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This article was downloaded by: [Rodrigo Dias]On: 06 October 2011, At: 14:54Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK
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Effects of concurrent training on interleukin-6, tumournecrosis factor-alpha and C-reactive protein in middle-aged menCleiton Augusto Libardi a , Giovana Verginia Souza a , Arthur Fernandes GÁspari a , ClaudineiFerreira Dos Santos a b , Sabrina Toffoli Leite a , Rodrigo Dias c d , Anelena B Frollini d , DiegoTrevisan Brunelli d , Claudia Regina Cavaglieri d , Vera Aparecida Madruga a & Mara P.T.Chacon-Mikahil aa School of Physical Education, University of Campinas – UNICAMP, Campinas, Brazilb Centre of Health Sciences, State University of Northern Paraná – UENP, Jacarezinho, Brazilc School of Physical Education, Herminio Ometto University Centre – UNIARARAS, Araras,Brazild School of Physical Education, Faculty of Health Sciences, Methodist University ofPiracicaba – UNIMEP, Piracicaba, Brazil
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To cite this article: Cleiton Augusto Libardi, Giovana Verginia Souza, Arthur Fernandes GÁspari, Claudinei Ferreira DosSantos, Sabrina Toffoli Leite, Rodrigo Dias, Anelena B Frollini, Diego Trevisan Brunelli, Claudia Regina Cavaglieri, VeraAparecida Madruga & Mara P.T. Chacon-Mikahil (2011): Effects of concurrent training on interleukin-6, tumour necrosis factor-alpha and C-reactive protein in middle-aged men, Journal of Sports Sciences, DOI:10.1080/02640414.2011.609896
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Effects of concurrent training on interleukin-6, tumour necrosisfactor-alpha and C-reactive protein in middle-aged men
CLEITON AUGUSTO LIBARDI1, GIOVANA VERGINIA SOUZA1,
ARTHUR FERNANDES GASPARI1, CLAUDINEI FERREIRA DOS SANTOS1,2,
SABRINA TOFFOLI LEITE1, RODRIGO DIAS3,4, ANELENA B FROLLINI4,
DIEGO TREVISAN BRUNELLI4, CLAUDIA REGINA CAVAGLIERI4,
VERA APARECIDA MADRUGA1 & MARA P. T. CHACON-MIKAHIL1
1School of Physical Education, University of Campinas – UNICAMP, Campinas, Brazil, 2Centre of Health Sciences, State
University of Northern Parana – UENP, Jacarezinho, Brazil, 3School of Physical Education, Herminio Ometto University
Centre – UNIARARAS, Araras, Brazil, and 4School of Physical Education, Faculty of Health Sciences, Methodist University
of Piracicaba – UNIMEP, Piracicaba, Brazil
(Accepted 29 July 2011)
AbstractThe purpose of this study was to evaluate the effects of moderate- to high-intensity resistance and concurrent training oninflammatory biomarkers and functional capacity in sedentary middle-aged healthy men. Participants were selected on arandom basis for resistance training (n¼ 12), concurrent training (n¼ 11) and a control group (n¼ 13). They performedthree weekly sessions for 16 weeks (resistance training: 10 exercises with 36 8–10 repetition maximum; concurrent training:6 exercises with 3 6 8–10 repetition maximum, followed by 30 minutes of walking or running at 55–85% _V O2peak).Maximal strength was tested in bench press and leg press. The peak oxygen uptake ( _V O2peak) was measured by anincremental exercise test. Tumour necrosis factor-a, interleukin-6 and C-reactive protein were determined. The upper- andlower-body maximal strength increase for both resistance (þ42.52%; þ20.9%, respectively) and concurrent training(þ28.35%; þ21.5%, respectively) groups (P¼ 0.0001). _V O2peak increased in concurrent training when comparing pre- andpost-training (P¼ 0.0001; þ15.6%). No differences were found in tumour necrosis factor-a and interleukin-6 for bothgroups after the exercise. C-reactive protein increased in resistance training (P¼ 0.004). These findings demonstrated that16 weeks of moderate- to high-intensity training could improve functional capacity, but did not decrease inflammatorybiomarkers in middle-aged men.
Keywords: Inflammation, systemic biomarkers, resistance training, endurance training
Introduction
Lipoprotein abnormalities, hypertension, and insulin
resistance (associated with metabolic syndrome) are
important and highly prevalent risk factors for the
development of premature coronary heart disease
(Lakka et al., 2002). Several blood biomarkers are
used as indicators of systemic inflammation, includ-
ing interleukin-6, tumour necrosis factor-a and C-
reactive protein (Petersen & Pedersen, 2005). It is
known that high levels of inflammatory markers are
strong predictors of mortality risk in middle-aged
and elderly people (Arsenault, Cartier, Cote, &
Lemieux, 2009; Bruunsgaard, Bjerregaard, Schroll,
& Pedersen, 2004). However, there are, at present,
no known definitive therapies for treating chronic
inflammation.
Regular physical exercise has been shown to
promote anti-inflammatory effects in skeletal muscle
and adipose tissue (Bruunsgaard, 2005). In addition,
it can be used as a therapeutic means to prevent age-
associated degenerative processes as well as the
increase in systemic markers of inflammation (Fer-
rucci et al., 2002; Greiwe, Cheng, Rubin, Yarashes-
ki, & Semenkovich, 2001). However, the effects of
exercise on inflammatory systemic biomarkers are
not clearly understood.
Decreases in tumour necrosis factor-a, interleu-
kin-6 and C-reactive protein levels have been
observed after resistance training (Donges, Duffield,
Correspondence: Cleiton Augusto Libardi, University of Campinas – UNICAMP, School of Physical Education, Campinas, Brazil.
