Frank
G. Shellock,
Exertional of Concentric with Serial
PhD
#{149} Tetsuo
Fukunaga,
PhD2
#{149} Jerrold
H. Mink,
MD
#{149} V.
R. Edgerton,
Muscle Injury: Evaluation versus Eccentric Actions MR Imaging’
Eccentric muscular actions involve the forced lengthening or stretching of muscles and tend to produce cxertional injuries. This study used magnetic resonance (MR) imaging to serially evaluate muscles in five healthy, untrained subjects who performed exhaustive biceps exercisc by doing isolated eccentric and concentric actions with a dumbbell. Symptoms were assessed, and T2weighted images of the arms were obtained before exercise and i, 3,5, 10, 25, 40, 50, 60, and 80 days after exercise. Statistically significant increases in T2 relaxation times indicative of muscle injury occurred on each day of MR imaging evaluation in muscles performing eccentric actions, peaking on day 3 in two subjects; day 5, two subjects; and day 10, one subject. The pattern and cxtent of the abnormalities on MR images were variable. Pain, soreness, and joint stiffness were present on days i, 3, and 5 in muscles that performed eccentric actions. MR imaging showed subclinical abnormalities that lasted as long as 75 days after the disappearance of symptoms (two subjects). Muscles that performed concentric actions had no changes in T2 relaxation times and were asymptomatic throughout the study.
M
USCLE
injuries
are
the
most
fre-
quent form of injury that occurs during physical activities (1-4). Sports-related injuries to the muscles usually occur when exercise is intense, unaccustomed, of a long duration, or includes eccentric muscular actions (1,2,5-7). Eccentric muscular actions involve the forced active lengthening or stretching of muscles and are considered the primary cause of exertionrelated muscle injuries because excessive force develops in the muscle during this type of muscular action (ie, greater tension is produced in muscle fibers when they stretch than when they shorten) (1,5-7). Prior mesearch has demonstrated that eccentric actions are typically associated with muscle pain, soreness, ultrastructural changes indicative of musdc damage, and increased plasma levels of creatine kinase as well as other intracellular enzymes (5-18). By comparison, concentric (or shortening) muscle actions performed at the same relative work level do not produce the same degree of muscle injury, if any, that eccentric actions do (5,6,i2). In a previous study by Fleckenstein et al (19), magnetic resonance (MR) imaging was used to evaluate sports-related muscle injuries, and the authors examined untrained sub-
jects with muscle damage caused by unaccustomed exercise that involved a combination of eccentric and concentric muscular actions. Although the study by Fleckenstein et al (19) clearly demonstrated that MR imaging was useful for assessing exertional muscle injuries, it was not designed to enable distinction between muscle damage caused by concentric versus eccentric muscular actions. Because eccentric actions are most likely to produce exertion-related muscle injuries, our study was conducted with MR imaging to serially evaluate subjects who performed isolated eccentric and concentric actions and to determine whether any differences exist in (a) the presence and cxtent of muscle injuries produced by eccentric
versus
(b) the injuries
onset and produced
From
culoskeletal
Medical
the
Department Imaging
Center,
of MRI, Center,
8700 Beverly
Tower
Mus-
terms: Athletic injuries #{149} Extremities, injuries, 41.48, 41.833, 41.91 #{149} Extremities, MR studies, 41.1214 #{149} Magnetic resonance (MR), tissue characterization #{149} Muscles, injuries, 41.48, 41.833, 41.91 #{149} Muscles, MR studies, 41.1214 Radiology
1991; 179:659-664
J.H.M.);
Blvd, Los Ange-
and the Department
ology, University (T.F., V.R.E.). From sembly. Received requested January February 7; accepted print requests to 2 Current address: ences, University C RSNA, 1991
actions,
SUBJECTS
AND
METHODS
Subjects
Study
Five healthy volunteer subjects (three men and two women; average age, 36 years [range, 21-48 yearsj) participated in this
study.
These
individuals
were
un-
trained and had not performed any resintance training of the arms for a period of 6 months
ment
before
their
involve-
in this study.
Cedars-Sinai
les, CA 90048 (F.G.S., J.H.M.); Department of Radiological Sciences, University of California, Los Angeles School of Medicine, Los Angeles
(F.G.S.,
concentric
resolution of muscle by eccentric versus concentric actions, and (c) the relationship between muscle injuries and clinical symptoms produced by cccentric versus concentric actions.
at least 1
Index
PhD2
of Kinesi-
of California, Los Angeles the 1990 RSNA scientific asNovember 26, 1990; revision 29, 1991; revision received February 14. Address re-
Exercise
Protocol
A previously described exercise protocol was used to study exertional muscle injuries produced selectively by concentric
and
centage men)
eccentric
actions
(20).
A single
weighted to a normalized per(ie, 10% for women and 20% for
dumbbell
of the
subject’s
body
weight
was
F.G.S. Department of Sports of Tokyo, Tokyo.
