitigate degenerative processes associated with age and systemic inflammation (Prestes et al., 2009).
However, the majority of published data reporting the effect of exercise and
associated changes in cytokines and oxidative stress are derived from studies
involving endurance training (Petersen & Pedersen, 2005; Zembroń‐Łacny,
Slowińska‐Lisowska, & Superlak, 2008; Zembron-Lacny, Slowinska-Lisowska,
& Ziemba, 2010); few studies have observed the effects of resistance training
(RT) and these data results are conflicting. For example, it has been reported
that RT (three sets, ten exercises, 3 × per week, 8–12 repetitions maximum) for
12 weeks reduced circulating C-reactive protein, and TNF-α with no change in

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Indices of Inflammatory and Oxidative Stress

75

body composition in obese, postmenopausal women (Phillips et al., 2012). On
the other hand Libardi, De Souza, Cavaglieri, Madruga, and Chacon-Mikahil
(2012) report no significant changes in TNF-α, IL-6, and CRP after sixteen
weeks resistance training in sedentary middle-age men (Libardi, et al., 2012).
While the general aim of resistance training is to gain strength or muscle
mass, a plethora of different training models, including various combinations
of sets, repetitions, intensities, and exercise order, are prescribed. These
variables may affect individual response to RT (Fleck & Kraemer, 2004). For
example, it has been reported that performing multi-joint exercises first
improves general coordination and force, while the use of smaller muscle
groups first may best target specific muscle weakness (Balsamo et al., 2013).
In addition, and in a health-related context, moderate and high intensity RT
appears to lower blood glucose levels to a greater extent than low intensity RT
(Silveira et al. 2014).
Although some information exists on the effect of RT on circulating
inflammatory markers, there is insufficient knowledge concerning the effects
of RT intensity on cytokines and oxidative stress simultaneously. Therefore,
based on a limited number of studies on this topic and their conflicting results,
this study was designed to investigate whether RT increased antioxidant
defense and decreased inflammation and whether the intensity of RT modulated any such effect. We hypothesized first that eight weeks of RT at moderate and high intensity would increase plasma superoxide dismutase and
glutathione peroxide activities. Accordingly, we also hypothesized that moderate and high intensity RT would reduce concentration of malondialdehyde
(MDA) as an index of oxidative stress, and IL-6 and TNF-α as inflammation
biomarkers after eight weeks RT. Lastly, we hypothesized that a relationship
would exist between MDA and IL-6 and/ or TNF-α.

METHODS
Subjects
Thirty untrained males volunteered to participate in the study and were
randomly assigned to one of three groups: Moderate intensity (MR; n = 10),
High intensity resistance training (HR; n = 10) and Control (C; n = 10).
Subjects were considered untrained based on the fact that none had participated in a resistance training program for the last 12 months. All subjects
were physical education students, and were otherwise recreationally physically active; participating in activities involving running, volleyball, or soccer
once a week.
The subjects were asked to refrain from resistance and any aerobic-based
exercise training during the study. Subjects completed a medical history,
obtained written approval from a physician, and signed an informed consent
form. The investigation was approved by the committee on use of Human

76

K. Azizbeigi et al.

Research Subject at Kurdistan University. Subjects attended an information
and familiarization session in which all details of the research procedures
were explained. The criteria of exclusion were indicators of cardiovascular
and pulmonary disease, smoking, obesity, and hormonal abnormalities. None
of subjects reported taking exogenous anabolic-androgenic steroids, drugs,
medication, or dietary supplements with potential on redox and inflammatory
responses.

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Performance and Physiological Measurements
Before the intervention period, all study subjects visited the laboratory for two
days at baseline. In their first day, 10 ml venous blood was obtained from
antecubital region of the left arm whilst in a seated position after 20 min of
rest. In their second day, a series of anthropometric measurements, including
high and weight (Seca, Mod 220, Germany) and skin fold thickness (Lafayette,
Mod 01127, USA) were done. Then 1RM bench press and leg press measures
were made on Heeger Sport equipment using trained staff (Tabriz, Iran).
Further 1RM measures at the end of each six session of training (every two
weeks) were made, but were not done on the same days that the subject
completed their main training program sessions.
In order to estimate 1RM, subjects were required to perform ten repetitions at 50% of 1RM estimated according to each participant’s capacity. After
2–3 min, a subsequent trial was performed for 1RM with progressively heavier
weights until the 1RM was determined within three attempts, with 3–5 min of
rest between trials. Physical Characteristics of Subjects at the Start of the Study
are presented in Table 1.