E-mail: [email protected]
Journal of Sports Sciences, 2011; 1–9, iFirst article
ISSN 0264-0414 print/ISSN 1466-447X online � 2011 Taylor & Francis
http://dx.doi.org/10.1080/02640414.2011.609896
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& Drink Water, 2010; Greiwe et al., 2001; Prestes
et al., 2009) and endurance training (Adamopoulos
et al, 2001; Goldhammer et al., 2005; Larsen,
Aukrust, Aarsland, & Dickstein, 2001;). On the
other hand, some studies did not find any reductions
in some of these inflammatory biomarkers after both
these training regimes (Bruunsgaard et al., 2004;
Hammett et al., 2004; White, Castellano, & McCoy,
2006). These differences may be associated with the
type and intensity of training that was conducted.
Several standard positions and guidelines have
proposed exercise programmes that combine both
resistance and endurance training, known as con-
current training, to decrease prevalent risk factors in
the development of coronary heart disease (Chodz-
ko-Zajko et al., 2009; Haskell et al., 2007; Nelson
et al., 2007; Taylor et al., 2004). However, few
studies have investigated the effects of concurrent
training on inflammatory systemic biomarkers. Con-
raads et al., (2002) did not find decreases in tumour
necrosis factor-a and interleukin-6 after 16 weeks of
concurrent training in young, middle-aged and
elderly participants with coronary artery disease. A
similar result was found in C-reactive protein after
home-based concurrent training (Astengo et al.,
2010). It has been suggested that the lack of
reduction in these biomarkers is linked to lower
intensity and non-supervised training.
Therefore, our hypothesis was that resistance and
concurrent training, when the workload is progres-
sively increased and performed with moderate- to
high- intensity, decrease these inflammatory systemic
biomarkers. Thus, the purpose of this study was to
compare 16 weeks of both resistance and concurrent
training, performed with the same weekly frequency
and session length in relation to tumour necrosis
factor-a, interleukin-6, C-reactive protein and func-
tional capacity in middle-age healthy men.
Methods
Participants
Thirty-six inactive males were recruited to partici-
pate in the study. They were randomly assigned to
either a resistance training (n¼ 12), concurrent
training (n¼ 11) or control group (n¼ 13) (Table I).
Before being included in the study, all participants
underwent a thorough physical examination, which
consisted of medical history review, resting and
exercise electrocardiogram (Tavel, 2001) and blood
pressure assessment. Participants had not been
engaging in regular exercise programmes during
the previous 6 months, according to the Baecke
Habitual Physical Activity Questionnaire (Florindo
& Latorre, 2003). The exclusion criteria were; no
regular consumption of medication, acute illness,
severe hypertension, insulin-dependent diabetes
mellitus, metabolic syndrome, orthopaedic limita-
tions, obesity (body mass index 430 kg/m2) and
myocardial infarction. All participants were informed
about the importance of maintaining their previous
nutritional patterns, about the purpose and risks of
the study and signed an informed consent document.
The experimental protocol was approved by The
Research Ethics Committee at the State University of
Campinas, Brazil. A cardiorespiratory test, muscle
strength assessment and measurements of inflam-
matory biomarkers (tumour necrosis factor-a, inter-
leukin-6 and C-reactive protein) were done before
and after the 16 weeks training period.
Blood samples
Blood samples (*10 ml) were obtained from the
antecubital vein in the morning (07:00–09:00 h),
after a 12-hour overnight fast before and after the
experimental period. All blood was collected, pro-
cessed, divided into plasma aliquots, and stored at
7708C for subsequent analysis.
Cytokine measures
Tumour necrosis factor-a, interleukin- 6 and C-
reactive protein were determined in duplicate by
enzyme-linked immunosorbent assay, according to
the specifications of the manufacturer (Quantikine
High Sensitivity Kit, R&D Systems, Minneapolis,
MN). The tumour necrosis factor-a and interleukin-
6 results are presented in picograms per millilitre
(pg � mL71) and C-reactive protein in milligrams
per litre (mg � L71). The sensitivity, intra-assay and
inter-assay were as follows: 0.106 pg � mL71, 4.3%
and 7.3% for tumour necrosis factor-a, 0.039
Table I. Before and after comparison of anthropometric char-
acteristics for resistance training (RT), concurrent training (CT)
and control group (CG).
Variables RT CT CG
Age (years) 48.6+5.0 48.5+5.3 49.1+ 5.5
Height (m) 1.7+0.0 1.7+0.0 1.7+ 0.1
Body mass (kg) Before 82.8+15.1 84.1+8.8 73.3+ 13.3
After 83.1+15.0 83.6+9.0 73.0+ 13.4
D þ0.4 70.6 71.0
BMI (kg � m2) Before 27.5+4.1 28.3+3.0 24.7+ 3.3
After 27.7+3.8 28.1+3.2 24.5+ 3.3
D þ0.9 70.7 71.0
Waist Before 92.6+9.0 94.7+5.0 85.5+ 9.7
circumference After 92.0+10.4 92.6+5.0 85.8+ 10.1
(cm) D 70.7 72.1 þ1.0
Data are shown as mean+SD.
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pg � mL71, 7.8% and 7.2% for interleukin-6 and
0.00001 mg � L71, 3.8% and 7.0% for C-reactive
protein.
Maximal strength assessment
Maximal strength was measured by 1- repetition
maximum test on bench press and leg press exercises
performed using the RIGUETTO1 equipment (Sao
Paulo, SP). Individuals were required to perform
eight repetitions at 50% of 1- repetition maximum,
estimated according to each participant’s capacity, to
rest for 1 min, and then perform a further three
repetitions at 70% of 1- repetition maximum (Braith,
Graves, Leggett, & Pollock, 1993). After a 3-minute
rest, subsequent trials were performed for 1-repeti-
tion with progressively heavier weights until the 1-
repetition maximum was determined within three
attempts, with 3–5 minutes rest between trials.
