Pamela James

Nurenberg, L. Fleckenstein,

MD

J. Giddings, J. Gonyea,

#{149} Catherine

MD

#{149} William

PhD PhD

#{149} James

MR Imaging-guided Muscle of Increased Signal Intensity Change and Delayed-Onset after Exercise’

E

To determine if there is a correlation between the degree of delayed increase in signal intensity (SI) of muscle after exercise on magnetic resonance (MR) images and the amount of ultrastructural (ULS) injury and delayed-onset muscle soreness (DOMS), MR imaging-guided muscle biopsy was performed to obtain tissue from the legs of nine sedentary subjects 48 hours after downhill running on a treadmill. The degree of soreness was subjectively graded. Ti-weighted, spin-density, T2weighted, and short inversion time inversion-recovery images were obtamed before and after biopsy, at 48 and 96 hours after exercise, respeclively. The delayed SI increase of muscle on images obtained before biopsy was subjectively graded and measured. The degree of ULS injury was determined with electron micrographs. Serum creatine kinase levels were obtained before and up to i44 hours after exercise at 24-hour intervals. The measured SI, SI grades, and DOMS grades were correlated with the degree of ULS injury. Linear regression analysis revealed poor correlation between the DOMS grades and the degree of ULS injury and good correlation between the SI grade and the degree of ULS injury.

Index

terms:

Athletic

injuries

mediate

protracted intensity

I

From

nance ceived

the

University

April 2. Supported dowed professorship

delayed (SI)

increases

of muscle

in signal

at magnetic

subjects

48 hours

after

exercise.

We

asked the following questions: (a) Is there a correlation between the degree of SI increase at 48 hours and the degree of ULS injury? (b) Is there a correlation between the degree of DOMS and the degree of SI increase at 48 hours, the degree of ULS injury, or the serum creatine kinase (CK) levels? PATIENTS

AND

METHODS

Studies were performed according to protocols approved by the Institutional Review Board for Human Studies at the University of Texas Southwestern Medical Center, and informed consent was obtamed from all subjects. Six men and three women participated. Ages ranged from 23 to 39 years. No subject had regularly engaged in exercise before this study.

Extremities,

#{149}

Exercise

and

Serum

CK Sampling

Subjects performed eccentric muscle action by running on a treadmill fixed at a negative 8% grade for hour at a rate of 8

of Texas

Southwestern

Park Rd. Dallas, revision requested

Medical TX 75235. February

Center

at Dallas,

Rogers

Address

reprint

requests

Magnetic

to P.N.

km/h. Eccentric muscle action (7) was performed because it is more commonly assodated with the production of ULS injury than is concentric muscle action (9,1 1). Serum CK bevels were obtained before and up to 144 hours after exercise at 24hour intervals. Because of scheduling difficulties, three of the nine subjects missed one blood sampling interval.

Questionnaire Forty-eight hours after exercise, subjects indicated regions of soreness on diagrams of posterior and lateral views of the beg and graded their soreness on a scale of 0 (none) to 5 (extremely severe) (12-16). Subjects were questioned regarding the time of onset of soreness and the time of peak soreness after exercise.

MR

Imaging

Technique

MR imaging 0.35-T

was

imager

performed

(Toshiba

America

with

a

MRI,

South San Francisco, Cabif) 48 and 96 hours after exercise. The center of acquisition was marked on the subject’s skin 9 cm below the joint line with the MR baser centering device. A clamshell coil was used for all subjects. Two of the subjects were also studied with an extremity coil. Axial Ti-weighted spin-echo (SE) 600/30,40

(repetition

time [TR] msec/echo

time

[TE]

msec), spin-density 2,000/40, T2-weighted SE 2,000/80, and short inversion time inversion-recovery (STIR) 1,500/30/100 (TR msec/TE msec/inversion time msec) sequences were used, with 10-mm-thick contiguous sections, a 1.7 x 1.7 x 10-mm voxel, a 256 x 256 matrix, and two signals

averaged.

Repeat

MR imaging

was per-

formed 96 hours after exercise to confirm the location of the biopsy (Figs 1, 2).