Sd-
Abbreviations: tion
TE
=
echo
time,
TR
repeti-
time.
659
used for the resistance exercise. weights ranged from 12 to 15 lb women and from 28 to 30 lb for The subjects performed a “biceps movement for the exercise while standing position. One arm was randomly
to perform
isolated
The for the the men. curl” in a selected
50
Table 1 Estimated
40
Each
30
Measurement
U) .
,_
10
0
bell with the palm up, moving from extension to full flexion. The weight was then passed to the ipsilateral arm by an assistant to perform isolated eccentric (ie, lengthening) actions. This was accomplished by lowering the dumbbell with strict form, beginning with the arm at full flexion and lowering it to extension. The extremities
were
in
supinated
positions
throughout movement.
the range of motion of each The rate at which the concentric and eccentric actions took place was monitored, so that each movement lasted approximately 2 seconds. Using this protocol, the subjects performed concentric and eccentric actions in an alternating manner. Each subject exercised to the point of perceived exhaustion and “failure” (ie, the subject no longer could move the dumbbell). The concentric-action arm fatigued first in four of the subjects and the eccentric-action arm in the other. Exercise was stopped at this point to ensure that both
arms
performed
contractions
and
the
same
to compare
number
of
10 IMAGING
Figure
1.
25
40
50
INTERVAL
Graph
shows
60
with
T2 relaxation
(DAY)
T2 relaxation
times
0). Values
are
deviation;
the “T” lines
bar
means
represent
the
before
plus plus
times
exercise
or minus
(day
standard
of standard
de-
viation.
was made us and
between
radius,
the line of the humerthe arm hanging at side (i2).
with
rest at the subject’s MR
Imaging
Protocol
MR imaging was performed with a i.5T 64-MHz unit and a quadrature-driven, transmit/receive body coil (GE Medical Milwaukee).
Because
muscle
in-
juries
onds). listed
necessary image information was obtamed from both limbs for data analysis. The subjects were placed in a supine posi-
bers
sented in subsequent tables, figures, and text.) The subjects did not engage in any further physical activity that involved resistance training of the muscles used in this
study
during
the
ing evaluation
period
of MR imag-
(ie, for up to 80 days).
tend to be conspicuous on MR images when pulse sequences with a long echo time (TE) and repetition time (TR) are used (19,22,23), T2-weighted and proton
density,
imaging
msec);
field
ness;
pain
or soreness;
soreness; ness;
5, severe
pain
very severe pain Elbow stiffness arms ercise
average
pain
pain
or soreness;
or soreness. was assessed
quisition
tion
in
to keep
to a minimum
MR imager,
and
These data
while
images
ac-
the
were
obtained from the midforearms to the deltoids, with the subjects’ arms placed together over their heads and held in place with loosely applied cloth tape to motion
obtained and (n
=
(2i).
before i day
5),
(n
iO days
Serial
MR images (n = 5 pa5), 3 days (n 5), 5 (n = 5), 25 days (n =
exercise
i,
Data
mild
The
or
6,
the
of four of the five subjects before and on each day of MR imaging
#{149} Radiology
in the
gap.
selected
exby
correspond tables,
to those figures.
and
or brachialis
muscles,
had
inactive subject’s
depending
greater
signal
muscles middle the with
on
intensity)
and
(ie, the triceps) upper arms that
concentric special
care
of each per-
and eccentric acto avoid inclusion
of subcutaneous fat, fascia, blood vessels, or bone structures (20). T2 relaxation times were determined for these regions
of interest the
with
manufacturer T2 relaxation
forming before (days
the
provided
by
unit. biceps
per-
concentric and eccentric actions and on the days after exercise 1, 3, 5, 10, 25, 40, 50, 60, and 80)
were
compared
ance
for
with
repeated
differences
analysis
an analysis
measures
between
overall
these
of variance
of vari-
to determine values.
If the
showed
statis-
(P < .05), the data were
tical significance further analyzed ison
software
of the MR times of the
with
a multiple
compar-
test.
RESULTS Imaging
No abnormalities were observed in any of the muscles before exercise. Muscles that performed concentric actions had no changes in signal intensity, statistically significant changes in T2 relaxation times, or as-
sociated exercise
symptoms on days 1-80 after (Fig 1, Tables 2, 3). Statistically significant (P < .05) increases in T2 relaxation times ocin the biceps muscles performing eccentric actions on days 180 after exercise compared with baseline measurements (Fig 1). The highest mean T2 relaxation times occurred on days 3 and 5 and decreased toward the baseline value by day 80 curred
Analysis
after
images
times though icant,
were minimally increased, althese were statistically signifon days 40, 50, 60, and 80 com-
pared On
with days
chialis
and
were
obtained
with
stan-
dardized window settings, and the relative signal intensities of the muscles in the arms that performed concentric and eccentric actions were compared visually with those of the nonexercising muscles (ie, the triceps) (20). Regions of interest were selected in the center
numbers
subsequent
text.