Resistance Training Protocols
Resistance training was performed three times per week on nonconsecutive
days for eight weeks, in a “circuit” fashion. The movements involved were
upper body and lower body exercises: chest press, lat pull down, leg extension and flexion, biceps and triceps curls, squats, and sit-ups. The MR group
performed three sets of 10–12 repetitions at an intensity corresponding to
65–70% of 1RM, with a 1–2 min rest period between sets. The HR group
performed three sets of 3–6 repetitions at an intensity corresponding to
85–90% of 1RM, with a 3–4 min rest period between sets (Cakir-Atabek
et al., 2010).
Subjects’ 1RM was measured again at the end of the second, fourth and
sixth weeks, and the prescribed loads were adjusted accordingly and to verify
the effectiveness of the exercise protocol. All training sessions were performed at the same time of the day (4–6 pm) and took place at the laboratory
under the supervision of a qualified and experienced instructor.

Indices of Inflammatory and Oxidative Stress

77

Blood Collection and Plasma Preparation

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After a 12-hours fasting between 10–12 am and prior to the determination of
functional and physiological measurements, a 10 ml blood sample was
obtained from an antecubital vein. The same procedure took place 72 hours
after the completion of the training program. For plasma collection, heparinized blood samples were centrifuged at 3000 (4°C) rpm for 15 min. The
supernatants were separated from cells and transferred to sterile micro-tubes
and were stored at –70°C until analysis. Plasma samples were used for
measurement of MDA, SOD, and GPX. Also, TNF-α, IL-6 and CK were measured in plasma samples.

BIOCHEMICAL ANALYSES
Antioxidant and Oxidative Stress Markers
Total SOD activity was measured using a commercially available kit RANSOD,
Cat. No. SD 125, Randox, UK). The activity GPX was measured using a
commercially available kit (RANSEL, Cat. No. RD 505, Randox, UK).
Activities of total SOD and GPX were expressed U/ml and U/l respectively.
The intra- and inter-assay CVs were lower than 6% and 7%, respectively.
Plasma malondiadehyde (MDA) was measured based on the method of
Buege and Aust and was expressed nmol/ml (Buege & Aust, 1978).

Cytokines Measurements
Concentrations of TNF-α and IL-6 were determined in duplicate by an
enzyme-linked immunosorbent assay (ELISA) according to the specifications
of the manufacturer (Bender Med System). Cytokines are presented in
values of picograms per milliliter (pg.mL−1). The intra- and inter-assay coefficients of variation were less than 7% for these biochemistry variables. To
reduce inter-assay variation, samples from each participant in each group
were analyzed on the same ELISA micro-plate on the same day. CK activity
was measured using standard kit (Pars Azmoon, Iran) and was used to
estimate exercise-induced muscle damage.

NUTRITION
All subjects were instructed to maintain their normal diet during the intervention period. Subjects completed a detailed daily food diary in which they
recorded all food and drink consumed for the four consecutive days before
beginning the training protocol. At the end of the training period, subjects
again recorded food intake for four consecutive days (prior to blood

78

K. Azizbeigi et al.

sampling). Records were analyzed for total kilocalories, protein, carbohydrate,
fat, vitamin C, vitamin E, and vitamin A using the Food Processor software
package (Esha Research, Salem, USA).

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STATISTICAL ANALYSES
All data are presented as mean ± SD. First, the Kolmogrov-Smirnov test was
used in order to determine the normality of data distribution. Homogeny of
physical characteristics of subjects at the start of the study was tested with one
way ANOVA. Dependent variables were compared using two-way, repeated
measures (pre and post-training) ANOVA to investigate the influence time and
the training intervention. A significant interaction between group and time
indicates a significant effect of training on the dependent variable of interest. If
the interaction between groups was significant, one-way ANOVA was used for
comparing means of MR, HR and control groups. Also, post hoc comparisons
using the Bonferroni method were applied to determine pairwise differences.
Dependent t-testing was used for comparing pre and post-test in groups if
time were significant. Correlation between MDA as the index of lipid peroxidation and TNF-α, IL-6, and CK was tested with Pearson’s correlation analysis.
All statistical analyses were carried out using the 17.0 version of SPSS. A p <
0.05 level of significance was used.

RESULTS
The daily energy intakes of the HR (52% ± 6%, 35% ± 6%, and 13 ± 4%;
carbohydrate, fat, and protein respectively) and MR (54% ± 5%, 34% ± 4%,
12% ± 2%; carbohydrate, fat, and protein respectively) groups were not
significantly different from those in C (56.5% ± 3%, 31% ± 2%, 12.5% ± 4%;
carbohydrate, fat, and protein respectively) during the study. As expected,
TABLE 1 Physical Characteristics of Subjects at the Start of the Study
High intensity RT
Age (yr)
Weight (kg)
Height (cm)
BMI (kg.m–2)
Body fat%
1RM(chest press) kg
1RM(squat) kg

20.5
70.5
173.8
23.5
18.5
48.5
57.3

±
±
±
±
±
±
±

1.1
3.5
2.5
1.3
2.1
7.8
5.4

Moderate intensity RT
20.8
72.9
175.2
23.8
19.1
50.6
61.5

±
±
±
±
±
±
±

1.8
4
4.8
1.5
1.9
7.54
6.8

Control
21.5
73.8
176
22.2
20.5
48.1
58.6

±
±
±
±
±
±
±

2.2
3.6
1.3
2.4
2.5
3.2
5.8

F

P

0.68
2.04
0.40
0.19
0.29
0.25
1.13

0.51
0.14
0.66
0.82
0.74
0.77
0.33

Homogeny of physical characteristics of subjects at start of the study was done with one-way ANOVA. The
values are presented as Mean ± SD of HR, MR and control. P < 0.05.

