Dissociated time course recovery between rate of force development and peak torque after eccentric...

Dissociated time course recovery between rate of forcedevelopment and peak torque after eccentric exerciseRenato Molina1,2 and Benedito S. Denadai1

1Human Performance Laboratory, Sao Paulo State University, UNESP, Rio Claro and 2Physical Education Department, Air Force Academy, Pirassununga, SP, Brazil

CorrespondenceBenedito S. Denadai, Human Performance

Laboratory, UNESP, Av. 24A, 1515, Bela Vista,

CEP 13506-900, Rio Claro, SP, Brazil

E-mail: [email protected]

Accepted for publicationReceived 29 September 2011;

accepted 8 November 2011

Key wordscreatine kinase; delayed-onset muscle soreness;

exercise-induced muscle damage; power; strength

Summary

This study investigated the association between Isokinetic peak torque (PT) ofquadriceps and the corresponding peak rate of force development (peak RFD)during the recovery of eccentric exercise. Twelve untrained men (aged21Æ7 ± 2Æ3 year) performed 100 maximal eccentric contractions for knee extensors(10 sets of 10 repetitions with a 2-min rest between each set) on isokineticdynamometer. PT and peak RFD accessed by maximal isokinetic knee concentriccontractions at 60� s)1 were obtained before (baseline) and at 24 and 48 h aftereccentric exercise. Indirect markers of muscle damage included delayed onset ofmuscle soreness (DOMS) and plasma creatine kinase (CK) activity. The eccentricexercise resulted in elevated DOMS and CK compared with baseline values. At 24 h,PT ()15Æ3%, P = 0Æ002) and peak RFD ()13Æ1%, P = 0Æ03) decreased significantly.At 48 h, PT ()7Æ9%, P = 0Æ002) was still decreased but peak RFD have returned tobaseline values. Positive correlation was found between PT and peak RFD at baseline(r = 0Æ62, P = 0Æ02), 24 h (r = 0Æ99, P = 0Æ0001) and 48 h (r = 0Æ68, P = 0Æ01)after eccentric exercise. The magnitude of changes (%) in PT and peak RFD frombaseline to 24 h (r = 0Æ68, P = 0Æ01) and from 24 to 48 h (r = 0Æ68, P = 0Æ01)were significantly correlated. It can be concluded that the muscle damage induced bythe eccentric exercise affects differently the time course of PT and peak RFD recoveryduring isokinetic concentric contraction at 60� s)1. During the recovery fromexercise-induced muscle damage, PT and peak RFD are determined but not fullydefined by shared putative physiological mechanisms.

Introduction

Typically, maximal force occurs after 300 ms from the onset of

maximal isometric voluntary contraction (MVC) (Aagaard et al.,

2002). However, fast and forceful muscle contraction during

explosive-type sports (e.g. jumping and sprint running)

involves contractions times between 50 and 250 ms (Aagaard

et al., 2002; Andersen & Aagaard, 2006). Therefore, time spans

involved in the explosive movements may not allow maximal

muscle force to be reached. In this case, the best functional

analysis is the rate of rise in muscle force at the onset of

contraction [i.e. rate of force development (RFD)] determined

under isometric (Aagaard et al., 2002; Andersen & Aagaard,

2006) and isokinetic conditions (Connelly & Vandervoort,

2000; Miller et al., 2006; Oliveira et al., 2010).

Some studies have found a positive correlation between RFD

and maximal force (Mirkov et al., 2004), especially the RFD

recorded in the later phase (more than 100 ms relative to the

onset of contraction) of the MVC (Andersen & Aagaard, 2006).

In addition, concomitant increases in maximal force and RFD

have been observed (Aagaard et al., 2002), which could be

attributed to shared putative mechanisms [e.g. discharge

doublets (Miller et al., 1981)] underlying maximal force ⁄ RFD

changes with resistance training. However, other researches

using different experimental designs (resistance training and

verbal instructions during protocol) have questioned whether a

direct relationship between maximal force and RFD exists

(Griffin & Cafarelli, 2005; Holtermann et al., 2007).

