Effects of concurrent training on interleukin-6, tumour necrosis factor-alpha and C-reactive protein...

10
This article was downloaded by: [Rodrigo Dias] On: 06 October 2011, At: 14:54 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Sports Sciences Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rjsp20 Effects of concurrent training on interleukin-6, tumour necrosis factor-alpha and C-reactive protein in middle- aged men Cleiton Augusto Libardi a , Giovana Verginia Souza a , Arthur Fernandes GÁspari a , Claudinei Ferreira Dos Santos a b , Sabrina Toffoli Leite a , Rodrigo Dias c d , Anelena B Frollini d , Diego Trevisan Brunelli d , Claudia Regina Cavaglieri d , Vera Aparecida Madruga a & Mara P.T. Chacon-Mikahil a a School of Physical Education, University of Campinas – UNICAMP, Campinas, Brazil b Centre of Health Sciences, State University of Northern Paraná – UENP, Jacarezinho, Brazil c School of Physical Education, Herminio Ometto University Centre – UNIARARAS, Araras, Brazil d School of Physical Education, Faculty of Health Sciences, Methodist University of Piracicaba – UNIMEP, Piracicaba, Brazil Available online: 21 Sep 2011 To cite this article: Cleiton Augusto Libardi, Giovana Verginia Souza, Arthur Fernandes GÁspari, Claudinei Ferreira Dos Santos, Sabrina Toffoli Leite, Rodrigo Dias, Anelena B Frollini, Diego Trevisan Brunelli, Claudia Regina Cavaglieri, Vera Aparecida 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 To link to this article: http://dx.doi.org/10.1080/02640414.2011.609896 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.

Transcript of Effects of concurrent training on interleukin-6, tumour necrosis factor-alpha and C-reactive protein...

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

Journal of Sports SciencesPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/rjsp20

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

Available online: 21 Sep 2011

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

To link to this article: http://dx.doi.org/10.1080/02640414.2011.609896

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.

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

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

& 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.

2 C.A. Libardi et al.

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

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

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

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

4 C.A. Libardi et al.

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

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

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

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.

Dow

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011

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

nloa

ded

by [

Rod

rigo

Dia

s] a

t 14:

54 0

6 O

ctob

er 2

011