MR
thick-
4), 40 days (n = 4), 50 days (n 4), 60 days (n 2), and 80 days (n 3) after exercise.
measuring the angle of elbow flexion with a goniometer (i2). The measurement 660
time
section
intersection
were
in
of inaxial
80 (TR msec/TE two excitations;
10-mm
subject
155 155 109 100 142
were
and of ion
or soreand
2-mm
parameters
tients)
3, moderate
4, above
and
of view;
images
the presence parameters:
44-cm
days
The subjective perceptions of pain soreness were determined on a scale 6 in each subject before exercise and each day of MR imaging, as follows: normal, no pain or soreness; 2, very
(SE)
plane; 2,000/20, 128 X 256 matrix;
inhibit
of Symptoms
spin-echo
obtained to determine jury with the following
were Assessment
These
formed tions,
loads. Therefore, the concentric and eccentric actions were performed at the same relative work levels. This exercise protocol was similar to those used by othera to study concentric versus eccentric actions (12,20) and was also designed to simulate resistive training techniques frequently used by body builders and strength trainers (2i). The estimated total work performed by each arm was calculated by measurement of power, as follows: power = mass (kilograms) X distance (meters)/time (secresults numpre-
S
Male Male Female Female Male
presented
which
at the top of each range
1 2 3 4 5
80
of the muscles before (day 0) and after (days 1, 3, 5, 10, 25, 40, 50, 60 and 80) the subjects performed exercise involving eccentric actions. A statistically significant (P < .05) increase in T2 relaxation times existed for each post-exercise imaging interval compared
Systems,
comparable
work
This calculation yielded the in Table 1. (Note that subject in Table 1 correspond to those
Sex
Subject*
This was accom-
actions.
Power (kg.m-sect)
20
concentric
by
Power
01
plished with strict form by bending the arm at the elbow and raising the dumb-
(ie, shortening)
Total Work Performed Calculated by
Arm,
of the
active
muscles
(ie, the
biceps
exercise.
The
T2 relaxation
the baseline level. 1-80 after exercise, biceps
muscles
formed creased
eccentric actions signal intensity
amount
and
spatial
bra-
that
per-
showed inthat varied in
distribution
(Figs
June
1991
Table 2 Subjective
Perceptions
of Pain Day
Associated
with
Ecc
Muscular Day
Ecc
Conc
Actions 5
Day
Conc
10
Conc
Ecc
Ecc
Conc
1 2 3 4 5
1 1 1 1 1
1 i 1 1 1
1 1 1 1 1
4 2 3 3 1
1 1 1 1 1
4 2 3 4 5
1 1 i 1 1
4 1 3 3 3
1 1 1 1 1
1 1 1 1 1
Mean
1
1
1
2.6
1
3.6
1
2.8
1
1
further changes occurred action, Day 0 pre-exercise,
after day 5. The scale for assessment Ecc eccentric action.
of subjective
perceptions
of symptoms
is described
in Subjects
and
Methods.
Conc
-
3 Elbow
in
Flexion
Angles
Associated
with
Concentric
and Eccentric
Muscular
Day 3
Actions
Day 5
Day 10
Subject
Conc
Ecc
Conc
Ecc
Conc
Ecc
Conc
Ecc
i 2 3
0 0 NA
0 5 NA
0 0 NA
10 5 NA
0 0 NA
10 5 NA
0 0 NA
0 0 NA
4
0
20
0
30
0
30
0
0
5
0
20
0
20
0
20
0
0
Mean
0
11.2
0
16.2
0
16.2
0
0
Note-Numbers concentric action,
2, 3). After
in columns 2-9 represent Ecc eccentric action, NA
careful
inspection
increase in angle not available.
in the exthat all intensity
changes,
found
at the
of the biceps
insertion muscles,
primarily
day
of se-
quential images obtained tremities, it was determined of the subjects had signal
site
of the brachialis and on the distal aspect of
the elbow joint, slightly higher Subject 1 had signal intensity
and up to a region than the middle arm. the least amount of changes that were fo-
cal in small areas of the brachialis muscle and somewhat diffuse in the biceps (Fig 3). Subjects 2 and 4 had marked increases in signal intensity that affected the entire brachialis and deep biceps muscles, with a diffuse distribution
in the
biceps (Fig increased
approximately
peripheral
aspects
3). Subject 3 had signal changes in
50%
of the
the biceps (Fig marked increased
3). Subject signal
5 had changes
that
affected the entire brachialis muscle and a significant portion of the biceps, with the exception of the lateral aspect of the The onset, the increased
biceps peak, signal
(Fig 3). and persistence intensity
were apparent eccentric-action
179
#{149} Number
in all muscles
3
subjects on
1 after
with
exercise.
pro-exercise
The
value
peak
in degrees.
signal
ish
for
four
three subjects was performed centric action, nal
intensity
of the
subjects.
