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Article Title: Effect of Resistance Training Systems on Oxidative Stress in Older Women
DOI: https://doi.org/10.1123/ijsnem.2016-0322
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
Alex S. Ribeiro 1,2, Rafael Deminice 2, Brad J. Schoenfeld 3, Crisieli M. Tomeleri 2, Camila S.
1
Center for Research in Health Sciences. University of Northern Paran, Londrina, Brazil;
2
Metabolism, Nutrition, and Exercise Laboratory. Londrina State University. Londrina, Brazil;
3
Exercise Science Department, CUNY Lehman College, Bronx, New York, USA;
4
Clinical Analyses Laboratory. Londrina State University, Londrina, Brazil;
5
Exercise and Health Laboratory, CIPER, Faculty of Human Kinetics, Universidade de Lisboa,
Lisbon, Portugal.
Address for correspondence: Alex S. Ribeiro, Carmela Dutra Street 862, Jataizinho, PR, Brazil;
silvaribeiro@hotmail.com
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
Abstract
The purpose of this study was to investigate the effect of two different resistance training (RT)
systems on oxidative stress biomarkers in older women. Fifty-nine older women (67.95.0
years) were randomly assigned to one of three groups. Two training groups performed an 8
week RT program either in traditional (TD, n= 20) or a pyramid (PR, n= 20) system 3 times
per week, or a control group (CG, n= 19). The TD program consisted of 3 sets of 8-12 RM with
constant load for the 3 sets, whereas the PR training consisted of 3 sets of 12/10/8 RM with
incremental loads for each set. As compared with the CG, both TD and PR achieved
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upregulation of the antioxidant system as evidenced by higher (P<0.05) values of total radical-
protein oxidation adducts, TD and PR presented lower (P<0.05) scores compared to CG (TD=
91.225.0 mol/L, PR= 93.030.3 mol/L, CG= 111.020.4 mol/L). However, there were
no differences (P> 0.05) between trained groups in the antioxidant capacity markers and in the
protein oxidation adducts markers. The results suggest that 8 weeks of progressive RT
load-management RT system.
Introduction
oxygen and nitrogen species (RONS) and the bodys antioxidant defense, where the production
of RONS exceeds the bodys antioxidant capacity to scavenge these products. Older adults are
under constant and increasing assault by RONS, as indicated by enhanced lipid peroxidation
and protein oxidation, given that there is an age-related decrease in bodily antioxidants
(Pansarasa et al., 2000).The deleterious and cumulative effects of chronic OS are associated
with impairments on health and development of health-related conditions in older ages such as
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insulin resistance, cardiovascular diseases, and cancers, among others (Halter et al., 2014;
Sugamura & Keaney, 2011). Specific to women, the acceleration of age-associated declines in
cardiovascular capacity are associated with reduced estrogen production and oxidative stress
observed in postmenopausal women (Moreau & Hildreth, 2014). Furthermore, chronic OS has
been associated with the age-related loss of skeletal muscle mass and strength (Cesari et al.,
2012; Howard et al., 2007), and older women are particularly susceptible to the damaging
effects of sarcopenia and dynapenia because this population possess lower levels of muscular
strength and muscle mass compared to men (Brady et a., 2014;Goodpaster et al., 2006; Hughes
et al., 2001).
Resistance training (RT) has been promoted as a primary strategy to attenuate these
age-related dysfunctions (American College of Sports Medicine, 2009; Garber et al., 2011).