It is well documented that eccentric muscle actions are

associated with muscle damage (Clarkson, 1992, Byrne et al.,

2004; Racinais et al., 2008). Warren et al. (1999) have suggested

that the measures of mechanical muscle function [e.g. peak

torque (PT)] provide the most effective means of evaluating the

magnitude and time course of damage induced by eccentric

muscle actions. Recently, Racinais et al. (2008) have shown

acute PT loss after exercise-induced muscle damage, which was

partly attributed to an alteration in contractile properties ()23%

in electrically evoked mechanical twitch). However, PT failed to

Clin Physiol Funct Imaging (2012) 32, pp179–184 doi: 10.1111/j.1475-097X.2011.01074.x

� 2011 The AuthorsClinical Physiology and Functional Imaging � 2011 Scandinavian Society of Clinical Physiology and Nuclear Medicine 32, 3, 179–184 179

recover before the third day, while contractile properties had

completely recovered. Intrinsic muscle contractile properties

have been considered important for RFD, especially in the early

contraction phase (<100 ms) (Andersen & Aagaard, 2006).

These data highlight the possibility that the mechanisms

underlying PT and RFD may not be the same, supporting the

hypothesis proposed by Holtermann et al. (2007). To our

knowledge, no studies have analysed the relationship between

PT and RFD during recovery from exercise-induced muscle

damage.

Therefore, the purposes of the present study were twofold (i)

to describe the effect of maximal isokinetic eccentric exercise on

PT and RFD, and (ii) to compare and to correlate the magnitude

of changes in PT and RFD during recovery from exercise-

induced muscle damage. It is hypothesized that f PT and RFD are

mediated by similar physiological factors, PT will be as affected

as RFD by the exercise-induced damage. Moreover, the

magnitude of changes in PT and RFD will be correlated.

Methods

Subjects

Twelve male students (21Æ7 ± 2Æ3 years, 72Æ8 ± 9Æ8 kg,

175Æ4 ± 5Æ6 cm) who were physically active but none took

part in any regular physical exercise or sport programme

volunteered for the study. All subjects were healthy and free of

cardiovascular, respiratory and neuromuscular disease. All risks

associated with the experimental procedures were explained

prior to involvement in the study, and each participant

completed a written informed consent. The experiments were

conducted according to the Helsinki Declaration and approved

by the Institutional Review Board of the university.

Experimental design

Participants visited the laboratory for five times. During the first

visit, each participant was required to attend laboratory

familiarizations to lessen any effect of learning during

subsequent strength testing. In this session, they performed

one set of five-maximal concentric isokinetic knee extensions at

60�.s)1. In the second visit, indirect markers of muscle damage

[delayed onset of muscle soreness (DOMS), and plasma creatine

kinase activity (CK)] and neuromuscular variables (PT and RFD)

were determined. In the third visit, subjects performed the

eccentric exercise protocol. After 24 and 48 h of this session,

they returned to the laboratory to determine indirect markers of

muscle damage and neuromuscular variables. Figure 1 presents

an overview of the experimental design.

Testing procedures

A System 3 Biodex isokinetic dynamometer (Biodex Medical

Systems Inc., Shirley, NY, USA) and computer software were

used to measure the PT. Subjects were placed in a sitting

position and securely strapped to the test chair. Excessive

movement of the upper body was limited by two cross-over

shoulder harnesses and an abdominal belt. The trunk ⁄ thigh

angle was 95�. The axis of the dynamometer was aligned to

right knee �flexion–extension� axis, and the lever arm was

attached to the shank using a strap. The subject was asked to

relax their leg so that passive determination of the effects of

gravity on the limb and lever arm could be carried out. Ninety

degrees of knee flexion was measured manually using a

goniometer, and the range of motion (ROM) determined was

70� [from 90� to 20� knee flexion (0� = full extension)].

Subjects were instructed react to an audible signal generated by

the dynamometer to start isokinetic measurements. They were

asked to push the lever up as hard and fast as possible for knee

extensions.

Peak torque and total work measurements

The isokinetic data (PT, PT angle, PT time and work) were

analysed using specific algorithms created in MatLab environ-

ment (The MathWorks, Natick, MA, USA). Torque curves were

smoothed using a 10-Hz Butterworth fourth-order zero-lag

filters. After this, the contraction with the highest PT produced

1st visit 2nd visit 3rd visit 4th visit 5th visit

Eccentric exercise protocol

Familiarization

Baseline data collection

Data collection 24 h post eccentricexercise

Data collection 48 h post eccentricexerciseexercise exercise

24–48 h 48–72 h 24 h

48 hFigure 1 Schematic representation of theexperimental design.