79

Indices of Inflammatory and Oxidative Stress

TABLE 2 Nutrient Analysis of the Dietary Records of the HR, MR, and Con Groups Before and
After the Training Period. Data Expressed as Mean ± SD
HR

Pre-training
0.82
0.79 ±
Post-training 1.03 ± 0.1
0.92 ±
Carbohydrates (g/kg/d) Pre-training
3.3 ± 0.8
3.7 ±
Post-training
4.8 ± 0.9
4.6 ±
Fat (g/d)
Pre-training
70.1 ± 8.5
73.7 ±
Post-training 80.1 ± 9.4
83.9 ±
Vitamin C (mg/d)
Pre-training
60 ± 6.8
49.6 ±
Post-training 66.5 ± 8.2
62.7 ±
α- tocopherol (mg/d)
Pre-training
3.8 ± 1.1
4.2 ±
Post-training
5.6 ± 0.9
5.1 ±
Vitamin A (µg/d)
Pre-training 462.5 ± 118
392.5 ±
Post-training 508.7 ± 132.4 431.8 ±

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Proteins (g/kg/d)

MR

Con
0.1
0.84
0.1
0.88 ± 0.9
1
4.1 ± 1.1
0.9
4.2 ± 1.2
7.2
75.7 ± 5.3
9.7
77.2 ± 8.2
10.5
57 ± 13.2
8.4
58.4 ± 10.6
1.1
4 ± 0.8
1.3
4.4 ± 1.2
106
387 ± 143.5
84.7 405.6 ± 125.4

F

P

0.74
2.79
1.24
0.76
0.45
1.73
2.57
1.95
0.24
2.47
1.16
2.12

0.48
0.07
0.30
0.47
0.64
0.19
0.09
0.16
0.78
0.10
0.32
0.13

Nutrient data comparison between HR, MR and Con was done with one way analyzing. P < 0.05.

total macronutrient intake increased during training in both HR and MR,
though we did not detect a significant difference between HR, MR, and C.
Nutrient analysis of the dietary records of the HR, MR and control groups
before and after the training period using one-way ANOVA test are presented
in Table 2.
Results showed no significant difference between MR and HR in chest
press and squat before beginning the study. However, chest press increased
significantly by 46.5% and 39.1% in HR (pre: 48.5 ± 7.8 vs. post: 71.1 ± 4.9 kg;
P < 0.001) and MR (pre: 50.6 ± 7.5 vs. post: 70.4 ± 5.7 kg; P < 0.001),
respectively. In addition, squat exercise significantly increased by 36.1%
and 28.9% in HR (pre: 57.3 ± 5.4 vs. post: 78 ± 4.5 kg; P < 0.001) and MR
(pre: 61.5 ± 6.8 vs. post: 79.3 ± 6.9 kg; P < 0.001), respectively. However,
there were no significant difference between HR and MR in chest press and
squat exercise after eight weeks’ resistance training. In addition, the data
revealed no significant statistical difference between MR [(BMI: pre: 23.8 ±
1.5vs. post: 23.5 ± 1.3 kg.m−2); (BF: pre: 19.1 ± 1.9 vs. post: 18.6 ± 2.3 %] and
HR [(BMI: pre: 23.5 ± 1.3 vs. post: 24.4 ± 1.2 kg.m−2); (pre: 18.5 ± 2.1 vs. post:
19.5 ± 1.4 %)] in BMI and body fat percent before and after intervention. In
addition, analyzing with one way-ANOVA showed that there was no significant
difference between HR and MR and control in all dependent variables (SOD,
GPX, MDA, IL-6, TNF-α, and CK) before the study. There was a significant
main effect of RT in SOD (P = 0.009), GPX (P = 0.001) and MDA (P = 0.003)
after resistance training protocols. Analyzing with t-test dependence showed
that SOD increased significantly in HR (p = 0.029) and MR (p = 0.024). GPX in
HR (p = 0.012) and MR (p = 0.017) increased significantly after training. There
was a significant reduction in MDA in MR (p = 0.004) and HR (p = 0.011) after
intervention (See Figure 1). In addition, the results showed that there was a


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