Standardisation of range of motion and performance
of the exercises was conducted according to Brown
and Weir (2001).
Before the beginning of the study, participants
performed two familiarisation trial sessions com-
posed of two sets of moderate intensity exercises,
with 48h of rest between them. The purpose of this
familiarisation was to reduce learning effects and
establish the reproducibility in the two tests.
Cardiorespiratory test
The cardiorespiratory test was performed at three
points in time: before the beginning of the training
period; after 8 weeks of training to adjust exercise
intensity; and at the end of 16 weeks of training
protocol. The participants performed a maximum
effort protocol in a ‘‘Quinton’’ TM55 treadmill
(Bothell, Washington, EUA), where gas exchange
data were collected continuously using an automated
breath-by-breath metabolic cart (CPX, Medical
Graphics, St. Paul, Minnesota, USA).
The protocol consisted of a 2-minute warm-up at
4 km � h71, followed by increments of 0.3 km � h71
each 30 seconds, and 1% grade (Jones & Doust,
1996) until exhaustion. After this, a 4-minute
recovery period was allowed, with the first minute
at 5 km � h71, with each minute progressively
decreasing (1 km � h71).
The highest 30-second mean value of oxygen
consumption (Heubert et al., 2005) was expressed as
the peak oxygen consumption ( _V O2peak) since a
plateau of _V O2 was not observed during the test in
all cases. Other criteria for _V O2max, established in
the literature [i.e., respiratory exchange ratio 4 1.1
and maximum heart rate (HR) within 10 beats of the
age-appropriate reference value], were met (Howley,
Bassett, & Welch, 1995).
Ventilatory threshold and respiratory compensa-
tion point were detected by visual graphic analysis by
three experienced researchers, familiar with the CPX
Medical Graphics system. The first inflection point
of carbon dioxide output and ventilation, where
there is a loss of linearity of these variables in relation
to linear increment of oxygen consumption ( _V O2)
(Wasserman, Whipp, Koyal, & Beaver, 1973), is
denominated as the ventilatory threshold. The
respiratory compensation point was identified in
duplicate using ventilatory equivalents for oxygen
and carbon dioxide, considering the abrupt rise in
carbon dioxide, according to the criteria proposed by
McLellan (1985).
Training programme
The training programme was composed of two
different protocols: resistance and concurrent train-
ing each one lasting 16 weeks. Participants per-
formed three weekly sessions on alternate days
(Mondays, Wednesdays and Fridays). Before the
training programme, both resistance and concurrent
training groups performed two familiarisation trials
with exercises that were part of the training
programme and muscular strength test.
Resistance training
During the first 8 weeks, participants performed
three lower body exercises (leg press, leg extension
and leg curl) and six upper body exercises (bench
press, lat pulldown, lateral raise, triceps pushdown,
arm curl, basic abdominal crunch). The resistance
training consisted of three sets of 10-repetition
maximum for both upper and lower body, with a
1-minute rest between sets and exercises. Exercises
were maintained after 8 weeks but performed with 8-
repetition maximum with a 1 minute and 30 seconds
rest period (American College of Sports Medicine
[ACSM], 2009). The workloads were adjusted
weekly and participants were encouraged to perform
the greatest number of repetitions they had achieved
in the previous training session when they came to
the last set of each exercise, maintaining the same
range of motion and execution velocity previously
determined. Workloads were increased by 1 kg for
lower body and ½ kg for upper body for each
repetition performed over the established training
protocol, according to the greatest number of
repetitions accomplished by the participants the
previous week.
Concurrent training
Concurrent training protocol was composed of
resistance and endurance training performed in the
Concurrent training and inflammatory markers 3
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same session. In the first 8 weeks there were three
exercises for the lower body (leg press, leg extension
and leg curl) and three exercises for the upper body
(bench press, lat pulldown, arm curl) comprising the
resistance training protocol, consisting of three sets
of 10-repetition maximum with a 1-minute rest, with
the session lasting about 30 minutes (ACSM, 2009).
After this, participants were taken to an athletic
track, where they performed 30 minutes of endur-
ance training, consisting of walking or running with
varying intensity (5 minutes at less than ventilatory
threshold intensity, 10 minutes at ventilatory thresh-
old intensity, 10 minutes above ventilatory threshold
and at less than respiratory compensation point
intensity, 5 minutes at less than ventilatory threshold
intensity), with these intensities corresponding to
50–85% of _V O2peak (ACSM, 1998).
After 8 weeks, the resistance training session was
performed by 8-repetition maximum with a 1 minute
and 30 seconds rest period (ACSM, 2009). In
endurance training the session duration was main-
tained. However, there was an adjustment in the
training zone intensity and time duration (5 minutes
at less than ventilatory threshold intensity, 10
minutes at ventilatory threshold and at less than
respiratory compensation point intensity, 10 minutes
at respiratory compensation point intensity, 5 min-
utes at less than ventilatory threshold intensity). As
for the resistance training, the concurrent training
session duration was about 60 minutes.
Endurance training intensity for ventilatory thresh-
old and respiratory compensation point was con-
trolled by the velocity achieved during the treadmill
test, since it was performed in 1% grades to
reproduce athletic track conditions (Jones & Doust,
1996). The concurrent training load adjustments
were the same as used in the resistance training.
