Downloaded from www.ajronline.org by 190.221.255.156 on 10/05/15 from IP address 190.221.255.156. Copyright ARRS. For personal use only; all rights reserved

765

Acute Effects of Exercise on MR Imaging of Skeletal Muscle: Concentric

Frank G. Shellock1 Tetsuo Fukunaga2’3 Jerrold H. Mink1 V. R. Edgerton2

vs Eccentric

Actions

Eccentric (lengthening) muscle actions involve the forced lengthening of active muscles. Compared with concentric (shortening) muscle actions subjected to the same relative work load, eccentric actions have lower oxygen consumption requirements, fewer activated motor units, and less lactate production. This study was conducted to determine if T2-weighted MR could show any difference in muscles performing these specific types of actions and, therefore, be useful for physiologic investigations of eccentric and concentric actions. Five subjects performed exhaustive exercise by doing isolated concentric actions (raising a dumbbell, flexing at the elbow) and eccentric muscle actions (lowering a dumbbell, extending the contralateral arm). T2-weighted MR images of the arms were obtained immediately before and after exercise. Muscles that performed concentric actions had increases in signal intensity, whereas muscles that performed eccentric actions showed little or no change. T2 relaxation times increased significantly (p < .01) in all volunteers, but T2 relaxation times for the muscles that performed concentric actions were significantly higher than those for muscles that performed eccentric actions (p < .01). Therefore, T2 times increased with both concentnc

and

eccentric

actions,

but

the

images

failed

to show

the

changes

in the

muscles

that performed the eccentric actions. These data demonstrate that assessment of T2 values can be used to distinguish between muscles that perform concentric actions and those that perform eccentric actions, and this phenomenon may be useful for further physiologic investigations of these specific types of muscle actions. AJR

1

Tower

Musculoskeletal

1990;

accepted

Imaging

after

Center,

Ce-

dars-Sinai Medical Center, Los Angeles, CA 90048 and Department of Radiological Sciences, UCLA School of Medicine, Los Angeles, CA 90024. Address reprint requests to F. G. Shellock, CedarsSinai Medical Center, MRI, 8700 Beverly Blvd., Los

Angeles, CA 90048. 2

fomia,

Department

of Kinesiology,

Los Angeles,

Los Angeles,

3 Present address: Department ences, University of Tokyo, Tokyo,

0361 -803X/91/1 564-0765 0 American Roentgen Ray Society

University

of Cali-

CA 90024. of Sports Japan.

Sci-

April

1991

Eccentric (lengthening) muscle actions involve the forced lengthening of active muscles and the transfer of external power from the environment to the subject [1 2]. Examples include the use of resistance equipment, such as weight-lifting devices, or deceleration processes during activity, such as running downhill. Therefore, eccentric muscle actions produce active tension while the muscle is being lengthened. Various investigations have shown that, compared with concentric (shortening) muscle actions, eccentric actions are associated with reduced oxygen consumption, fewer activated motor units, and less lactate production for the same power output [3-7]. Therefore, concentric actions apparently require more energy than eccentric actions do when subjected to the same relative work load [3-7]. Fleckenstein et al. [8] first reported that T2-weighted spin-echo images of active skeletal muscle showed increased signal intensity immediately after exercise. Other studies have also investigated this phenomenon [9-1 1 }. This contrast enhancement of exercised muscle was suggested to be caused by increased vascular and extracellular volumes [8], as well as by changes in intracellular water [1 1 ]. Research has additionally shown that T2 relaxation times of active skeletal muscles depend on exercise intensity [8, 1 1]. In consideration of these facts, the present study was conducted to determine if ,

Received September 24, revision October 23, 1990.

156:765-768,

SHELLOCK

766

T2-weighted acute

MR images

exercise

vs eccentric

actions

information

technique

of muscles

show

of muscles

is available

perform

relative

because,

performing

any difference that

at the same

is important

accurate Downloaded from www.ajronline.org by 190.221.255.156 on 10/05/15 from IP address 190.221.255.156. Copyright ARRS. For personal use only; all rights reserved

could

response

work

currently,

and MR could be used to precisely involved muscles.

direct

a long

TE

Study

samples

actions

sampling

[1],

of the

images

are

were

used,

T2-weighted

obtained

and

frorn the mid-forearms

immediately

proton-

to the deltoids,

jects’ arms placed together over their head loosely applied cloth tape to inhibit motion.

and Methods

and held

before

and

with the subin place

with

Subjects

Five

two

women; in this

normal

volunteer

gation. These arm resistance the study.