Muscle damage and power, R. Molina and B. S. Denadai

� 2011 The AuthorsClinical Physiology and Functional Imaging � 2011 Scandinavian Society of Clinical Physiology and Nuclear Medicine 32, 3, 179–184

180

from three individual efforts was considered for further analysis.

The PT was taken in an averaged window of 10� around the PT.

In addition to the PT, other variables were also calculated during

this contraction: angle (PT angle) and time at which PT was

attained (PT time), and total work (area under the torque curve

during the whole contraction).

Rate of force development

The calculation of RFD was according to previous studies

(Aagaard et al., 2002; Oliveira et al., 2010), allowing for the

calculation of the maximal force development during the

contraction. Throughout the contraction, the RFD was derived

as the average slope of the moment–time curve (Dtorque ⁄ D-time) over time. The peak RFD was defined as the peak

Dtorque ⁄ Dtime over time achieved during the isokinetic

contraction (Oliveira et al., 2010). Onset of muscle contraction

was defined as the time point at which the moment

curve exceeded baseline moment by >7Æ5 Nm (Aagaard et al.,

2002).

Eccentric exercise

In the third visit, the eccentric exercise protocol was performed.

Each participant performed 100 maximal isokinetic (10 sets of

10 repetitions with a 2-min rest between each set) ⁄ eccentric

contractions for knee extensors of dominant leg at 60� s)1

(Paschalis et al., 2005). Participants exercised in the seat position

through a 70� range of motion from 160� extension to 90� knee

flexion. Each eccentric action of knee was followed by a passive

return to the start angle. Participants were instructed to resist

Table 1 Mechanical muscle function during maximal concentricisokinetic test at baseline and at 24 and 48 h after eccentric exerciseprotocol. N = 12.

Baseline 24 h 48 h

PT (Nm) 236Æ2 ± 50Æ9 200Æ0 ± 51Æ0a 217Æ4 ± 51Æ9a

PT angle (�) 67Æ9 ± 3Æ9 72Æ3 ± 5Æ2a 73Æ3 ± 3Æ2a

PT time (ms) 406Æ3 ± 62Æ6 313Æ3 ± 85Æ9a 310Æ8 ± 37Æ7a

Work (J) 286Æ2 ± 55Æ3 235Æ8 ± 62Æ4a 261Æ1 ± 63Æ4a

Peak RFD(N ms)1)

1546Æ6 ± 392Æ6 1342Æ7 ± 346Æ6a 1655Æ9 ± 388Æ6b

Time peakRFD (ms)

74Æ1 ± 37Æ0 73Æ3 ± 39Æ3 50Æ8 ± 31Æ7a,b

PT, peak torque; RFD, rate of force development.Values are means ± SD.aDifference from baseline values.bDifference from 24 h (P<0Æ05).

0

200

400

600

800

1000

1200

1400

1600

150100500

Pea

k R

FD

(N

m s

–1)

Time (ms)

Baseline 24 h 48 h

PeakRFD baseline

PeakRFD 24 h

PeakRFD 48 h

0

20

40

60

80

100

120

140

160

180

200

0 100 200 300 400 500 600

To

rqu

e (N

m)

Time (ms)

Baseline 24 h 48 h

PT baselinePT 48 hPT 24 h

(a)

(b)

Figure 2 Example of a maximal voluntaryconcentric isokinetic (60� s)1) quadricepscontraction before (baseline) and after (24 and48 h) eccentric exercise. Representative calcu-lated peak rate of force development (a) andpeak torque (b). Data are from one represen-tative subject.



181

against the lever arm with maximal extension as the first

movement. Prior to the eccentric exercise, participants per-

formed a warm-up consisting of 5 min of cycling on a cycle

ergometer (Lode Excalibur Sport, Groningen, Netherlands).

Muscle damage indicators

Perceived muscle soreness was rated on an 11-point verbal

rating scale, where 0 is �no soreness� and 10 is �extremely

painful� (Hamill et al., 1991). Plasma creatine kinase activity was

determined in a spectrophotometer in duplicate using a

commercially available kit (CK_NAC UV AA, Wiener lab).