Statistical analysis
Data are presented as means+ standard deviations
(SD). Initially, the Shapiro-Wilk test of normality
and a test of homoscedasticity (Bartlet criteria)
were performed. The training-related effects were
conducted using a 2-way Analysis of Variance
(ANOVA) with repeated measures (group6time).
Tukey’s post hoc test was applied where indicated
by ANOVA. To identify percentage differences
between _V O2peak, 1-repetition maximum leg press
and bench press, the independent samples T-test
was used. Post hoc power analyses were conducted
using G*power (version 3.0.10) (Faul, Erdfelder,
Lang, & Buchner, 2007), using effect size (0.25)
and power set at 80% in the power calculations.
The data were analysed using the Statistica1 6.1
software (StatSoft Inc., Tulsa, OK). The threshold
for significance was set at P5 0.05.
Results
Anthropometric
Repeated measures ANOVA identified no significant
group effects, time and group x time interactions for
body mass (P¼ 0.08; P¼ 0.54; P¼ 0.48 res-
pectively), body mass index (P¼ 0.09; P¼ 0.73;
P¼ 0.29 respectively), and waist circumference
(P¼ 0.08; P¼ 0.07; P¼ 0.09 respectively) (Table I).
Maximal strength
After the training period, significant group effects,
time and group x time interactions in upper-
(P¼ 0.0001) and lower-body (P¼ 0.0001) maximal
strength were detected by ANOVA. Post hoc tests
demonstrated that significant increases were found in
the leg press and bench press maximal strength for
resistance training (þ42.5% and þ20.9% respec-
tively; P¼ 0.0001) and concurrent training (þ28%
and þ21.5% respectively; P¼ 0.0001). There were
no significant differences between these two groups
in the leg press (P¼ 0.19) and bench press (P¼ 0.90)
(Table II). No significant differences were found in
maximal strength after the experimental period for
the control group (P¼ 0.99).
Peak oxygen uptake ( _V O2peak)
Although there was a significant time effect
(P¼ 0.001), there was no observed group effect
(P¼ 0.24), and group x time interaction (P¼ 0.053)
by ANOVA. Post hoc tests demonstrated a significant
increase in _V O2peak (þ15.6%; P¼ 0.01) after 16
weeks for the concurrent training. However, there
were no changes for the resistance training (þ8.3%;
P¼ 0.30) and control group (þ1.5%; P¼ 0.99)
(Table II).
Cytokines and C-reactive protein
Repeated measures ANOVA identified no significant
group effects (P¼ 0.52), time (P¼ 0.89) and group x
time interactions (P¼ 0.83) for tumour necrosis
factor-a after 16 weeks of the resistance training
(3.3+ 1.1 to 3.5+ 1.4 pg � mL71), concurrent
training (2.9+ 1.2 to 2.2+ 0.8 pg � mL71) and
control group (3.3+ 1.0 to 3.1+ 1.3 pg � mL71)
(Figure 1). Similarly, ANOVA identified no signifi-
cant group effects (P¼ 0.20), time (P¼ 0.68) and
group x time interactions (P¼ 0.91) for interleukin-6
after the resistance training (1.0+ 0.5 to 0.88+ 0.4
pg � mL71), concurrent training (0.8+ 0.2 to
0.83+ 0.4 pg � mL71) and control group
(0.7+ 0.1 to 0.9+ 0.5 pg � mL71) (Figure 2).
However, significant group effects (P¼ 0.005) and
a group x time interaction (P¼ 0.004) were observed
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for the C-reactive protein. Post hoc tests demon-
strated a significant increase for resistance training
after 16 weeks training (1.6+ 1.2 mg � L71 to
3.2+ 2.2 mg � L71; P¼ 0.004), but no significant
changes for concurrent training (1.5+ 1.2 to
1.3+ 1.2 mg � L71; P¼ 0.99) and control
group (1.2+ 1.4 to 0.8+ 1.1 mg � L71; P¼ 0.99)
(Figure 3).
Discussion
This is the first study to compare the effects of
concurrent and resistance training on these inflam-
matory markers in healthy middle-aged men. The
main findings of the present study were the increase
in lower and upper body maximal strength for both
groups and the increase in _V O2peak in concurrent
training, as well as the lack of changes in tumour
necrosis factor-a, interleukin-6 and C-reactive
protein.
Tanaka and Swensen (1998) verified that resis-
tance training promotes increased muscle strength
and induces muscle hypertrophy, as measured by an
increased cross-sectional area in all fibre types.
Endurance training increases capillary and mito-
chondrial density, intramuscular substrate storage
and oxidative enzyme activity, while reducing glyco-
lytic enzyme activities (Tanaka & Swensen, 1998).
Moreover, there is a decrease in muscle fibre size, as
well as a negative impact on muscular strength and
power.
The association between endurance and resistance
training, as seen in concurrent training, can promote
gains in muscular strength, related to cardiorespira-
tory fitness (Balabinis, Psarakis, Moukas, Vassiliou,
& Behrakis, 2003; Dolezal & Potteiger, 1998),
besides preventing chronic diseases (Chodzko-Zajko
et al., 2009; Haskell et al., 2007; Nelson et al., 2007;
Taylor et al., 2004). However, studies in young
Table II. Comparisons before and after training for maximal strength (1-RM) and peak oxygen uptake ( _V O2peak) tests for resistance training
(RT), concurrent training (CT) and control group (CG).