Exercise

subjects

(three

men

and

aver-

any in

Protocol

weighted

to a normalized

percentage

(i.e., 15%

for women and 20% for men) of the subject’s body weight was used for the resistance exercise. The weights ranged from 1 2 to 1 5 lb. for the women and from 25 to 30 lb. for the men. The subjects performed a “biceps curl” movement for the exercise while in a standing position. One arm was selected randomly to perform concentric (i.e. , shortening) actions. This was accomplished with strict form, by bending the arm at the elbow and raising the dumbbell with the palm up, moving from extension to full flexion. The weight was then passed to the contralateral arm by an assistant to perform the eccentric (i.e., lengthening)

actions.

This

was

bell with strict form,

beginning

it to extension.

extremities

The

accomplished

by lowering

with the arm at full flexion were

in supinated

out the range of motion of each movement. concentric and eccentric actions took place each movement took approximately 2 sec. subjects performed isolated concentric and alternating manner. Exercise was performed by each of the perceived exhaustion and “failure” (i.e., the raise

the dumbbell)

with

each

and the

extremity.

same

Therefore,

number the

the

dumb-

and lowering

positions

to the point of no longer could

of repetitions

concentric

and

were

achieved

eccentric

actions

were performed to the same relative work level. This exercise protocol was similar to those used by others to study concentric vs eccentric actions

[12]

techniques

and

was

also

frequently

designed

to

used

by body

work

performed

simulate

builders

resistive

and strength

by measuring

total

power,

(kg) x distance time

yielded

iOO kg m/sec

the

results

arm was calculated

subjects

in this

1 09 kg rn/sec (woman), 1 55 kg m/ sec (man), 142 kg rn/sec (man), and 155 kg rn/sec (rnan).

(woman),

MR Protocol MR was performed ture-dniven,

with a 1 .5-T, 64-MHz

transmit/receive

body

coil

MR imager

(General

determined vided

for these

by General

Electric

that

performed

the

care

to avoid

inclusion

or bony anatorny. regions

of interest

concentric

and

eccentric

of subcutaneous

T2 relaxation by using

fat,

times were

the software

pro-

Electric.

T2 relaxation times measured before and after exercise for each muscle group (e.g. , biceps before exercise concentric action vs biceps after exercise concentric action, triceps before exercise concentric action extrernity vs triceps after exercise concentric action extremity) were compared by using a paired t-test. A comparison between the postexercise concentric action biceps data and the postexercise eccentric action biceps data also was made by using a paired t-test.

Results Visual inspection of the images differences in the signal intensities

and quadraCompany,

Milwaukee, WI). Inasmuch as Fleckenstein et al. [8] showed that active muscles are most conspicuous on MR when pulse sequences

(Fig. 1) showed no apparent of any of the muscle groups

before exercise (i.e., the biceps and triceps). Immediately after exercise, increases were apparent in the signal intensity of the biceps and brachialis muscles that performed concentric actions, intensity eccentric

whereas little or no change occurred in the signal of the biceps and brachialis muscles that performed actions (Fig. 1). The signal intensity of the triceps

(i.e., inactive concentric

muscles)

and eccentric

of the extremities

that per-

actions

to be un-

appeared

changed from that on the preexercise images. The data on T2 relaxation times are summarized in Figure 2. The T2 relaxation times were not significantly different for the triceps

the

special

fascia, blood vessels,

muscles

(m)

for

arms

with

formed

(sec)

following

mid-upper

actions,

training

as follows:

mass

calculation

by each

ject’s

trainers

113]. The estimated

The images were filmed with standardized window settings, and the relative signal intensities of the active muscles in the arrns involved in concentric and eccentric actions were compared visually with those of the nonexercising muscles (i.e. , the triceps). Regions of interest were selected in the center of the biceps (i.e., the active muscles) and triceps (i.e., inactive muscles) of each sub-

through-

The rate at which the was monitored, so that Using this protocol, the eccentric actions in an subjects subject