Of
the
in whom MR imaging up to 80 days after econe had increased sigchanges
that
persisted
for 60 days (subject 4) and two had increased signal intensity changes that persisted for 80 days (subjects 3 and 5). In subjects 4 and 5, signal intensity changes were also localized to the subcutaneous tissue that extended to the middle portion of the forearm, to the
site
of muscle
injury
(Fig
4). Images obtained from each subject also demonstrated apparent (although not quantified) increases in the circumferences of the muscles affected by eccentric action that were predominantly seen on days 3, 5, and 10 (Fig 2). Symptoms
of
changes were slightly varied among the subjects. Small signal intensity
compared
intensity changes occurred on day 3 for subjects 3 and 4, on day 5 for subjects 1 and 5, and on day 10 for subject 2. On or after day 10, the signal intensity changes appeared to dimin-
distal
brachialis
muscle and a portion of the deep biceps, with no apparent signal intensity changes in the peripheral aspect of
Volume
Eccentric
3
Ecc
Day 1
changes in the
and
Day
Conc
Increase
of the marked
Concentric
1
Day
Subject
Note-No concentric
Table
and Soreness 0
Subjective perceptions of muscle pain and soreness occurred to varying degrees in each subject and only affected the arms that performed eccentric actions (Table 2). Four of the five subjects had symptoms on day i
No further
changes
occurred
after
day 5. Conc
-
after eccentric-action exercise. Mean peak symptoms occurred on day 3, and each subject was asymptomatic by day 10 after exercise involving eccentric actions (Table 2). Each subject reported that the primary site of pain and soreness was localized to the insertion sites of the biceps and brachialis muscles. Elbow flexion indicative of joint stiffness also occurred to varying degrees in each subject and only affected the arms that performed eccentric actions (Table 3). The largest mean increase in elbow flexion angles occurred on days 3 and 5 after exercise. The elbow flexion angles returned to the
preexercise
values
by
day
10 after
exercise. All
subjects
(particularly
subjects
4
and 5) had grossly apparent swelling and distention of the arms that performed eccentric action compared with the concentric-action arms; this swelling and distention was noted on days 3 and 5 after exercise and slightly decreased ecchymosis
on was
day 10. No associated noted in any of the
extremities. DISCUSSION Eccentric muscular actions produce a higher specific muscle tension than concentric actions and are therefore more likely to cause exertional musRadiology
#{149} 661
Figure
2.
mance
of eccentric
Axial
T2-weighted
SE (2,000/80) images obtained from the middle upper arm of subject 5 before (day 0) and serially The slight peripheral shading of the image obtained on day 0 was caused by slight contact of the magnet during MR imaging. Anatomy is best depicted on the day 1 image (biceps, solid arrows;
muscular
ject’s arm with the bore muscle, bordered by open arrows; triceps tendon, arrowhead). A subtle increase in signal intensity des on day 1 image after exercise. Day 3 image shows a more diffuse pattern of greater increased and almost the entire biceps muscles (with the exception of the lateral aspect of the biceps, which out
the
time
of the
MR
anatomy
of the affected
minishes
on
days
40,
imaging
evaluation).
muscles. 50,
and
The
60.
The
increased
Note
also
the
peak
increased
signal
intensity
on days
increase
in circumference
marked
obtained on days 3, 5, 10, and 25. The image obtained of the affected muscles. This subject had the severest actions.
‘j’
10 and
T2-weighted
SE (2,000/80)
signal
in the
biceps
intensity,
and
observed
brachialis
brachialis
mus-
in the brachialis
appears to have been unaffected through5, along with the greatest distortion in the compared with that on day 5 and further dimuscles, which is most apparent on images with regard to signal intensity as well as the size
is seen on day 25 is diminished of the affected
stiffness
associated
with
eccentric
muscular
#{149}
.‘
.--‘
-, ..,‘.
.
-
a,, -.,
,.
---
.‘
..
,,
j.,,
...,,
4.
5
4
aU)
exercise involving eccentric muscles. Anatomy is best depicted
chialis
“,,-
1)
‘1
intensity
is seen
:
.-
Axial-plane,
.
-“
\±: 3. day 5 after
signal
on day 80 shows a return to baseline symptoms of pain, soreness, and joint
A’’
Figure
after perforof the sub-
actions.
images
obtained
actions. Note the variability in subject 2 (biceps, solid
from
the middle
upper
in the arrow;
pattern brachialis
of increased muscle,
arms
of five subjects
signal bordered
changes by open
(numbered affecting arrows;
at bottom) the biceps and triceps tendon,
on braar-
rowhead).
cle injuries of muscle
(5-7). In fact, the majority strain injuries encountered
in sports-related
settings
are
believed
to be the result of eccentric actions (1-4). Muscles that cross two joints (such as the biceps, gastrocnemius, or rectus femoris) and that are used in the control of movement are most hable to this type of injury (i,5,6), as was seen in the muscles injured in our
study.