Biopsy

and

Electron

Microscopy

The location for biopsy was on the basis of the MR images

determined obtained

48

Reso-

From the 1991 RSNA scientific assembly. Re12, 1992; revision received March 25; accepted

in part by a grant from Toshiba America MRI. W.J.G. supported in exercise sciences from the University of Texas Southwestern

at Dallas, grant 569835. C RSNA, 1992

immore

mine the basis of the delayed SI variation, we performed MR imagingguided muscle biopsy in nine healthy

184:865-869

Center, 5801 Forest December 4, 1991;

both transient occasionally

MD MD

for Correlation Ultrastructural Soreness

extracellular water that accompany exercise (4-6). The delayed increase in SI (2,3) appears to parallel the time course of delayed-onset muscle soreness (DOMS) and ultrastructural (LJLS) injury, peaking 48-96 hours after exercise (7-10). In an attempt to deter-

45.48, 45.833 #{149}Extremities, MR, 45.1214 S Magnetic resonance (MR), tissue characterization #{149}Muscles, injuries, 45.48, 45.833 #{149}Muscles, MR. 45.1214

1992;

Biopsy with Muscle

resonance (MR) imaging (i-3). The immediate SI increase is a normal response and parallels known increases in intracellular and predominantly

injuries,

Radiology

causes and

XERCISE

Stray-Gundersen, M. Peshock,

#{149} Ronald

in part by an enMedical Center

Abbreviations: CK DOMS = delayed-onset spin echo, inversion time, TR hire.

SI time =

=

creatine muscle

kinase, soreness,

SE

=

signal intensity, STIR = short inversion recovery, TE = echo repetition time, ULS = ultrastruc=

865

a.

b.

d.

C.

f.

e. 1.

Figure

Images of the right leg of a 25-year-old nor tibial muscles after exercise. (a) Ti-weighted 30/100) images obtained 48 hours after exercise

sedentary man show mild (grade 1) SI increase of the soleus (arrow in a, b, and d) and ante(SE 600/30), (b) spin-density (SE 2,000/40), (c) T2-weighted (SE 2,000/80), and (d) STIR (1,500/ (before biopsy). Note that the SI increase is more prominent on Ti-weighted, spin-density, and

STIR images.

after

(e) STIR image

obtained

96 hours

features,

including

Z bands

the letters

1), and

myofilament

(row

hours after exercise, and the area was marked on the skin with indelible ink. Biopsy was performed in muscles with varying degrees of SI increase and in one with no SI increase. The biopsy specimen was obtained with a Bergstrom needle (Karolinska Institute, Stockholm) with a sterile technique and after administration of local anesthesia with 1% lidocaine. A total of 10 biopsy specimens were obtained (one subject underwent biopsy twice) from the soleus (n = 4), lateral gastrocnemius (n = 1), medial gastrocnemius (n = 1), tibialis antenor (n = 3), and peroneus longus muscles (n = I). Each biopsy specimen was pinned to dental wax and immersed in a solution of

were

cut from each

2%

10 muscle fibers were analyzed for each subject. Three nonoverbapping regions per muscle fiber were photographed, yielding a total of 30 electron micrographs per subject. A mean of 913 ± 200 sarcomeres were analyzed per subject. Sarcomeres were classified as normal if no structural disruption was present in any component of the sarcomere, that is, if the I bands, A bands, and Z bands were intact. Abnormalities were then subcategorized according to the component of the sarcomere that was affected. The degree of ULS injury was determined by calculating the percentage of normal sarcomeres, the

strates

primarily

letters

A

splitting

normal

), I bands (large

ULS

(between

and

Tissue

minutes

were

then

in fresh

2%

glutarabde-

of cacodylate

buffer.

were

allowed

at room

processing

Tissue

samples

mium

tetroxide,

and

pieces,

refrigerated

for electron were

dehydrated

to fix for

temperature.

cut into smaller

fixative,

until

acetate,

and

0.1 mmob

samples

20-30

then

stained

with

They

stored at 4#{176}C

microscopy. fixed

in 1%

os-

en bloc

in uranyl

graded

alcohols

and propylene oxide, and embedded in Epon (Electron Microscopy Sciences, Fort Washington, Pa). Fiber bundles were oriented for bongitudma! analysis. Thick sections (0.5 pm)

866

#{149} Radiology

demonstrates

(small

biopsy

arrowheads),

site (arrow).

sarcomeres

of sarcomeres

(f) Electron

(delimited

between

open

micrograph

from

Z bands),

A bands

by two

arrows).