Variables RT CT CG
_VO2peak (ml � kg71 � min71) Before 33.0+ 5.0 30.2+5.5 30.9+ 5.3
After 35.4+ 4.6 34.4+5.4* 31.9+ 4.3
D þ8.3 þ15.6{ þ1.5
1-RM Leg press (kg) Before 243.6+ 57.9 219.2+39.3 219.3+ 48.1
After 339.1+ 80.9* 284.3+82.4* 216.0+ 48.1
D þ42.5 þ28.3 71.8{1-RM Bench press (kg) Before 75.5+ 13.9 69.3+9.7 62.9+ 9.9
After 90.0+ 14.8* 84.4+13.5* 61.5+ 10.5
D þ20.9 þ21.5 72.2{
Data are shown as the mean+SD; *Significant within-group difference (P50.05);
{Significant between-group difference (P5 0.05); D, before-after difference.
Figure 1. Plasma tumour necrosis factor-alpha (TNF-a) concen-
tration (pg � mL71). The TNF-a was evaluated before (black
bars), and after 16 weeks of resistance training (RT), concurrent
training (CT) and control group (CG) (white bars). Values are
reported as mean+SD.
Figure 2. Plasma interleukin-6 (IL-6) concentration (pg � mL71).
IL6 was evaluated before (black bars), and after 16 weeks of
resistance training (RT), concurrent training (CT) and control
group (CG) (white bars). Values are reported as mean+SD.
Concurrent training and inflammatory markers 5
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people have revealed a decrease in strength gain
when endurance training is associated with resistance
training (Hickson, 1980; Kraemer et al., 1995). In
the present study, there were no significant differ-
ences in strength gains in either the lower or upper
body. This was probably due to the fact that the
resistance and concurrent training sessions had the
same duration and weekly frequencies, since
Kraemer et al., (1995) and McCarthy Pozniak, and
Agre, (2002) have shown that these variables can be
key for optimising concurrent training adaptations.
Several blood biomarkers are used as indicators of
systemic inflammation, including interleukin-6, tu-
mour necrosis factor-a and C-reactive protein
(Petersen & Pedersen, 2005). In particular, tumour
necrosis factor-a is known to cause increased basal
energy expenditure, anorexia, and loss of muscle and
bone mass in vivo (Reid & Li, 2001) and has been
associated with wasting/cachexia in chronic inflam-
matory disorders (Roubenoff et al., 2002). Consis-
tent with this, muscle protein synthesis was inversely
related to local levels of tumour necrosis factor-aprotein in muscles in a previous study of frail, old
people who also performed resistance training
(Greiwe et al., 2001). Interleukin-6 is a multi-
functional cytokine that plays a pleiotropic role in
immune regulation and inflammation, and its over-
production in older people is associated with
cardiovascular disease, osteoporosis, rheumatoid
arthritis, type II diabetes and Alzheimer’s disease
(Kiecolt-Glaser et al., 2003). Elevated interleukin-6
concentrations are also associated with frailty, a
decline in functional capacity, decreased muscle
strength, and may be used as a predictor of future
disability in older adults (Cohen, Pieper, Harris,
Rao, & Currie, 1997; Ferrucci et al., 2002). The
elevations in interleukin-6 and tumour necrosis
factor-a, stimulators of C-reactive protein released
from hepatocytes, are strongly associated with
increased risk for several diseases (Streetz, Wuste-
feld, Klein, Manns, & Trautwein, 2001). The Center
for Disease Control and the American Heart
Association provide clinical recommendations con-
cluding that individuals with C-reactive protein
values in the upper tertile of the adult population
(43.0 mg � L71) have a twofold increase in cardio-
vascular disease risk compared to those with a C-
reactive protein concentration below 1.0 mg � L71
(Koening et al., 2006; Pearson et al., 2003).
Regular physical exercise can promote anti-in-
flammatory effects in skeletal muscle and adipose
tissue (Bruunsgaard, 2005). Studies have shown
decreases in tumour necrosis factor-a (Phillips,
Flynn, McFarlin, Stewart, & Timmerman, 2010),
interleukin-6 (Prestes et al., 2009) and C-reactive
protein (Olson, Dengel, Leon, & Schmitz, 2007)
after periodised resistance training. On the other
hand, no differences were found in inflammatory
biomarkers after concurrent training (Conraads
et al., 2002; Wong et al., 2008). Recently, elderly
people with cardiovascular disease did not show
changes in interleukin-6 and C-reactive protein after
32 weeks of home-based concurrent training (As-
tengo et al., 2010). These discrepancies in the
inflammatory biomarkers after resistance and con-
current training may be associated with the intensity
of training, since the studies used low intensity or
uncontrolled training.
In the present study, no differences in inflamma-
tory biomarkers were found for either resistance or
concurrent training when performed with moderate-
to high-intensity and increasing workloads during the
protocol. These results may be related to unchanged
body mass, body mass index and waist circumfer-
ence. A systematic review evaluated the loss of
weight, regardless of body region and revealed a
reduction in 0.13 mg � L71 in C-reactive protein for
each 1.0 kg of body mass loss (Selvin, Paynter, &
Erlinger, 2007). A limitation in the present study was
the lack of food intake control before and after the
experimental protocol, which may account for there
being no changes in anthropometric measurements.
According to these findings, it was found that one
year of physical activity, consisting of a combination
of aerobic, strength, balance, and flexibility exercises,
did not promote noticeable decreases in body mass,
C-reactive protein and tumour necrosis factor-a(Beavers et al., 2010). Nicklas et al., (2004) found
decreases in tumour necrosis factor-a, interleukin-6,
C-reactive protein, body mass and body mass index
in obese individuals after 18 months of energy-
restricted diet with or without physical exercise.
Figure 3. C-reactive protein (CRP) concentration (mg � L71).
The CRP was evaluated before (black bars), and after 16 weeks of
resistance training (RT), concurrent training (CT) and control
group (CG) (white bars). *Statistically significant difference
compared with before resistance training (P50.05).