Previous trastructural centric and 662
studies that evaluated ulchanges related to coneccentric actions per-
#{149} Radiology
formed at comparable work levels have shown that concentric actions did not affect the muscles, while eccentric actions caused muscle damage (5,6,9,10,12,14). The immediate, postexercise muscle damage produced by the eccentric actions was considered mechanically
induced
and
was
rela-
tively minor (10,12,14). Muscle damage was seen to progressively increase over the subsequent few days because of mechanical and/or biochemical factors (iO,i2,i4). Therefore, the extent of muscle damage
produced by eccentric solely that of the initial strain; an even greater
actions is not mechanical amount of
damage occurs during cise period (5,6,10,12,14).
the
postexerThis, in
turn, causes other additional abnormal morphologic alterations of the muscle (ie, edema, distortion of anatomic features) and the associated symptoms (5,6,9,iO-i4,24). The symptoms related to exertional muscle injury follow a distinct pattern, referred to as delayed onset muscle soreness (5,6). Muscle pain,
June
1991
I
Figure
4.
Axial-plane, 12-weighted images obtained from
(2,000/80)
upper before
arm and middle forearm (a, c) and on day 5 after
involving
creased
V
0
O
eccentric
d.
cle,
soreness (5,6,12,19). These are usually localized to the or attachment of the mus-
that
is, the
deep creased signal intensity localized to the subcutaneous tissue of the forearm (b) that is distal to the site of the muscle injury. Anatomy is best depicted on d (biceps, solid arrow; brachialis muscle, open arrows; triceps
junction. In addition, gradually increase in the first 24 hours
peak
2-5
days
the symptoms in intensity withafter exercise,
after
exercise,
and
de-
crease until they disappear 7-10 days after exercise (5,6). The severity and duration of each component of the symptom pattern in delayed onset muscle soreness are varied and de-
pend
on the
training muscle amount
relative
level
of the muscles, the specific group injured, and the of muscle damaged, as well
as a myriad of other (5,6,9,12,14-17,25).
The quence torns injury
of our
previously of muscle
factors
mentioned changes
described in exertional are compatible with
study.
Muscles
eccentric actions with symptoms apparent swelling,
postulated intramuscular
that
seand sympthe
muscle results
performed
were associated of pain, soreness, and as well as measur-
able joint stiffness. of these symptoms
Volume
of prior
The precise is unknown
origin but is
to be related to increased fluid pressure, inflam-
179
#{149} Number
3
arrowhead).
Joint subject’s mation,
and/or
damage
to the
corre-
sponding connective tissues (5-8, 12,14,24). According to our data, it is possible that damaged connective tissue is one of the main sites responsible for symptoms,
musculotendinous
actions.
cumference and distortion of the normal shape of the involved muscles (Fig 2). In a study of eccentric actioninduced muscle injury, Frid#{233}net al (iO) hypothesized that disruption of the myofibrillar Z bands causes the development of degraded protein components and the release of protein-bound ions that, in turn, cause a buildup of edema that results in swelling (iO). Pain and soreness during delayed onset muscle soreness may be partially related to the tension that swelling from edema causes in the fibers of intramuscular connective tissue (10,12). However, it appears that the symptoms may disappear before the swelling is totally gone (12).
b.
muscle symptoms insertion
of subject 4 (b, d) exercise There is in-
signal intensity of the brachialis and biceps muscles (d) as well as an in-
tendon,
soreness, joint stiffness (if a joint is involved), and swelling are the cornmon symptoms of delayed onset
SE middle
the
the
most
because
pain
was
musculotendinous
in each
subject
localized junctions
to the of the
biceps and brachialis muscles, which were also seen to have the greatest spatial distribution of increased signal intensity site of soreness also correlates site of soreness
on
the and with and
MR images. This tissue damage the maximum muscle damage
produced by eccentric ed by others (9,10,12,13).
actions Pain
tors are known to be prevalent gions of the tendons and related
reportrecepin mecon-
nective tissues (26-28). Therefore, the musculotendinous junction should be carefully inspected when one evaluates exertional muscle damage with MR imaging (i9). Swelling of the involved extremity from edema accumulating in the damaged muscle typically develops shortly after severe exertional muscle injuries (5,6,10,12,24,29). This symptom was present in each subject and
involved the eccentric-action arm. Swelling could be appreciated on the MR images as an increase in the cir-
stiffness, manifested by unwillingness to extend
the the
affected limb so that it is held in a slight flexion (12), was observed to varying degrees in each subject in this
study.
Jones
In a previous
et al (12),
joint
study
by
stiffness
was
found 1-4 days after an eccentric-action exercise similar to the one used in our study. Joint stiffness related to
eccentric jury
action-induced
is believed
creased amassed pansion
and tive
muscle
to be caused
intramuscular edema that of the
pressure produces
muscle
in-
by in-
from an ex-
compartment
ensuing damage to the connectissue parallel to the affected
muscle
(10,12).