Some studies have shown that RT provides benefits to older adults health by attenuating OS
(de Gonzalo-Calvo et al., 2013; Padilha et al., 2015; Parise et al., 2005). This evidence is based
on the traditional RT system, which is characterized by the use of same loads related to a given
repetition zone. However, other training systems have been developed in an attempt to
for strength training prescription. The pyramid system is characterized by increasing the load
with a corresponding decrease in repetitions across sets (Fleck & Kraemer, 2014). The changes
program, such as manipulation of training volume and intensity (Bloomer, 2008; akir-Atabek
et al., 2015; Deminice et al., 2011; Hudson et al., 2008; Parker et al., 2014; Santana et al., 2013;
Scheffer et al., 2012). Moreover, endogenous antioxidant adaptations are dependent on the
magnitude of RONS produced acutely by exercise bouts (Radak et al., 2001). Studies indicate
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that there is a dose-response relationship between magnitude of load and muscular strength
increases in older individuals (Borde et al., 2015; Csapo & Alegre, 2015; Raymond et al., 2013;
Steib et al., 2010). The pyramid system, due to its inherent characteristic of varying loads and
therefore conceivable that the pyramid system may induce differential chronic adaptations on
Therefore, the purpose of the present randomized controlled trial was to investigate the
Methods
Participants
Participant recruitment was carried out through newspaper and radio advertisings, and
home delivery of leaflets in the central area and residential neighborhoods. All participants
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
completed health history and physical activity questionnaires and met the following inclusion
criteria: 60 years old or more, physically independent, non-smokers, free from cardiac or
orthopedic dysfunction, not receiving hormonal replacement therapy, and not performing any
regular physical exercise for more than once a week over the six months preceding the
beginning of the study. Participants passed a diagnostic graded exercise stress test with 12-lead
Ninety older women were assessed for eligibility. After individual interviews, 23 were
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dismissed as potential candidates because they did not meet the inclusion criteria for the study.
The remaining 67 older women were selected for participation and then randomly divided into
one of three groups: a group that performed the RT program in traditional system (TD, n = 22),
a group that performed the RT program in a pyramid system (PR, n = 23), and a control group
that did not perform any type of physical exercise (CG, n = 22). Fifty-nine participants
completed the experiment (TD, n = 20, PR, n = 20, and CG, n = 19), and were included in the
analyses. The reasons for withdrawal were reported as lack of time (PR, n = 1), difficulty of
getting to University facilities (TD, n = 1; PR, n = 2), lack of motivation (TD, n = 1), and
personal reasons (CG, n = 2). Adherence to the program was satisfactory, with all subjects
participating in > 85% of the total sessions. Figure 1 is a schematic representation of participant
Written informed consent was obtained from all participants after a detailed description
of study procedures was provided. This investigation was conducted according to the
Declaration of Helsinki, and was approved by the local University Ethics Committee.
Experimental design
The investigation was carried out over a period of 12 weeks, with 8 weeks dedicated to
the RT program and 4 weeks used for measurements. Anthropometric and blood samples
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
measurements were performed at weeks 1-2, and 11-12. A supervised progressive RT was
Blood was collected from the antecubital vein with participants seated after a 12-hour
fasting period. After collection, tubes containing ethylenediamine tetra-aceticacid plus samples
were centrifuged at 3.000 g for 15 min and plasma aliquots stored at -70C until assayed.
Advanced oxidation protein products (AOPP) were determined in the plasma using a
et al. (Repetto et al., 1996). This method detects hydrosoluble and/or liposoluble plasma
amidinopropane). The system was calibrated with the vitamin E analog TROLOX , and the
al., 1994) and results were expressed in mmol/L. Serum nitric oxide metabolites (NOx) levels
were assessed by nitrite (NO2-) and nitrate (NO3-) concentration according to the Griess
reaction, supplemented by the reduction of nitrate to nitrite with Cadmium (Cd) (Guevara et
al., 1998).
A Z-score of the percentage changes (from pre- to post-training) of the raw data for
each parameter was calculated. Thus, a composite Z-score, derived from the average of the
components was calculated as per the following formula: (TRAP Z-core) + (-1 x AOPP Z-
Supervised RT was performed during the morning hours in the University facilities.
muscular strength and hypertrophy (American College of Sports Medicine, 2009; Garber et al.,
2011). Physical education professionals personally supervised all training programs to help
ensure consistent and safe performance. Participants performed RT using a combination of free
weights and machines. The sessions were performed 3 times per week on Mondays,
Wednesdays, and Fridays. The RT program was a whole body program with 8 exercises
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comprising one exercise with free weights and seven with machines performed in the following
order: chest press, horizontal leg press, seated row, knee extension, preacher curl (free
Participants in the TD group performed 3 sets of 8-12 repetitions maximum with the
same load in the 3 sets. Alternatively, participants in the PR group performed 3 sets with the
load increasing and number of repetitions simultaneously decreasing for each set; thus, the
number of repetitions used in each set was 12/10/8/ repetition maximum, respectively, with
variable resistance. For both systems the participants carried out exercises until volitional
Participants were instructed to inhale during the eccentric phase and exhale during the
1:2 (concentric and eccentric phases, respectively). Participants were afforded 1 to 2 min of
rest interval between sets and 2 to 3 min between each exercise. Instructors adjusted the loads
of each exercise according to the subjects abilities and improvements in exercise capacity
throughout the study in order to ensure that they were exercising with as much resistance as
possible while maintaining proper exercise technique. Progression for TD was planned when
the upper limits of the repetitions-zone were completed for two consecutive training sessions
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
and for PR when the participants were able to perform two more repetitions in the last set. For
both systems weight was increased 2-5% for the upper limb exercises and 5-10% for the lower
limb exercises to the next session (American College of Sports Medicine, 2009).