6 C.A. Libardi et al.
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Possibly, exercise interventions effectively improve
chronic inflammation only in association with a
concomitant weight loss.
In the present study, we observed lower values in
inflammatory biomarkers than in obese (body mass
index 430 kg/m2) (Dvorakova-Lorenzova et al.,
2006), cardiac (Conraads et al., 2002) and elderly
individuals (Nicklas et al., 2004) and in people with
multiple sclerosis (White et al., 2006). These
findings may be related to low inflammation status
at baseline, although participants had a body mass
index of 5 30 kg/m2, and did not show associated
pathologies, which may explain the lack of reductions
in the inflammatory biomarkers studied.
We observed a significant increase in C-reactive
protein levels after 16 weeks of resistance training.
According to recently published guidelines (Pearson
et al., 2003), the baseline levels of C-reactive protein
in resistance training were classified as ‘‘moderate
risk’’ and after 16 weeks they were reclassified as
‘‘high risk’’. It is known that C-reactive protein has
an acute phase response after exercise, possibly
maintaining elevated levels for several days after the
last training session (Kasapis & Thompson, 2005).
De Salles et al., (2010) suggest that training
programmes with higher weekly frequencies (six
sessions per week) and maximal training intensity
(100% 1-repetition maximum) may be too stressful
and may result in increased C-reactive protein serum
levels, even in healthy participants. Even with
intensities and weekly frequencies of lower than
those reported by De Salles et al., (2010), the
resistance training proposed in our study could have
caused a stressful factor responsible for increasing C-
reactive protein levels. This is probably associated
with the interval between the last training session and
blood collected after the experimental period, which
was of one week in duration and may be relatively
short for some participants because they show lower
anti-inflammatory response to exercise.
In summary, the present study highlights impor-
tant benefits of resistance and concurrent training
with regard to functional capacity in middle-aged
healthy men. Sixteen weeks of concurrent training
induced an increase in upper- and lower-body
muscle strength, similar to that observed for resis-
tance training, as well as increasing peak oxygen
uptake. However, these results did not support the
idea that moderate- to high-intensity resistance and
concurrent training decrease inflammatory biomar-
kers in healthy middle-aged men.
Acknowledgements
This study was supported by the National Council of
Technological and Scientific Development, Brazil.
References
American College of Sports Medicine. (1998). The recom-
mended quantity and quality of exercise for developing and
maintaining cardiorespiratory and muscular fitness, and
flexibility in healthy adults. Medicine and Science in Sports
and Exercise, 30, 975–991.
American College of Sports Medicine. (2009). Progression models
in resistance training for healthy adults. Medicine and Science in
Sports and Exercise, 41, 687–708.
Adamopoulos, S., Parissis, J., Kroupis, C., Georgiadis, M.,
Karatzas, D., Karavolias, G., et al. (2001). Physical
training reduces peripheral markers of inflammation in
patients with chronic heart failure. European Heart Journal,
22, 791–797.
Arsenault, B.J., Cartier, A., Cote, M., & Lemieux, I. (2009). Body
composition, cardiorespiratory fitness, and low-grade inflam-
mation in middle-aged men and women. The American Journal
of Cardiology, 104, 240–246.
Astengo, M., Dahl, A., Karlsson, T., Mattsson-Hulten, L.,
Wiklund, O., & Wennerblom, B. (2010). Physical training
after percutaneous coronary intervention in patients with stable
angina: Effects on working capacity, metabolism, and markers
of inflammation. European Journal of Cardiovascular Prevention
& Rehabilitation, 17, 349–354.
Balabinis, C.P., Psarakis, C.H., Moukas, M., Vassiliou, M.P., &
Behrakis, P.K. (2003). Early phase changes by concurrent
endurance and strength training. Journal of Strength and
Conditioning Research, 17, 393–401.
Beavers, K.M., Hsu, F., Isom, S. Kritchevsky, S.B., Church, T.,
Goodpaster, B., . . . Nicklas, B.J. (2010). Long-term
physical activity and inflammatory biomarkers in older
adults. Medicine and Science in Sports and Exercise, 42, 2189–
2196.
Braith, R.W., Graves, J.E., Leggett, S.H., & Pollock, M.L. (1993).
Effect of training on the relationship between maximal and
submaximal strength. Medicine and Science in Sports and Exercise,
25, 132–138.
Brown, L.E., & Weir, J.P. (2001). Procedures recommendation I:
Accurate assessment of muscular strength and power. Journal of
Exercise Physiology Online, 4, 1–21.
Bruunsgaard, H. (2005). Physical activity and modulation of
systemic low-level inflammation. Journal of Leukocity Biology,
78, 819–835.
Bruunsgaard, H., Bjerregaard, E., Schroll, M., & Pedersen, B.K.
(2004). Muscle strength after resistance training is inversely
correlated with baseline levels of soluble tumor necrosis factor
receptors in the oldest old. Journal of the American Geriatrics
Society, 52, 237–241.
Chodzko-Zajko, W.J., Proctor, D.N, Fiatarone Singh, M.A.,
Minson, C.T., Nigg, C.R., Salem, G.J., & Skinner, J.S.
(2009). Exercise and physical activity for older adults. Medicine
and Science in Sports and Exercise, 41, 1510–1530.
Cohen, H.J., Pieper, C.F., Harris, T.B., Rao, K.M., & Currie,
M.S. (1997). The association of plasma interleukin-6 levels
with functional disability in community-dwelling elderly.
Journals of Gerontology A: Biological Sciences and Medical Sciences,
52, 201–208.