A previous muscle
study
injury
of exertional
caused
by
unaccus-
tomed exercise showed that damaged muscles are depicted on T2-weighted MR images as increased signal intensity
abnormalities
and
corresponding
increased T2 relaxation times that may persist without symptoms long after the physical event that caused the damage (19). These abnormal changes on MR images are considered to be predominantly the result of accumulated edema, with a minor contribution from hemorrhage that is produced in response to muscle injury(20).
In our tensity
study, and
increases
T2 relaxation
in signal times
Radiology
in-
were
.
663
observed only on the MR images of the muscles that performed eccentric actions. Normally, muscle damage that involves eccentric actions is not associated with bleeding (6,8), and therefore we suspect that the various MR imaging changes seen in the muscles in this study were primarily due to edema. However, we did not obtain images with Ti-weighted or gradient echo techniques during thin study to demonstrate the lack of intramuscular hemorrhage. Furthermore, the MR imaging abnormalities
seen
in this
study
fol-
lowed a consistent pattern: Signal intensity gradually increased over a few days after the initial exercise, peaked after several days, and slowly decreased toward normal after a penod as long as 80 days. These changes are compatible with the previously described course of exertional muscle injury (5,6). It should be noted that the length of time required for recovcry
of exertional
muscle
damage
is
variable and may be considerably long under certain circumstances (57,12,14,16,25). The increase in signal intensity and increased T2 relaxation times of the muscles that performed eccentric actions lasted up to 75 days longer than the symptoms in two of the subjects in this study. The significant delay between the disappearance of symptoms observed previously
and the on serial reported
abnormal
changes
MR images by
was
Fleckenstein
et al (19), who reported changes, observed with MR imaging, that persisted for up to 21 days after symptoms in subjects with exertional musdc injuries. Our subjects had an even longer period for a return to baseline MR imaging values, most likely because the muscle injuries induced by isolated eccentric actions were more severe. These data also support the study of Fleckenstein et al (19), which shows that the clinical assessment of muscle injuries may be insufficient to demonstrate the total recovcry of damaged tion-induced
muscles damage.
after
aging is performed only immediately after the initial injury (ie, within 24 hours), when there may be moderate to severe symptoms, the amount and distribution of muscle damage is unlikely to be fully recognized. The onset of symptoms does not correlate with the greatest appearance of musdc abnormalities seen with MR imaging. Peak abnormalities may appear 3, 5 or even 10 days after the muscle injury. Jones et al (12,14) also indicated that a poor correlation cxists between pain and muscle fiber damage, regardless of whether one considers the time course or extent of the damage. Therefore, because of the disparity between symptoms and MR imaging abnormalities, it is recommended that serial MR imaging be used to best characterize exertional muscle injuries. In two subjects with severe symptoms of pain, soreness, and joint stiffness and with the largest degree of increased signal changes in the affected muscles, increased signal intensity was localized in the subcutaneous fat around the forearm, distal to the site of muscle injury (Fig 4). This apparent exudate likely originated from the site of muscle damage and collected at this remote site because of a gravistatic movement of the fluid. Because of the intense symptoms and extent of MR imaging abnormalities, the finding of fluid removed from the area of muscle damage may indicate a more serious injury. Because the pattern of exertional muscle injury is somewhat variable among subjects (Fig 3), it is recommended that MR imaging be used to guide evaluations of eccentric action-induced injury with spectroscopy or biopsy to ensure that only the affected muscle is assessed (30). 0therwise, it is possible that the sample site may not include the injured musdc or that an admixture of normal and injured muscle may be sampled
8.
9.
10. 11.
12.
13.
14.
15. 16. 17. i8.
19.
20.
21.
22.
References i. 2.
Garrett WE. Muscle strain injuries: clinical and basic aspects. Med Sd Sports Exerc 1990; 22436-444. Glick JM. Muscle strains: prevention and treatment. Physician Sportsmed 1980; 8:7377.
3. 4.
Ryan AJ. Quadriceps strain, rupture, and charlie horse. Med Sri Sports Exerc 1969; 16:123-129. Salter RB. Textbook of disorders and injuries of the musculoskeletal system. Baltimore: Williams & Wilkins, 1983; 423. Armstrong RB. Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med Sci Sports Exerc i984; i6:529-538.
