Effect of Resistance Training Systems on Oxidative Stress in Older Women

“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.

Note: This article will be published in a forthcoming issue of the International Journal of Sport Nutrition and Exercise Metabolism. This article appears here in its accepted, peerreviewed form; it has not been copyedited, proofed, or formatted by the publisher. Section: Original Research Article Title: Effect of Resistance Training Systems on Oxidative Stress in Older Women Authors: Alex S. Ribeiro1,2, Rafael Deminice2, Brad J. Schoenfeld3, Crisieli M. Tomeleri2, Camila S. Padilha2, Danielle Venturini4, Décio S. Barbosa4, Luís B. Sardinha5, and Edilson S. Cyrino2 Affiliations: 1Center for Research in Health Sciences. University of Northern Paraná, Londrina, Brazil. 2Metabolism, Nutrition, and Exercise Laboratory. Londrina State University. Londrina, Brazil. 3Exercise Science Department, CUNY Lehman College, Bronx, New York. 4Clinical Analyses Laboratory. Londrina State University, Londrina, Brazil. 5 Exercise and Health Laboratory, CIPER, Faculty of Human Kinetics, Universidade de Lisboa, Lisbon, Portugal. Running Head: Resistance training and oxidative stress Journal: International Journal of Sport Nutrition and Exercise Acceptance Date: April 7, 2017 ©2017 Human Kinetics, Inc.

DOI: https://doi.org/10.1123/ijsnem.2016-0322


Effect of resistance training systems on oxidative stress in older women

Running head: Resistance training and oxidative stress

Alex S. Ribeiro 1,2, Rafael Deminice 2, Brad J. Schoenfeld 3, Crisieli M. Tomeleri 2, Camila S.

Downloaded by New York University on 04/20/17, Volume 0, Article Number 0

Padilha 2, Danielle Venturini 4, Décio S. Barbosa 4, Luís B. Sardinha 5, Edilson S. Cyrino 2

1

Center for Research in Health Sciences. University of Northern Paraná, 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; Zip

code:

86210-000;

[email protected]

Phone:

+554391523899;

+554332593860;

e-mail:

alex-


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 (67.9±5.0 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 upregulation of the antioxidant system as evidenced by higher (P<0.05) values of total radicaltrapping antioxidant parameter plasma concentration after intervention (TD= 930.4±160.0 µmolTrolox®, PR= 977.8±145.2 µmolTrolox®, CG= 794.4±130.2 µmolTrolox®). For the protein oxidation adducts, TD and PR presented lower (P<0.05) scores compared to CG (TD= 91.2±25.0 µmol/L, PR= 93.0±30.3 µmol/L, CG= 111.0±20.4 µmol/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 promotes an improvement in markers of oxidative stress in older women independent of the load-management RT system. Keywords: strength training, TRAP, AOPP, NOx, FOX.


Introduction Oxidative stress (OS) is characterized by an imbalance between production of reactive oxygen and nitrogen species (RONS) and the body’s antioxidant defense, where the production of RONS exceeds the body’s 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 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 overproduction, which may considerably increase endothelial dysfunction vulnerability 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 maximize exercise-induced benefits.


Among the different RT systems, the pyramid approach is a well-established system 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 on OS parameters induced by RT may be dependent on the specific characteristics of the program, such as manipulation of training volume and intensity (Bloomer, 2008; Çakir-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 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 number of repetitions, permits exercise performance at higher absolute workloads without a substantial reduction in training volume, thus resulting in higher mechanical stresses. Hypothetically, this may stimulate different metabolic pathways of RONS production. It is therefore conceivable that the pyramid system may induce differential chronic adaptations on OS compared to traditional RT. Therefore, the purpose of the present randomized controlled trial was to investigate the effect of RT performed with a traditional versus pyramid system on OS biomarkers in older women. Based on the aforementioned information, we hypothesized that RT performed in both systems would induce improvement on OS modulation and this adaptation on OS biomarkers would be different between RT systems. 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


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 electrocardiogram reviewed by a cardiologist and were released with no restrictions for participation in this study.


Ninety older women were assessed for eligibility. After individual interviews, 23 were 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 recruitment and allocation. 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


measurements were performed at weeks 1-2, and 11-12. A supervised progressive RT was performed between weeks 3-10. Oxidative stress measurements 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 -70ºC until assayed.


Advanced oxidation protein products (AOPP) were determined in the plasma using a semiautomatic method described by Witko-Sarsat et al. (Witko-Sarsat et al., 1996). AOPP concentrations were expressed as micromoles per liter (µmol/L) of chloramines-T equivalents. Total radical-trapping antioxidant parameter (TRAP) was determined as reported by Repetto et al. (Repetto et al., 1996). This method detects hydrosoluble and/or liposoluble plasma antioxidants by measuring the chemiluminescence inhibition time induced by 2,2-azobis (2amidinopropane). The system was calibrated with the vitamin E analog TROLOX ®, and the values of TRAP are expressed in equivalent of μmol of Trolox ®. Plasma lipidhydroperoxides levels were determined by ferrous oxidation-xylenol orange (FOX) assay (Nourooz-Zadeh et 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 Zscore) + (-1 x FOX Z-score) + (NOx Z-score) / 4.