Data Analysis

investi-

individuals were untrained and had not performed training for at least 6 months before involvement

A single dumbbell

study:

TR

load. This

age age, 36 years; range, 21 -48 years) were involved

This

long

after exercise with the following pararneters: axial imaging plane; 2000/80, 20 (TR/TE); 128 x 256 matrix; two excitations; 44-cm field of view; 1 0-mm slice thickness; and 2-mm interslice gap. These pararneters were selected to minimize data acquisition tirne while still obtaining the necessary image information from both exercising limbs for analysis. The subjects were placed supine in the MR irnager, and images

were obtained Subjects

and

spin-echo

April 1991

density,

biopsy

vs eccentric

with

AJR:156,

concentric

no sufficiently

for obtaining

concentric

in the

ET AL.

and SD, 0.4 29.8

muscles

of the extremities

performing

concentric

eccentric actions (note: all reported values are mean ± triceps preexercise concentric action extremity, 29.5 ± msec, triceps postexercise concentric action extremity, ± 0.5 msec, p = N.S.; triceps preexercise eccentric

action extremity, 29.6 ± 0.3 msec, triceps postexercise centric action extremity, 29.6 ± 0.5 msec, p = N.S.). Statistically significant increases in T2 relaxation times

ecwere

seen for the biceps muscles performing concentric actions (biceps preexercise concentric action, 29.1 ± 0.6 msec, biceps postexercise concentric action, 38.5 ± 0.9 msec, p = .0001

)

and the biceps

performing

eccentric

actions

(biceps

AJR:156,

EXERCISE

April 1991

AND

MR OF SKELETAL

centric action,

action, 33.1

MUSCLE

767

38.5 ± 0.9 msec,

1 .1 msec, p

±

=

biceps .0006).

postexercise

eccentric

Downloaded from www.ajronline.org by 190.221.255.156 on 10/05/15 from IP address 190.221.255.156. Copyright ARRS. For personal use only; all rights reserved

Discussion MR imaging has developed into the foremost noninvasive imaging technique for examining normal and diseased conditions of the musculoskeletal system [1 4]. When MR imaging is used, biological tissues and fluids with excess amounts of

free water have long T2 values and, therefore, tend to be the most conspicuous on T2-weighted images [1 4, 15]. Exercise-induced

water content

changes

produce

in extracellular

changes

and intracellular

in proton relaxation

times [8-

1 1] and correlate with the level of exertion [8, 1 1]. Fleckenstein et al. [8] first showed that exercise is associated with statistically significant changes in Ti T2, and spin-density relaxation times observed on MR. The greatest effect was ,

seen on images obtained with T2-weighted pulse sequences and, to a lesser degree, on those obtained with gradientreversal techniques in which the flip angle was reduced to decrease the effect of Ti differences on the images [8]. In consideration of the results of previous studies [8, 1 1 ], we decided to use T2-weighted MR selectively for our investigation to maximize the suspected differences between muscles performing concentric actions and those performing eccentric actions.

The preexercise

occurs

In signal

actions,

and they are not differentiated

ifty

of active

muscles

that

performed

eccentric

as easily.

actions

-

PREEXC BICEPS POST

EX.C

BICEPS PREEXC



45

TRICEPS

40

II

POST EX.C TRICEPS

35

__

30

PRE EX-E

25

BICEPS

!