Conraads, V.M., Beckers, P., Bosmans, J., De Clerck, L.S.,
Stevens, W.J., Vrints, C.J., & Brutsaert, D.L. (2002). Com-
bined endurance/ resistance training reduces plasma tumor
necrosis factor-a receptor levels in patients with chronic heart
failure and coronary artery disease. European Heart Journal, 23,
1854–1860.
De Salles, B.F., Simao, R., Fleck, S.J., Dias, I., Kraemer-Aguiar,
L.G., & Bouskela E. (2010). Effects of resistance training
on cytokines. International Journal of Sports Medicine, 31, 441–
500.
Concurrent training and inflammatory markers 7
Dow
nloa
ded
by [
Rod
rigo
Dia
s] a
t 14:
54 0
6 O
ctob
er 2
011
Dolezal, B.A., & Potteiger J.A. (1998). Concurrent resistance and
endurance training influence basal metabolic rate in nondieting
individuals. Journal of Applied Physiology, 85, 695–700.
Donges, C.E., Duffield, R., & Drink Water, E.J. (2010). Effects of
resistance or aerobic exercise training in interleukin-6, C-reactive
protein and body composition. Medicine and Science in Sports and
Exercise, 42, 304–313.
Dvorakova-Lorenzova, A., Suchanek, P., Havel, P.J., Stavek, P.,
Karasova, L., Valenta, Z., . . . Poledne, D.L. (2006). The
decrease in C-reactive protein concentration after diet and
physical activity induced weight reduction is associated with
changes in plasma lipids, but not interleukin-6 or adiponectin.
Metabolism, 55, 359–365.
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007).
G*Power 3: A flexible statistical power analysis program for the
social, behavioral, and biomedical sciences. Behavior Research
Methods, 39, 175–191.
Ferrucci, L., Penninx, B.W.J., Volpato, S., Harris, T.B., Bandeen-
Roche, K., Balfour, J., . . . Guralnik, J.M. (2002). Change in
muscle strength explains accelerated decline of physical
function in older women with high interleukin-6 serum levels.
Journal of the American Geriatrics Society, 50, 1947–1954.
Florindo, A.A., & Latorre, M.R.D.O. (2003). Validacao e
reprodutibilidade do questionario de Baecke de avaliacao da
atividade fısica habitual em homens adultos. Revista Brasileira
de Medicina do Esporte, 9, 121–128.
Goldhammer, E., Tanchilevitch, A., Maor I., Beniamini, Y.,
Rosenschein, U., & Sagiv, M. (2005). Exercise training
modulates cytokines activity in coronary heart disease patients.
International Journal of Cardiology, 100, 93–99.
Greiwe, J.S., Cheng, B.O., Rubin, D.C., Yarasheski, K.E., &
Semenkovich, C.F. (2001). Resistance exercise decreases
skeletal muscle tumor necrosis factor a in frail elderly humans.
FASEB Journal, 15, 475–482.
Hammett, C.J.K., Oxenham, H.C., Baldi, J.C, Doughty, R.N.,
Ameratunga, R., French, J.K., . . . Stewart, R.A. (2004). Effect of
six months’ exercise training on C-reactive protein levels in healthy
elderly subjects. Journal of the American College of Cardiology, 44,
2411–2413.
Haskell, W.L., Lee, I.-M., Pate, R.R., Powell, K.E., Blair, S.N.,
Franklin, B.A., . . . Bauman, A. (2007). Physical activity and
public health: Updated recommendation for adults from the
American College of Sports Medicine and the American Heart
Association. Medicine and Science in Sports and Exercise, 39,
1425–1434.
Heubert, R.A., Billat, V.L., Chassaing, P., Bocquet, V., Morton,
R.H., Koralsztein, J.P., & Di Prampero, P.E. (2005). Effect of a
previous sprint on the parameters of the work-time to exhaustion
relationship in high intensity cycling. International Journal of Sports
Medicine, 26, 583–592.
Hickson, R.C. (1980). Interference of strength development by
simultaneously training for strength and endurance. European
Journal of Applied Physiology, 45, 255–263.
Howley, E.T., Bassett, D.R., JR., & Welch, H.G (1995). Criteria
for maximal oxygen uptake: Review and commentary. Medicine
and Science in Sports and Exercise, 27, 1292–1301.
Jones, A.M., & Doust, J.H. (1996). A 1% treadmill grade most
accurately reflects the energetic cost of outdoor running.
Journal of Sports Science, 14, 321–327.
Kasapis, C., & Thompson, P.D. (2005). The effects of physical
activity on serum C-reactive protein and inflammatory markers:
A systematic review. Journal of the American College of
Cardiology, 45, 1563–1569.
Kiecolt-Glaser, J.K., Preacher, K.J., MacCallum, R.C.,
Atkinson, C., Malarkey, W.B., & Glaser, R. (2003). Chronic
stress and age-related increases in the proinflammatory cytokine
IL-6. Proceedings of the National Academy of Sciences USA, 100,
9090–9095.
Koenig, W., Khuseyinova, N., Baumert, J., Thorand, B., Loewel,
H., Chambless, L. (2006). Increased concentrations of C-
reactive protein and IL-6 but not IL-18 are independently
associated with incident coronary events in middle-aged men
and women: Results from the MONICA/KORA Augsburg
case-cohort study, 1984–2002. Arteriosclerosis, Thrombosis, and
Vascular Biology, 26, 2745–2751.
Kraemer, W.J., Patton, J., Gordon, S.E., Harman, E.A.,
Deschenes, M.R., Reynolds, K., . . . Dziados, J.E., (1995).
Compatibility of high intensity strength and endurance training
on hormonal and skeletal muscle adaptations. Journal of Applied
Physiology, 78, 976–989.