Mild

ULS damage

biopsy

site demon-

(between

is seen

the

as Z-band

arrowheads).

paraformaldehyde

hyde

exercise

block

and stained

with

tobonium chloride evaluation. Tissue form fiber diameter

for light microscopic blocks that showed uniwere selected for ULS

analysis

that

to ensure

the

muscle

fibers

percentage

of Z-band

Results

were not cut obliquely. Thin sections were obtained from three to five tissue blocks per subject. The sections were stained with uranyl acetate and lead citrate and examined with an electron microscope (model iOOC; JEOL America, Peabody,

were

to allow

whole) affecting the sarcomere. percentage

is a standard

and

printed

to a final

The structural

magnifica-

features

of

(ie,

as percentages

between

subjects.

Determining the percentage of normal sarcomeres is an indirect way of quantitating the various forms of ULS injury (as a

The structural features of the muscle fiber were assessed from electron micrographs obtained at a magnification of x5,300

expressed

comparisons

Mass).

tion of x 10,000.

“streaming”

Z-band material displayed an irregular pattern across all or part of the sarcomere), and the percentage of normal Z bands.

Data

different We chose

of Z-band

components to determine

streaming

index

of the

because (17).

of muscle

it

injury

Analysis

The biopsy images,

axial

image

site

was

and

regions

drawn in various to avoid including fascia.

SI values

appearing

corresponding selected

percentage

prebiopsy

of interest

muscles, nearby were

of increase

were

with care taken fat, vessels, and

of normal-

muscle

to the

from

and

abnormal-

recorded, in SI was

and

the

deter-

mined.

The images vidual

degree was and

of SI increase subjectively overall images

on prebiopsy graded for mdion a scale of 0

(normal) to 5 (very severe SI increase) by two radiologists (P.N., J.L.F) in a blinded fashion.

September

1992

b.

‘-.,‘,‘.,,

/,

#{163}

after exercise (before biopsy). and d = lateral gastrocnemius strates biopsy sive structural same biopsy

C.

site (arrow). disorganization sample shows

Note

.&,

more

prominent

#{163}&((*b..

I

SI increase

..‘

in a, b, and

c. Arrows

#{163}

in a, b,

g.

muscle. (e) STIR image obtained 96 hours after exercise demon(f) Electron micrograph of specimen from biopsy site shows exten(arrowheads). (g) Electron micrograph from another region of structural disorganization involving only two sarcomeres (arrow-

heads). had

no

increased Statistical Linear

Analysis regression

analysis

mild n =

was per-

formed to determine the correlations between the calculated parameters of injury (percentages of normal sarcomeres,

Z-band

streaming,

and normal

Z bands)

SI grade, (b) the SI images, (c) the measured SI increase, and (d) the perceived grade of soreness in the biopsy region. Correlations between the perceived grade of soreness in the biopsy region and observed SI grade overall in the biopsy reand (a) the overall grade for individual

gion,

as well as between

soreness

overall

and

CK

peak levels,

perceived

to moderate, 1; and severe,

n n

1; moderate, 5). DOMS

= =

peaked 12-36 hours after exercise. Peak CK levels ranged from 205 to 1,166

U/L

(mean,

500

U/L)

and

usu-

ally occurred 24 hours after exercise. In one subject, the CK level did not increase after exercise. One subject’s highest known CK level was reached 144 hours after exercise; however, the specimens hours were tion of CK

obtained unsuitable level.

at 24 and 96 for determina-

calculated. MR RESULTS DOMS DOMS

and mild

Volume

184

Nine subjects experienced an increase in SI in multiple muscles in each leg 48 hours after exercise. Six

CK Levels

ranged

ity from

in subjective

to severe #{149} Number

Imaging

(mild, 3

severn

=

2;

patients in only

experienced one

muscle,

an increase and

three

in SI subjects

in SI. Muscles

SI included

the

with

anterior

tib-

iab (n = beus (n (n = 3), (n = 4). biopsy

9), posterior tibial (n = 8), so= 7), lateral gastrocnemius and medial gastrocnernius The MR images obtained after demonstrated the location of

biopsy change

relative to muscle after exercise.

If SI increased in posterior tibial, and muscles, the increase lateral (four of five three subjects, and jects, respectively).

muscle

were

increase

increased,

with

SI

the anterior tibial, gastrocnemius was usually bisubjects, three of two of three subIf SI in the soleus

it usually

occurred

asymmetrically (five of six subjects). that increased 48 hours after exercise remained increased at 96 hours. No new areas of SI increase were detected after 48 hours.