Statistical analysis

Mean ± SD was calculated for all variables. We used non-

parametric statistics after the normality and equal variance tests

were checked for all data. Within-group analysis was performed

using Friedman test to compare differences over time (baseline;

24 and 48 h posteccentric exercise) of the study on the

indicators of the muscle damage and isokinetic test. Wicoxon

signed rank test was used to compare the differences between

each pair of time points. The magnitude of changes in PT and

peak RFD were performed using the Spearman correlation test.

The significance was set at P£0Æ05.

Results

The protocol of eccentric exercises produced significant DOMS

at 24 h (3Æ8 ± 1Æ4 au; P = 0Æ002) and 48 h (4Æ1 ± 1Æ9 au;

P = 0Æ003) compared with baseline values (0Æ0 ± 0Æ0 au). CK

activity was significantly higher after 24 h (184Æ6 ± 44Æ7 U l)1;

P = 0Æ03) and 48 h (145Æ9 ± 60Æ9 U l)1; P = 0Æ03) of the

eccentric exercise, when compared to baseline (71Æ6 ±

26Æ8 U l)1).

Peak torque was reduced at 24 h ()15Æ3%, P = 0Æ002) and

48 h ()7Æ9%, P = 0Æ02) after eccentric exercise. In contrast, the

PT angle showed a significant increase by 6Æ4% (P = 0Æ009) at

24 h and 7Æ7% (P = 0Æ006) at 48 h posteccentric exercise. The

PT time decreased by 22Æ8% (P = 0Æ01) and 23Æ5% (P = 0Æ002)

at 24 and 48 h, respectively. The total work was reduced by

17Æ6% (P = 0Æ006) and 8Æ7% (P = 0Æ02) at 24 and 48 h,

respectively. Peak RFD ()13Æ1%, P = 0Æ03) decreased signifi-

cantly only at 24 h (Table 1 and Fig. 2).

There is no difference in change (%) between peak RFD

(86Æ8 ± 25Æ8%) and PT (84Æ6 ± 27Æ6%) from the onset of

muscle contraction to 24 h. However, the peak RFD recovery

(107Æ0 ± 23Æ4%) was higher (P = 0Æ004) than PT recovery

(92Æ0 ± 25Æ6%) at 48 h, relative to baseline values.

Positive correlation was found between PT and peak RFD at

baseline (r = 0Æ62, P = 0Æ02), 24 h (r = 0Æ99, P = 0Æ0001) and

48 h (r = 0Æ68, P = 0Æ01) after the eccentric exercise (Fig. 3).

The magnitude of changes (%) in PT and peak RFD from baseline

to 24 h was significantly correlated (r = 0Æ68, P = 0Æ01). Simi-

larly, there was significant correlation (r = 0Æ68, P = 0Æ01)

between magnitude of changes (%) in PT and peak RFD from 24

to 48 h (Fig. 4).

Discussion

In the present study, we have investigated the association

between PT and peak RFD during recovery of fatiguing eccentric

exercise. The main findings were that the magnitude of changes

in PT and peak RFD at 24 h were similar and significantly

correlated, suggesting that the relationship between PT and peak

RFD during the initial phase of recovery can be causal or

mediated by the same physiological changes. However, the

faster recovery of peak RFD at 48 h suggests that putative

mechanisms underlying maximal force ⁄ peak RFD changes

during intermediary recovery phase of muscle damage are not

completely shared.

Muscle damage results in an immediate and prolonged

reduction in muscle function, specifically the force-generating

0

500

1000

1500

2000

2500

0 100 200 300 400PT (N m)

Peak

RFD

(N m

s–1

)Pe

ak R

FD (N

m s

–1)

Peak

RFD

(N m

s–1

)

r = 0·68p = 0·02N = 12

0

500

1000

1500

2000

2500

0 100 200 300 400PT (N m)

r = 0·99p = 0·001N = 12

0

500

1000

1500

2000

2500

3000

0 100 200 300 400PT (N m)

r = 0·68p = 0·02N = 12

(a)

(b)

(c)

Figure 3 Relationship between peak torque and peak rate of forcedevelopment before (a) and at 24 (b) and 48 h (c) after eccentric exercise.