During each RT session, researchers recorded the load performed by participants for
each set of the 8 exercises. The sum of the load used in the 3 sets of the 8 exercises was
considered the total session load, and then the sum of the 3 sessions of a week was utilized as
Statistical analysis
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Two-way analysis of variance for repeated measures was applied for comparisons. A
one-way ANOVA was applied to verify the differences among groups on the isolated and
composite Z-scores. When the F-ratio was significant, Fishers post hoc test was employed to
identify the mean differences. Baseline comparisons between groups were explored with one-
way analysis of variance. The effect size (ES) was calculated as post-training mean minus pre-
training mean divided by pooled standard deviation of pre-training and post-training (Cohen,
1992). An ES of 0.20-0.49 was considered a small effect, 0.50-0.79 a moderate effect, and
0.80 a large effect (Cohen, 1992). For all statistical analyses, significance was accepted at P <
0.05. The results were analyzed in accordance with the principle of the intention to treat
analysis, whereby the baseline measurement for each individual who withdrawal from the study
was carried forward to post-intervention (Gupta, 2011). The data were analyzed using
Results
The total training load at weeks 1 and 8 are depicted in Table 2. There was a significant
group effect, in which, as expected, the PR presented higher values than the TD. There was a
significant time effect with both groups showing increases; no group-by-time interaction was
noted.
according to groups. At baseline, there was no statistical difference (P > 0.05) among groups
for any variable. After the intervention period, both TD and PR groups presented higher (P <
0.05) values for antioxidant capacity (TRAP) compared to CG, while for the protein oxidation
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adducts measured as AOPP, TD and PR presented lower (P < 0.05) scores compared to CG.
There were no differences (P > 0.05) between trained groups in the antioxidant capacity
markers and in the protein oxidation adducts markers. Lipid peroxidation (FOX) and NOx did
not reach statistical significance (P > 0.05) for any main effects.
The Z-scores of the percentage changes from pre- to post-training for each biomarker
are presented in Table 4. For TRAP and AOPP both trained groups presented significant
differences (P < 0.05) compared to CG. However, no significant differences (P > 0.05) were
observed for FOX and NOx. The composite Z-score of the percentage changes from pre- to
post-training of the OS according to group are displayed in Figure 2. A significant effect (P <
0.05) was observed, whereby the both training groups presented higher positive variations in
0.60).
Discussion
The main and novel finding of the present study was that RT as both traditional and
pyramid system promotes significant changes in antioxidant metabolism that are positively
reflected in OS markers in older women. We had hypothesized that RT systems would produce
markers were found between training systems. To the best of our knowledge, this is the first
randomized controlled trial that has endeavored to compare the effects of RT systems on OS
in older women.
We can speculate on some possible reasons for the lack of observed differences on OS
between RT systems. For one, the repetition range applied in PR may have been too narrow to
elicit sufficiently higher mechanical stresses compared to TD and thus induce differential
adaptations. Alternatively, there may be a threshold for intensity in older women with respect
to maximizing OS, and this threshold may have been achieved in the TD group, thereby
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rendering the higher load achieved by PR irrelevant from an OS standpoint. Further studies
using the pyramid system with a wider repetition range (e.g. 15, 10, 5 RM) are warranted to
Although we did not observe any difference between systems, the RT induced a positive
changes in a composite Z-score. This approach may be an important tool to estimate the effect of
training, because it considers the overall response of a RT program, allowing the ability to draw
found that both training groups presented similar composite Z-scores that were significantly higher
than CG, indicating that of the whole sample, the participants who performed the RT achieved greater
positive improvements in OS. To date, few studies have investigated the RT effect on OS biomarkers,
and our outcomes agree with some previous investigations that observed improvement on OS in older
individuals (Padilha et al., 2015; Parise et al., 2005; Vincent et al., 2006). Parise et al. (2005) showed
that 12 weeks of RT with three sessions per week increased muscle antioxidant capacity in older
individuals (mean age 71 years). Similar results were demonstrated by Vincent et al. (2006), who
found OS reductions in older individuals (age range 60 to 72 years) following 24 weeks of RT.