Resistance training program Supervised RT was performed during the morning hours in the University facilities. The protocol was based on recommendations for RT in an older population to improve 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 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 weights), leg curl, triceps pushdown, and seated calf raise. 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 failure or an inability to sustain exercise performance with proper exercise technique. Participants were instructed to inhale during the eccentric phase and exhale during the concentric phase while maintaining a constant velocity of movement at a ratio of approximately 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 subject’s 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


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


the weekly training load in kilograms. Statistical analysis 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, Fisher’s post hoc test was employed to identify the mean differences. Baseline comparisons between groups were explored with oneway analysis of variance. The effect size (ES) was calculated as post-training mean minus pretraining 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 STATISTICA software version 10.0 (Statsoft Inc., Tulsa, Ok, USA). Results The anthropometric characteristics of the participants at baseline are presented in Table 1. There was no significant statistical difference among groups.


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. Table 3 indicates the OS biomarkers values at pre- and post-intervention period 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 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 comparison to CG (composed Z-score: TD = 0.08 ± 0.32; PR = 0.14 ± 0.39; CG = -0.20 ± 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 differential changes in OS markers; this hypothesis was refuted since no difference in OS


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 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 determine if training over a spectrum of loads differentially influences OS. Although we did not observe any difference between systems, the RT induced a positive improvement on OS. The overall changes induced by RT in OS were expressed by percentage 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 inferences of the intervention as a whole as opposed to isolated outcomes. In this investigation we 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.


The physiological mechanisms by which RT improves OS may be attributed to some 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 inflammatory factors that contribute to the production of reactive oxygen species in 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 defense capacity. We observed that RT was effective in maintaining the body’s antioxidant 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 mechanism to support such a contention, it is logical to speculate that differences between 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 timedependent, protocol-dependent, and/or simply an effect of the individual responsiveness to training without direct mechanistic investigation. Taken together these results allow us to hypothesize that RT may induce improvements in OS by different mechanisms. This hypothesis warrants investigation in future studies with different combinations of volume and intensity.


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 after a 6-week RT program. Alternatively, other investigations have observed increases in NO levels following regimented RT (Maeda et al., 2006; Maiorana et al., 2003). The reason for these conflicting results are not apparent at this time. 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


physically independent older women. Moreover, endogenous antioxidants such as catalase, 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 subject’s 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 Our results suggest that 8 weeks of progressive RT promotes an improvement on OS in 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


prescription, and the physiological mechanisms related to improvement of oxidative stress


induced by RT.


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Figure 1. Flowchart of the study.



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.



Table 1 General characteristics of the sample at baseline. Data are expressed as mean and standard deviation. Traditional

Pyramid

Control

F

P

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

Table 2 Training loads in kg at first and last week of the resistance training program. Data are expressed as mean and standard deviation. Traditional

Pyramid

Effects

F

P

Week 1

1196.5 ± 128.8

1324.9 ± 114.1§

Group

3.84

0.05

Week 8

1827.6 ± 212.4*

1949.1 ± 250.8*§

Time

391.05

< 0.001

Δ%

52.7

47.1

Interaction

2.29

0.11

Effect size

3.70

3.42

Note: * P< 0.05 vs. pre-training. §P< vs. traditional group.


Table 3 Participants’ scores at baseline and after 8 weeks of intervention. Data are expressed as mean and standard deviation. Effects

SP (ƞ2p)

P

933.2 ± 165.2 961.7 ± 111.9 943.2 ± 140.0 930.4 ± 160.0§ 977.8 ± 145.2§ 794.4 ± 130.2* -0.3 1.7 -15.8 -0.02 0.13 -1.10

Group Time Interaction

0.55 (0.09) 0.83 (0.13) 0.99 (0.29)

0.06 < 0.01 < 0.001

105.2 ± 39.5 91.2 ± 25.0*§ -13.3 -0.43

108.3 ± 37.2 93.0 ± 30.3*§ -14.1 -0.45

96.2 ± 15.8 111.0 ± 20.4* 15.4 0.82


0.08 (< 0.01) 0.18 (0.02) 0.76 (0.14)

0.77 0.29 0.01

0.64 ± 0.2 0.66 ± 0.2 3.1 0.10

0.71 ± 0.3 0.81 ± 0.2 14.1 0.40

0.65 ± 0.3 0.60 ± 0.1 -7.7 -0.25


0.44 (0.07) 0.08 (< 0.01) 0.20 (0.03)

0.11 0.55 0.40

7.06 ± 2.9 6.08 ± 3.4 -13.9 -0.31

6.86 ± 3.2 6.60 ± 2.8 -3.8 -0.09

7.24 ± 3.6 8.6 ± 4.9 18.8 0.32


0.32 (0.05) 0.05 (< 0.01) 0.27 (0.04)

0.21 0.92 0.28


Traditional TRAP (µmolTrolox®) Pre Post Δ% Effect size AOPP (µmol/L) Pre Post Δ% Effect size FOX (mmol/L) Pre Post Δ% Effect size NOx (µmol/L) Pre Post Δ% Effect size

Pyramid

Control

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. pre-training. §P< vs. control group. SP = statistical power. ƞ 2p = partial eta-squared.


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. Traditional

Pyramid

Control

P

TRAP

0.34 ± 0.68*

0.50 ± 1.1*

-0.73 ± 0.59

< 0.001

AOPP

-0.23 ± 0.91*

-0.36 ± 0.80*

0.63 ± 1.01

< 0.01

FOX

-0.03 ± 1.10

0.18 ± 1.02

-0.15 ± 0.86

0.57

NOx

-0.25 ± 0.62

-0.11 ± 0.53

0.39± 1.49

0.10


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.

Effect of Resistance Training Systems on Oxidative Stress in Older Women

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