In all subjects anterior ripheral throughout

in whom

the

SI

SI of the

tibiab muscle increased, a perim of increased SI was noted the length of the muscle

Radiology

#{149} 867

(Fig 3). However, all other muscles in which SI increased showed a diffuse pattern of increased SI. Only one subject had perifasciab SI increase. The peak CK level of this subject was 539 U/L, which was well below the highest peak CK level in our study (1,166 U/L).

Statistical

Correlations

Linear

between

bated

parameters

of ULS

centages

of normal

Z-band

material

27%of the

displayed

missing.

teration

This

was

type

often

Z

an

of Z-band

associated

al-

with

observed (0.5% [35 of 8,216]). Muscle fiber injury was not uniform along the length of the fiber. Focal regions of myofibriblar disruption were observed in some biopsy speciSome

of these

extensive

structural

involving

the

regions

showed

I bands,

and

Z

bands of the sarcomeres (Fig 2f). Although the structural and contractile proteins were present in these regions, the normal sarcomeric organization into discrete bands was not identifiable. In other regions of the same biopsy sample, only one or two sarcomeres

were

affected

(Fig

biopsy specimens from other the focal myofibrillar disruption peared as a loss of sarcomeres Within

one along ing. dria files

an

area

of normal

2). In

subjects, ap(Fig 4).

sarcorneres,

or several adjacent sarcomeres a myofibril appeared to be missIn these regions, the mitochonand sarcotubular membrane proappeared more prominent and

occupied the tile elements.

space

devoid

of contrac-

No evidence of phagocytic cell infiltration into the injured muscle fibers was observed. In addition, cellular accumulation in the perifascicular space (indicative response) was this study. 868

#{149} Radiology

not

of an inflammatory observed during

spin-density

between of injury

the

calculated (a) the mea-

and (b) the

sured SI increase and ceived grade of soreness region. There was also tion between grade of biopsy region and the in SI (r = .408), as well peak grade of soreness

perin the biopsy poor correlasoreness in the overall increase as between the overall and the CK bevels (r = .349). These r values are summarized in the Table. Forty-eight percent (i4 of 29) of the regions of perceived soreness correbated with regions of SI increase. Twenty-four percent (seven of 29) of the regions of perceived soreness were in the area of the muscubotendinous junction of a muscle, which showed diffusely increased SI at MR imaging. Twenty-eight percent (eight

Figure 3. STIR (1,500/30/100) leg of a 33-year-old sedentary tamed 48 hours after exercise. high-SI peripheral rim in the tibial muscle (arrow).

image woman

of the ob-

Note

right

the

anterior

a.

of 29) of the regions of perceived soreness did not correspond to a region of increased SI. Twenty-one per-

disorganization

A bands,

on

SI

-

loss of the I band (6% [998 of 16,432)). A-band lesions were also occasionally

mens.

(per-

sarcomeres,

SI increase

no correlation parameters

irregular pattern across all or part of the sarcornere (Z-band streaming) (Fig 4). Two subjects had severe Z-band streaming involving multiple adjacent sarcomeres and along adjacent myofibrils. In other sarcorneres, the Z band was either partially or totally

calcu-

images, and (d) the observed SI increase on STIR images (Figs i, 2). There was less of a correlation between observed SI increase on T2weighted images and ULS injury and

z band

which

injury

streaming, and normal Z and (a) the observed overall increase, (b) the observed SI increase on Ti-weighted images, (c) the ob-

of 8,216) showed

were observed in 20% (i,963 of 9,431) of the sarcomeres examined. These abnormalities included mild degenerative changes, in which the bands of some sarcomeres split (Fig if), and more severe disruption, in

revealed the

Z-band bands)

Injury

Fifty-eight percent (4,790 of the sarcorneres examined normal ULS features (range, 65%). Structural abnormalities

analysis

correlations

served

ULS

regression

high

cent (seven of 33) of muscles creased SI did not correspond region of perceived pain.

with into a b.