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
known factors. Physical exercise can increase the synthesis of RONS through the activation
of the electron transport chain, and the synthesis of lactic acid, catecholamines and
mitochondria (McHugh et al., 1999). Additionally, anaerobic exercise, such as RT, can increase
the synthesis of xanthine oxidase and NADPH oxidase enzymes both of which affect OS
modulation (McHugh et al., 1999). In response to this process, the antioxidant system adapts
with adjustments favorable to the endogenous antioxidant system, thus increasing the body's
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defense capacity.
(TRAP) while reducing protein oxidation (AOPP). These findings are at odds with previous
work from our laboratory (Padilha et al., 2015) that showed RT chronically improves OS by
increasing TRAP while maintaining AOPP in older women. Although there is not a definitive
training protocols may have influenced adaptations. In the former study, the participants
performed one single set per exercise twice or thrice per week for 12 weeks, whereas the
present study lasted 8 weeks with three sets performed per exercise. Although speculative,
there may be a volume and/or frequency interaction that differentially influences the response
of TRAP and AOPP. That said, it is not possible to conclude whether the responses are time-
training without direct mechanistic investigation. Taken together these results allow us to
hypothesis warrants investigation in future studies with different combinations of volume and
intensity.
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
The results of this investigation indicate that RT did not significantly influence NOx.
These findings are consistent with those of Cocks et al. (2014), who also did not detect changes
in NO levels following regimented RT (Maeda et al., 2006; Maiorana et al., 2003). The reason
This investigation has some limitations that must be considered when attempting to
draw evidence-based conclusions. The results reported in this experiment are specific to
superoxide dismutase and glutathione peroxidase activities were not measured; investigation
of these markers could better reflect antioxidant system adaptation induced by RT. We also did
not control or evaluate subjects nutritional intake and daily physical activity levels, which may
have confounded results. The intake of antioxidants may upregulate the antioxidant system.
However, the older women were asked to maintain their regular daily living activities
throughout this period and not to change their nutritional habits to minimize life style
interferences.
Conclusion
older women regardless of the system, specifically by the maintenance of the antioxidant
capacity and a reduction in protein oxidant adducts formation. From a clinical point of view,
our findings indicate that RT can be applied as a therapeutic and preventative tool to attenuate
OS associated with aging in older women. From a practical standpoint, results indicate that a
flexible approach to training load manipulation can be used according to individual preferences
and responsiveness to the respective training programs. Future studies are warranted to verify
the effects of longer intervention periods, manipulation of different variables that make up RT
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
induced by RT.
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Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
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International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
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Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
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Figure 2. Composite Z-score of the percentage changes from pre- to post-training of the
oxidative stress according to groups in older women. P< 0.05 vs. control. #P< 0.05 vs. 1
control group.
Effect of Resistance Training Systems on Oxidative Stress in Older Women by Ribeiro AS et al.
International Journal of Sport Nutrition and Exercise Metabolism
2017 Human Kinetics, Inc.
Table 1 General characteristics of the sample at baseline. Data are expressed as mean and
standard deviation.
Age (years) 68.6 6.5 67.5 5.4 66.3 4.0 1.34 0.26
Body mass (kg) 67.4 10.0 65.2 9.7 64.7 12.8 0.28 0.75
Height (cm) 154.2 6.3 154.1 5.5 154.4 6.0 0.01 0.98
Body mass index (kg/m2) 28.3 4.1 27.5 3.3 27.0 4.8 0.47 0.62
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Table 2 Training loads in kg at first and last week of the resistance training program. Data are
expressed as mean and standard deviation.
Table 3 Participants scores at baseline and after 8 weeks of intervention. Data are expressed as mean and standard deviation.
Table 4 Z-scores of the percentage changes from pre- to post-training period (8 weeks)
according to group in older women. Data are expressed as mean and standard deviation.
Note: TRAP = total radical-trapping antioxidant potential. AOPP = advanced oxidation protein products. FOX
= ferrous oxidation-xylenol orange. NOx = nitric oxide metabolites. * P< 0.05 vs. control.
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