Stauber WT. Eccentric action of muscles: physiology. injury, and adaption. In: Exercise and sports sciences reviews. Philadelphia: Franklin Institute 1988; 157-185. Asmussen E. Observations on experimental muscle soreness. Acta Rheumatol Scand 1956; 2:109-i i6. Fritz VK. Stauber WT. Characterization of muscles injured by forced lengthening. II. Proteoglycans. Med Sri Sports Exerc 1988; 20:354-361. Newham DJ, Mills KR, Quigley BM, Edwards RHT. Pain and fatigue after concentric and eccentric muscle contractions. Clin Sd 1983; 64:55-62. Frid#{233}n J, Sj#{244}str#{244}m M, Ekblom B. A morphological study of delayed onset muscle soreness. Experientia 1981; 37:506-507. Newham DJ, Jones DA, Clarkson PM. Repeated high-force eccentric exercise: effects on muscle pain and damage. J AppI Physiol 1987; 63:1381-1386. Jones DA, Newham DJ, Clarkson PM. Skeletal muscle stiffness and pain following eccentric exercise of the elbow flexors. Pain 1987; 30:233-242. Clarkson PM, Fritz VK, Stauber WT. Extracellular matrix disruption in humans resultma from eccentric muscle action (abstr). Med Sci Sports Exerc 1989; 22(suppl):80. Jones DA, Newham DJ, Round JM, Tolfree SEJ. Experimental human muscle damage: morphological changes in relation to other indices of damage. J Physiol 1986; 375:435448. Armstrong RB, Ogilvie RW, Schwane JA. Eccentric exercise-induced injury to rat skeletal muscle. J AppI Physiol 1983; 54:80-93. Clarkson PM, Tremblay I. Exercise-induced muscle damage, repair, and adaption in humans. J Appl Physiol 1988; 65:1-6. Armstrong RB. Initial events in exercise-induced muscular injury. Med Sci Sports Exerc 1990; 22:429-435. Newham DJ, McPhail G, Mills KR, Edwards RHT. Ultrastructural changes after concentric and eccentric contractions of human musdc. J Neurol Sci 1983; 61:109-122. Fleckenstein JL, Wetherall PT, Parkey RW, Payne JA, Peschock RM. Sports-related musdc injuries: evaluation with MR imaging. Radiology 1989; 172:793-798. Shellock FG, Fukunaga T, Mink JH, Edgerton yR. Acute effects of exercise on MR imaging of skeletal muscle: concentric vs eccentric actions. AJR 1991; 156:765-768. Fleck SJ, Kraemer WJ. Designing resistance training programs. Champaign, Ill: Human Kinetics, 1987. Deutsch AL, Mink JH. Magnetic resonance imaging
23. 24.
25.
26. 27.
U
(30).
5.
#{149} Radiology
7.
exer-
The results of this study, which show occurrence of diverse MR imaging changes in damaged muscles at different points in time, demonstrate that a serial evaluation is likely needed for an accurate description and understanding of the associated abnormalities. For example, if MR im-
664
6.
28. 29. 30.
of musculoskeletal
injuries.
Radiol
Clin North Am 1989; 27:983-1002. Ehman RL, Berquist TH. Magnetic resonance imaging of musculoskeletal trauma. Radiol Clin North Am 1986; 24:291-319. Friden J, Sfakianos PN, Hargens AR. Muscle soreness and intramuscular fluid pressure: comparison between eccentric and concentric load. J AppI Physiol 1986; 61:2175-2179. Nimmo MA, Snow DH. Time course of ultrastructural changes in skeletal muscle after two types of exercise. J Appl Physiol 1982; 52:910-913. Carlsson CA, Pellettieri L. A clinical view on pain physiology. Acta Chir Scand 1982; 148:305-313. Kumazawa T, Mizumura K. Thin-fibre receptors responding to mechanical, chemical, and thermal stimulation in the skeletal musdc of the dog. J Physiol (Lond) 1977; 273:i79194. Stacey MJ. Free nerve endings in skeletal muscle of the cat. J Anat 1969; 105:23i-254. Brendstrup P. Late edema after muscular cxercise. Arch Phys Med Rehabil 1962; 43: 401-405. Fleckenstein JL, Canby RC, Parkey RW, Pcshock RM. Acute effect of exercise on MRI of skeletal muscle. AJR 1988; 151:231-237.
June
1991
G. Shellock,
Exertional of Concentric with Serial
PhD
#{149} Tetsuo
Fukunaga,
PhD2
#{149} Jerrold
H. Mink,
MD
#{149} V.
R. Edgerton,
Muscle Injury: Evaluation versus Eccentric Actions MR Imaging’
Eccentric muscular actions involve the forced lengthening or stretching of muscles and tend to produce cxertional injuries. This study used magnetic resonance (MR) imaging to serially evaluate muscles in five healthy, untrained subjects who performed exhaustive biceps exercisc by doing isolated eccentric and concentric actions with a dumbbell. Symptoms were assessed, and T2weighted images of the arms were obtained before exercise and i, 3,5, 10, 25, 40, 50, 60, and 80 days after exercise. Statistically significant increases in T2 relaxation times indicative of muscle injury occurred on each day of MR imaging evaluation in muscles performing eccentric actions, peaking on day 3 in two subjects; day 5, two subjects; and day 10, one subject. The pattern and cxtent of the abnormalities on MR images were variable. Pain, soreness, and joint stiffness were present on days i, 3, and 5 in muscles that performed eccentric actions. MR imaging showed subclinical abnormalities that lasted as long as 75 days after the disappearance of symptoms (two subjects). Muscles that performed concentric actions had no changes in T2 relaxation times and were asymptomatic throughout the study.