Figure

Our

data

indicate

high correlation of SI increase

that

between 48 hours

there the after

is a degree exercise

and the degree of ULS injury (disrupted proteins). The highest correlations were between the SI increase with the Ti-weighted and spin-density pulse sequences of ULS injury. This

from

and finding

the

that seen by Fleckenstein et al Shelbock et al (3), who noted prominent delayed SI increase T2-weighted pulse sequences sustained exercise. Our subjects

reached

markedly

CK levels the study U/L),

which

(

mean

between after

< 500 U/L)

local eccentric (i4,i5,i8-20).

established

peak

downhill

and

peak

did those in et ab (6,500

corroborates

differences obtained

lower

(500 U/L) than by Fleckenstein

bevels

old man streaming graph

(a) Electron from

micrograph

of biopsy

the lateral head of the right muscle of a sedentary 23-year-

after exercise (arrowheads).

of specimen

demonstrates (b) Electron

obtained

from

Z-band microthe

right

anterior tibial muscle of a 27-year-old sedentary man after exercise shows loss of sarcomeres chondna devoid

(arrows), with (arrowheads) of contractile

more

severe

more prominent occupying elements.

the

mitospace

degree differs

(2) and

more with after

4.

specimen gastrocnemius

DISCUSSION

CK bevels running

obtained

after

exercise ( > 2,000 U/L) We hypothesize that in

forms

of muscle

edema (free water) plays role, producing a greater on T2-weighted mean peak CK

low,

our

damage,

a greater SI increase

images. Although levels were relatively

subjects

experienced

our

DOMS,

as defined by other researchers, and sustained mild forms of ULS injury. The lack of visualization of an inflammatory response in the damaged muscle 48 hours after exercise corrob-

orates

the

findings

of Jones

et al (18),

who saw no evidence of cellular infiltration in human muscle until 5 days

September

1992

2.

3.

4.

Fleckenstein JL, Weatherall PT, Parkey RW, Payne JA, Peshock RM. Sports-related muscle injuries: evaluation with MR imaging. Radiology 1989; 172:793-798. Shellock FG, Fukanaga T, MinkJH, Edgerton yR. Exertional muscle injury: evaluation of concentric versus eccentric actions with serial MR imaging. Radiology 1991; 179:659-664. Sjogaard G, Salton B. Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. Am J Physiol 1982; 243: R271-R280.

5.

Sjogaard G, Adams ion shifts in skeletal intense

6.

7,

after the subjects performed eccentric contractions of the forearm or ran backward down an inclined treadmill. Additionally, Friden et al (7) saw only subcellubar-level abnormalities within human muscle 2 and 7 days after their subjects ran down stairs. Conversely,

10.

ence of edema and an inflammatory response in rat muscle 48 hours after injury produced by extensive strain (i30% of body weight, equaling

of Kuipers et al (25), who demonstrated that although exercise-induced CK elevation may indicate muscle injury, it does not provide an index of the magnitude of the injury. The correlation between ULS damage and SI increase and DOMS is intriguing. We have demonstrated a high correlation coefficient (r = .88) between areas of SI increase and ULS injury. However, there was no conebation between areas of DOMS and

80%

areas

13.

Nikolau

et al (21)

of ultimate

reported

the

rupture

pres-

force,

-

was

of SI increase.

applied), ate fiber Stauber

which produced immedirupture and hemorrhage. et ab (22) reported a complex

The muscles that ied despite controlled

reaction

of extraceblular

eccentric

matrix,

soleus

cells,

and inflammation mediators 48 hours after muscle damage caused by 70 maximal isokinetic-resisted movements of the elbow flexors. The variability in appearance and time of onset

of an

inflammatory

response

may

be related to the extent of injury produced by the exercise. Much more strain was exerted on muscle in the studies by Nikolau et al and Stauber et al than in ours. There was poor correlation between the perceived peak grade of soreness overall and the peak CK level. This supports the observations of Newham (23), who noted no obvious

relationship

tude was

between

of CK efflux also

poor

and

the

DOMS.

correlation

described

by

several

our

results,

There

aging-guided the

184

#{149} Number

3

during

damage.

we propose biopsy

9.

11.

12.

14.

to perform

downhill 15. 16.

also noted in the article by Shelbock et al (3) despite highly controlled isobated exercise. Variations in muscle recruitment not previously recognized have been revealed with MR imaging after exercise (26). These are all important caveats when one considers many previous muscle injury studies that focused the biopsy on areas of DOMS because it was assumed that those were the ar-

magni-

On

that provides

the

basis

17. 18.

19.

20.

21.

of

MR irnmore

accurate information regarding the extent and location of muscle injury and should play an important role in future research and investigation of exercise-induced muscle injury. U

22.

23.

24.

authors

(2,3,24) were seen in only one of our subjects, who had more substantial overall increases in SI of muscle (indicative of greater injury). The fact that this subject’s peak CK level was not as high as others with less severe SI changes corroborates the findings

Volume

actions

of muscle

between

is thought

running, and we hypothesized that this would be the primary muscle injured (7). However, this was not the case. Variability in SI increase was

eas

perceived grade of DOMS in the region of biopsy and the degree of ULS injury. The perifascial SI aberrations previously

muscle

were injuried varexercise. The

8.