182

capacity. Sites and mechanisms of failure in the neuromuscular

system responsible for altered muscle function after eccentric

exercise have been identified and demonstrated to be located

peripherally (i.e. E-C coupling failure, redistribution of sarco-

mere lengths, damage to contractile machinery and impaired

metabolism) rather than centrally (Byrne et al., 2004). However,

reduced voluntary activation during MVC after eccentric

exercise-induced muscle damage may indicate a supraspinal

modulation of muscle function (Racinais et al., 2008).

The protocol used in the present study was suitable to

produce changes in all indirect markers of muscle damage. The

magnitude of changes (expressed as absolute and relative values)

in these markers has presented great variability among studies.

This can be explained by both intersubject variability and the

characteristics of the protocol (intensity, number of repetitions,

range of motion and muscle group) used to induce muscle

damage (Nosaka et al., 2005; Paschalis et al., 2005; Crameri et al.,

2007). Thus, the comparison between our data and the

literature must be made with caution.

Moderate to high correlations between maximal muscle force

and RFD have been demonstrated during isometric MVC (Mirkov

et al., 2004; Andersen & Aagaard, 2006). In our study, PT and

peak RFD obtained during maximal isokinetic knee concentric

contractions at 60� s)1 were also significantly correlated,

particularly at 24 h from muscle damage. The association

between maximal muscle force and RFD seems to be influenced

by the time interval in which RFD is determined. Indeed,

Andersen & Aagaard (2006) have verified that RFD was

increasingly related to maximal muscle force and less dependent

on muscle contractile properties as the time from the onset of

contraction increased, particularly at time intervals later than

90 ms. Interestingly, in our study, the peak RFD was obtained at

�70 ms. The present result suggests that the acute neuromuscular

impairment determined by muscle damage increases the associ-

ation between PT and peak RFD, which was obtained during early

phase contraction (<100 ms). Racinais et al. (2008) have verified

significant acute reduction in PT, intrinsic muscle contractile

properties and voluntary activation (twitch interpolation) after

exercise-induced muscle damage. Moreover, PT and voluntary

activation failed to recover before the third day, while contractile

properties had completely recovered. Therefore, it is possible to

hypothesize that at 24 h, intrinsic muscle contractile properties

can mediate the increased association between PT and peak RFD.

The magnitude of changes in PT and peak RFD at 24 h were

similar and significantly correlated. Moreover, the correlation

between magnitude of changes in PT and peak RFD from 24 to

48 h were statistically significant. Our experimental design

precludes the conclusion as to whether the magnitude of

changes in PT and peak RFD during the initial phase of recovery

(24 h) are causal or mediated by the same physiological changes

(e.g. intrinsic muscle contractile properties). However, the

faster recovery of peak RFD at 48 h suggests that the hypothesis

of a direct causal association between PT and peak RFD can be

rejected. Maximal muscle force is influenced by muscle cross-

sectional area (Schantz et al., 1983) and neural drive to the

muscle fibres (Hakkinen et al., 1985). Thus, disruption within

the extracellular matrix (ECM) and ⁄ or between the ECM and

myofibres (Crameri et al., 2007) and the consequent changes in

–60

–40

–20

0

20

40

60

80

–50 –40 –30 –20 –10 0 10 20

% Change PT

% C

hang

e pe

akR

FD

% Change 0–24 h

% Change 24–48 h

Figure 4 Relationship between magnitudeof changes in peak torque (PT) (% change PT)and peak rate of force development (% changepeak RFD) from baseline to 24 h (O % change0–24 h –r = 0Æ68, P = 0Æ02) and from 24 to48 h (• % change 24–48 h )r = 0Æ68,P = 0Æ02).



183

neural drive (Racinais et al., 2008) may still be present at 48 h

after exercise-induced muscle damage, leading to reduced PT.

Conclusion

According to our results, it can be concluded that the muscle

damage induced by the eccentric exercise affects differently the

time course of PT and peak RFD recovery during isokinetic

concentric contraction at 60� s)1. The faster recovery of peak

RFD at 48 h suggests that during the recovery from exercise-

induced muscle damage, PT and peak RFD are determined but

not fully defined by shared putative physiological mechanisms.

Therefore, PT and peak RFD should not be used interchangeable

to determine the recovery of muscle function after exercise-

induced muscle damage. Moreover, explosive-type muscle

actions seem to be less affected by muscle damage, than

muscular activities involving maximum force production.

Acknowledgments

We thank the subjects for participation in this study, and FAPESP

and CNPq for financial support.

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