POST EX.E BICEPS

CJ

15

___

10

5

C’”’”?,

PRE EX-E TRICEPS POST EX-E TRICEPS

0

Fig. 2.-Graph

shows T2 values of biceps and triceps measured before extremities performed concentric and eccentric actions. Values are means ± SD. EX-C = concentric actions; EX-E = eccentric actions. and after

preexercise exercise addition, concentric biceps

eccentric action, 29.5 ± 0.5 msec, biceps posteccentric action, 33.1 ± 1 .1 msec, p = .004). In the T2 relaxation times for the biceps performing action were significantly higher than those for the

performing

eccentric

actions

(biceps

postexercise

con-

T2 values for the muscles

evaluated

in this

study were comparable to those reported by Fleckenstein et al. [8] and others [1 3, 1 6, 1 7]. The immediate postexercise T2 values for the muscles performing concentric and eccentric also

were

within

the

ranges

reported

by

previous

investigators for active muscles [8, 1 1]. Additionally, we observed that muscles performing eccentric actions had a statistically significant lower T2 value than did muscles performing concentric actions. Research studies have shown that muscle actions that involve eccentric actions require less oxygen, produce less lactate, and use fewer muscle fibers than do concentric actions subjected to the same relative work load [1 -7]. Of further note, Fisher et al. [1 1 ] reported a strong correlation between the increase in T2 values and the mean force during exercise. Therefore, considering that T2 values are related to exercise intensity and eccentric action requires less of an energy expenditure than does concentric action, it is not surprising that we found statistically significant differences between T2 values for each of these specific types of muscle action. Exercise produces rapid alterations in the content of water found in skeletal muscle [1 8, 1 9]. Several mechanisms appear to be involved in this process. The water content in the exercising muscles increases as a result of the movement of water across the capillary wall, which is mediated by the hydrostatic pressure in the capillary and the osmotic forces in both the capillary blood and interstitial fluid [1 8, 19]. The increase in muscle lactate during exercise causes an increased tissue osmolality that also contributes to the increased water content of skeletal muscle observed with exercise [18, 19]. Additionally, the vascular bed of active muscles has an enlarged functional capillary surface area and

SHELLOCK

768

an increased

creased interstitial

Downloaded from www.ajronline.org by 190.221.255.156 on 10/05/15 from IP address 190.221.255.156. Copyright ARRS. For personal use only; all rights reserved

mean

capillary

pressure

filtration of water space [1 8, 19].

from

that

produces

the capillary

an in-

crease in muscle water content occurs in the intracellular space [19]. Fleckenstein et al. [8] indicated that the increased

water,

also may be involved.

in intracellular

The prelim-

formed the concentric action, with a minor contribution from an increase in extracellular water, as our subjects performed

protocol.

tion of extracellular maximal concentric

studied

However,

the relative

et al. [9] localization

proposed technique

scopic studies of active muscles anatomy

and individual

from our data.

that exercise-enhanced for guiding MR spectro-

because

differences

variations

in muscle

pat-

terns exist, and palpation techniques used to identify the sample volume are relatively inaccurate. Therefore, the use of exercise-induced portant for avoiding

active

contrast enhancement is particularly admixtures of spectroscopic signals

and inactive

muscles

[9]. However,

intensity

changes

are not visually

images

of muscles

that perform

may

not

be possible

to rely

apparent

isolated

simply

because

imfrom

signal

on T2-weighted

eccentric

on visual

actions,

inspection

sensitive

volume

actions.

for MR spectroscopy

studies

involving

only

There is currently no sufficiently accurate technique available for obtaining biopsy samples of muscles performing concentric vs eccentric actions [1] and, therefore, MR could be used to precisely direct the sampling of the involved active muscles. MR also may be helpful in further elucidation of physiologic differences between these specific types of mus-

cle actions.

Day

Ohira, for their

John

Hodgson,

involvernent

in this

Tracey

Meeks,

study.

Armstrong

RB. Mechanisms

of exercise-induced

delayed

onset

muscular

5. Bigland-Ritchie B, Woods M. Integrated electromyogram and oxygen uptake during positive and negative work. J Physiol 1976;260:267-277 6. Davies CTM, Bames C. Negative (eccentric) work. II. Physiological responses to walking uphill and downhill on a motor-driven treadmill. Ergonomics 1972;15: 121 -131 7. Schwane JA, Watrous BG, Johnson SR. Armstrong RB. Is lactic acid related to delayed-onset muscle soreness? Physician Sportsmed 1983;1 1: 8. Fleckenstein JL, Canby RC, Parkey exercise on MR imaging of skeletal