Acknowledgments: We thank Maria Morgan, Jerry Payne, Cindy Miller, Christine Ward, Roxann Polo, Ken Bourell, Wyman Schultz, and Andrea Katz for their technical assistance.

References 1.

FleckensteinJL, Canby RC, Parkey RW, Peshock RM. Acute effects of exercise on MR imaging of skeletal muscle in normal volunteers. AJR 1988; 151:231-237.

25. 26.

dynamic

RP, Saltin B. Water and muscle of humans, with extension. Am J Physiol

knee

1985; 248:190-196. Fleckenstein JL, Canby RC, Parkey RW, Peshock RM. Acute effects of exercise on MR Imaging of skeletal muscle in normal volunteers. AIR 1988; 151 :231-237. Friden J, Sjostrom M, Ekbolm B. A morphologic study of delayed muscle soreness. Experientia 1981; 37:506-507. Friden J, Sjostrom M, Ekbolm B. Myofibrillar damage following intense eccentric exercise in man. mt J Sports Med 1983; 4:170-176. Newham DJ, McPhail C, Mills KR, Edwards RH. Ultrastructural changes after concentric and eccentric contractions of human muscle. Neurol Sci 1983; 61:109-122. Hikida RS, Hagerman FC, Sherman WM, Costill DL. Muscle fiber necrosis associated with human marathon runners. J Neurol Sci 1983; 59:185-203. Armstrong RB, Ogilvie RW, Schwane JA. Eccentric exercise induced injury to rat skeletal muscle. J AppI Physiol 1983; 54:80-93. Bobbert MF,Hollander AP, Huijing PA. Factors in delayed onset muscular soreness in man. Med Sa Sports Exerc 1986; 18:75-81. Byrnes WC, Clarkson PM. Delayed onset muscle soreness and training. Clin Sports Med 1986; 5:605-614. Byrnes WC, Clarkson PM, White JS, et al. Delayed onset muscle soreness following repeated bouts ofdownhill running. J AppI Physiol 1985; 59:710-715. Clarkson PM, Tremblay I. Rapid adaptation to exercise-induced muscle damage. J AppI Physiol 1988; 65:1-6. Talag TS. Residual muscular soreness as influenced by concentric, eccentric, and static contractions. Res Q 1973; 44:458-469. Ebbeling CB, Clarkson PM. Exercise-induced muscle damage and adaption. Sports Med 1989; 7:207-234. Jones DA, Newham DJ, Round JM, Tolfree SE. Experimental human muscle damage: morphologic changes in relation to other indices of damage. J Physiol 1986; 375:435-448. Clarkson DM, Litchfield P. GravesJ, Kirwan J, Bymes WC. Serum creatine kinase activity following forearm flexion isometric exercise. J AppI Physiol Occup Physiol 1985; 53:368-371. Schwane JA, Johnson SR. Vandermakker CB, Armstrong RB. Delayed onset muscle soreness and plasma CPK and LDH activities after downhill running. Med Sd Sports Exerc 1983; 15:51-56. Nikolau PK, Macdonald BL, Glisson RR, Seaber AV, Garrett WE. Biomechanical and histological evaluation of muscle after controlled strain in’ur . Am J Sports Med 1987; 15:9-14. Stauber , Clarkson PM, Fritz VK, Evans WJ. Extracellular matrix disruption and pain after eccentric muscle action. J Appl Physiol 1990; 69:868-874. Newham DJ. The consequences of eccentric contractions and their relationships to delayed onset muscle pain. Eur J AppI Physiol 1988; 57:353-359. DeSmet AA, Fisher DR, Heiner JP, Keene JS. Magnetic resonance imaging of muscle tears. Skeletal Radiol 1990; 19:283-286. Kuipers H, Janssen E, Keizer H, Verstappen F. Serum CPK and amount of muscle damage in rats (abstr). Med Sd Sports Exerc 1985; 17:195. Fleckenstein JL, Bertocci LA, Nunnaly RL, Parkey RW, Peshock RM. Exercise-enhanced MR imaging of variations in forearm muscle anatomy and use: importance in MR spectroscopy. AIR 1989; 153:63-698.

Radiology

#{149} 869