Lakka, H.M., Laaksonen, D.E., Lakka, T.A., Niskanen, L.K.,
Kumpusalo, E., Tuomilehto, J., & Salonen, J.T. (2002). The
metabolic syndrome and total and cardiovascular disease
mortality in middle-aged men. The Journal of the American
Medical Association, 288, 2709–2716.
Larsen, A.I., Aukrust, P., Aarsland, T., & Dickstein, K. (2001).
Effect of aerobic exercise training on plasma levels of tumor
necrosis factor-a in patients with heart failure. The American
Journal of Cardiology, 88, 805–808.
McCarthy, J.P., Pozniak, M.A., & Agre J.C. (2002). Neuromus-
cular adaptations to concurrent strength and endurance training.
Medicine and Science in Sports and Exercise, 34, 511–519.
McLellan, T.M. (1985). Ventilatory and plasma lactate response
with different exercise protocols: A comparison of methods.
International Journal of Sports Medicine, 6, 30–35.
Nelson, M.E., Rejesk, W.J., Blair, S.N., Duncan, P.W., Judge,
J.O., King, A.C., . . . Castaneda-Sceppa, C. (2007). Physical
activity and public health in older adults: Recommendation
from the American College of Sports Medicine and the
American Heart Association. Medicine and Science in Sports
and Exercise, 39, 1435–1445.
Nicklas, B.J., Ambrosius, W., Messier, S.P., Miller, G.D.,
Penninx, B.W.J.H., Loeser, R.F.. & Pahor, M. (2004). Diet-
induced weight loss, exercise, and chronic inflammation in
older, obese adults: A randomized controlled clinical trial.
American Journal of Clinical Nutrition, 79, 544–551.
Olson, T.P., Dengel, D.R., Leon, A.S., & Schmitz, K.H. (2007).
Changes in inflammatory biomarkers following one-year of
moderate resistance training in overweight women. International
Journal of Obesity (Lond), 31, 996–1003.
Pearson, T.A., Mensah, G.A., Alexander, R.W., Anderson, J.L.,
Cannon, R.O., Criqui, M., . . . Vinicor, F. (2003). Markers of
inflammation and cardiovascular disease: Application to clinical
and public health practice: A statement for healthcare pro-
fessionals from the Centers for Disease Control and Preven-
tion and the American Heart Association. Circulation, 107, 499–
511.
Petersen, A.M., & Pedersen, B.K. (2005). The anti-inflammatory
effect of exercise. Journal of Applied Physiology, 98, 1154–1162.
Phillips, M.D., Flynn, M.G., McFarlin, B.K., Stewart, L.K., &
Timmerman, K.L. (2010). Resistance training at eight-repeti-
tion maximum reduces the inflammatory milieu in elderly
women. Medicine and Science in Sports and Exercise, 42, 314–
325.
Prestes, J., Shiguemoto, G., Botero, J.P., Frollini, A., Dias, R.,
Leite, R., . . . Perez, S. (2009). Effects of resistance training on
resistin, leptin, cytokines, and muscle force in elderly post-
menopausal women. Journal of Sports Sciences, 27, 1607–1615.
Reid, M.B., & Li, Y.P. (2001). Tumor necrosis factor-alpha and
muscle wasting: A cellular perspective. Respiratory Research, 2,
269–272.
Roubenoff, R., Grinspoon, S., Skolnik, P.R., Tchetgen, E., Abad,
L., Spiegelman, D., . . . Gorbach, S. (2002). Role of cytokines
and testosterone in regulating lean body mass and resting
energy expenditure in HIV-infected men. American Journal of
Physiology - Endocrinology and Metabolism, 283, E138–E145.
8 C.A. Libardi et al.
Dow
nloa
ded
by [
Rod
rigo
Dia
s] a
t 14:
54 0
6 O
ctob
er 2
011
Selvin, E., Paynter, N.P., & Erlinger, T.P. (2007). The effect of
weight loss on C-reactive protein: A systematic review. Archives
of Internal Medicine, 167, 31–39.
Streetz, K.L., Wustefeld, T., Klein, C., Manns, M.P., &
Trautwein, C. (2001). Mediators of inflammation and acute
phase response in the liver. Cellular and Molecular Biology
(Noisy-legrand), 47, 661–673.
Tanaka, H., & Swensen, T. (1998). Impact of resistance training
on endurance performance a new form of cross-training? Sports
Medicine, 25, 191–200.
Tavel, M.E. (2001). Stress testing in cardiac evaluation: Current
concepts with emphasis on the ECG. Chest, 119, 907–925.
Taylor, A.H., Cable, N.T., Faulkner, G., Hillsdon, M., Narici,
M., & Van Der Bij, A.K. (2004). Physical activity and older
adults: A review of health benefits and the effectiveness of
interventions. Journal of Sports Sciences, 22, 703–725.
Wasserman, K., Whipp, B.J., Koyal, S.N., & Beaver, W.L. (1973).
Anaerobic threshold and respiratory gas exchange during
exercise. Journal of Applied Physiology, 35, 236–243.
White, L.J., Castellano. V., & McCoy, S.C. (2006). Cytokine
responses to resistance training in people with multiple
sclerosis. Journal of Sports Science, 24, 911–914.
Wong, P.C., Chia, M.Y., Tsou, I.Y., Wansaicheong, G.K., Tan,
B., Wang, J.C., . . . Lim, D. (2008). Effects of a 12-week
exercise training programme on aerobic fitness, body composi-
tion, blood lipids and C-reactive protein in adolescents with
obesity. Annals Academy of Medicine Singapore, 37, 286–293.
Concurrent training and inflammatory markers 9
Dow
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Rod
rigo
Dia
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011