RW, Peshock RM. Acute effects of muscle in normal volunteers. AJR

1988;151 :231 -237 9. Fleckenstein JL, Bertocci LA, Nunnally RL, Parkey RW, Peshock RM. Exercise-enhanced MR imaging of variations in forearm muscle anatomy and use: importance in MR spectroscopy. AJR 1989;153:693-698 1 0. Peshock R, Fleckenstein J, Payne J, Lewis 5, Mitchell J, HaIler R. Muscle

11 .

usage pattems during cycling: MRI evaluation (abstr.). Magn Reson Imaging 1990;7:23 Fisher MJ, Meyer RA, Adams GR, Foley JM, Potchen EJ. Direct relationship

between proton T2 and exercise intensity in skeletal muscle MR images. Invest Radiol 1990;25:480 12. Clarkson PM, Tremblay I. Exercise-induced muscle damage, repair, and adaption in humans. J AppI Physiol 1988;65: 1-6 13. Fleck SJ, Kraemer WJ. Designing resistance training programs. Champaign, IL: Human Kinetics Books, 1987 1 4. Mink JH, Deutsch A. MRI of the musculoskeletal system: a teaching file.

it of

images to identify transient increases in signal intensity. Accordingly, it may be necessary to measure T2 relaxation times or to quantify the signal intensity changes to identify the eccentric

Yoshio

Kathy

REFERENCES

in muscle

recruitment

thank

124-131

contribu-

and intracellular water changes related to or eccentric muscle actions has not been

before and could not be determined

Fleckenstein MR is a useful

and

1952;28:364-382

free water related

images in our present study depended primarily on an increase in intracellular water of the active muscles that per-

exercise

gratefully Slimp,

a brief review. Med Sci Sports Exer 1984;16:529-538 2. Stauber WT. Eccentric action of muscles: physiology, injury, and adaption. In: Exercise and sports sciences reviews. Philadelphia: The Franklin Institute, 1988:157-185 3. Armstrong RB, Laughlin MH, Rome L, Taylor CR. Metabolism of rats running up and down an incline. J Appl Physiol 1983;55:518-521 4. Asmussen E. Positive and negative muscular work. Acta Physiol Scand

to maximal exercise. In consideration of this, we presume that the signal intensity changes observed on T2-weighted

a maximal

April 1991

soreness:

mary work by Fisher et al. [1 1] suggested that the increased signal intensity seen on T2-weighted images of active muscles

was largely due to increases

We Gina

1.

in muscles that performed fatiguing mainly by an increase in extracellular

but other processes

AJR:156,

ACKNOWLEDGMENTS

bed into the

Mild to moderate levels of exercise appear to be associated with a large (i.e., up to 1 00%) increase in extracellular water and a slight increase (i.e., about 1 0%) in intracellular water [1 8]. However, with maximal work loads, the greatest in-

signal intensity seen exercise were caused

ET AL.

New York: Raven, 1990 15.

Fisher MR, Dooms GC, Hncak H, Reinhold C, Higgins CB. Magnetic resonance imaging of the normal and pathologic muscular system. Magn Reson Imaging 1986;4:491-496 16. Hazelwood CF, Chang DC, Nichols BL, Woessner DE. Nuclear magnetic resonance transverse relaxation times of water protons in skeletal muscle. Biophys J 1974;14:583 1 7. Pettersson H, Fitzsimmons J, Krop D, Hamlin D. Magnetic resonance imaging of the extremities. II. Ti and T2 relaxation times of muscle and fat: normal values, reproducibility and dependence on physiologic variatins. Acta Radiol Diagn 1985;26:413-4i6 18. Sjogaard G, Saltin B. Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. Am J Physiol 1982;243: R27i-R280 1 9. Sjogaard G, Adams RP, Saltin B. Water and ion shifts in skeletal muscle of humans with intense 1985;248:R190-R196

dynamic

knee

extension.

Am

J

Physiol

Acute effects of exercise on MR imaging of skeletal muscle: concentric vs eccentric actions.

Eccentric (lengthening) muscle actions involve the forced lengthening of active muscles. Compared with concentric (shortening) muscle actions subjecte...
764KB Sizes 0 Downloads 0 Views