M
USCLE
injuries
are
the
most
fre-
quent form of injury that occurs during physical activities (1-4). Sports-related injuries to the muscles usually occur when exercise is intense, unaccustomed, of a long duration, or includes eccentric muscular actions (1,2,5-7). Eccentric muscular actions involve the forced active lengthening or stretching of muscles and are considered the primary cause of exertionrelated muscle injuries because excessive force develops in the muscle during this type of muscular action (ie, greater tension is produced in muscle fibers when they stretch than when they shorten) (1,5-7). Prior mesearch has demonstrated that eccentric actions are typically associated with muscle pain, soreness, ultrastructural changes indicative of musdc damage, and increased plasma levels of creatine kinase as well as other intracellular enzymes (5-18). By comparison, concentric (or shortening) muscle actions performed at the same relative work level do not produce the same degree of muscle injury, if any, that eccentric actions do (5,6,i2). In a previous study by Fleckenstein et al (19), magnetic resonance (MR) imaging was used to evaluate sports-related muscle injuries, and the authors examined untrained sub-
jects with muscle damage caused by unaccustomed exercise that involved a combination of eccentric and concentric muscular actions. Although the study by Fleckenstein et al (19) clearly demonstrated that MR imaging was useful for assessing exertional muscle injuries, it was not designed to enable distinction between muscle damage caused by concentric versus eccentric muscular actions. Because eccentric actions are most likely to produce exertion-related muscle injuries, our study was conducted with MR imaging to serially evaluate subjects who performed isolated eccentric and concentric actions and to determine whether any differences exist in (a) the presence and cxtent of muscle injuries produced by eccentric
versus
(b) the injuries
onset and produced
From
culoskeletal
Medical
the
Department Imaging
Center,
of MRI, Center,
8700 Beverly
Tower
Mus-
terms: Athletic injuries #{149} Extremities, injuries, 41.48, 41.833, 41.91 #{149} Extremities, MR studies, 41.1214 #{149} Magnetic resonance (MR), tissue characterization #{149} Muscles, injuries, 41.48, 41.833, 41.91 #{149} Muscles, MR studies, 41.1214 Radiology
1991; 179:659-664
J.H.M.);
Blvd, Los Ange-
and the Department
ology, University (T.F., V.R.E.). From sembly. Received requested January February 7; accepted print requests to 2 Current address: ences, University C RSNA, 1991
actions,
SUBJECTS
AND
METHODS
Subjects
Study
Five healthy volunteer subjects (three men and two women; average age, 36 years [range, 21-48 yearsj) participated in this
study.
These
individuals
were
un-
trained and had not performed any resintance training of the arms for a period of 6 months
ment
before
their
involve-
in this study.
Cedars-Sinai
les, CA 90048 (F.G.S., J.H.M.); Department of Radiological Sciences, University of California, Los Angeles School of Medicine, Los Angeles
(F.G.S.,
concentric
resolution of muscle by eccentric versus concentric actions, and (c) the relationship between muscle injuries and clinical symptoms produced by cccentric versus concentric actions.
at least 1
Index
PhD2
of Kinesi-
of California, Los Angeles the 1990 RSNA scientific asNovember 26, 1990; revision 29, 1991; revision received February 14. Address re-
Exercise
Protocol
A previously described exercise protocol was used to study exertional muscle injuries produced selectively by concentric
and
centage men)
eccentric
actions
(20).
A single
weighted to a normalized per(ie, 10% for women and 20% for
dumbbell
of the
subject’s
body
weight
was
F.G.S. Department of Sports of Tokyo, Tokyo.
Sd-
Abbreviations: tion
TE
=
echo
time,
TR
repeti-
time.
659
used for the resistance exercise. weights ranged from 12 to 15 lb women and from 28 to 30 lb for The subjects performed a “biceps movement for the exercise while standing position. One arm was randomly
to perform
isolated
The for the the men. curl” in a selected
50
Table 1 Estimated
40
Each
30
Measurement
U) .
,_
10
0
bell with the palm up, moving from extension to full flexion. The weight was then passed to the ipsilateral arm by an assistant to perform isolated eccentric (ie, lengthening) actions. This was accomplished by lowering the dumbbell with strict form, beginning with the arm at full flexion and lowering it to extension. The extremities
were
in
supinated
positions
throughout movement.
the range of motion of each The rate at which the concentric and eccentric actions took place was monitored, so that each movement lasted approximately 2 seconds. Using this protocol, the subjects performed concentric and eccentric actions in an alternating manner. Each subject exercised to the point of perceived exhaustion and “failure” (ie, the subject no longer could move the dumbbell). The concentric-action arm fatigued first in four of the subjects and the eccentric-action arm in the other. Exercise was stopped at this point to ensure that both
arms
performed
contractions
and
the
same
to compare
number
of
10 IMAGING
Figure
1.
25
40
50
INTERVAL
Graph
shows
60
with
T2 relaxation
(DAY)
T2 relaxation
times
0). Values
are
deviation;
the “T” lines
bar
means
represent
the
before
plus plus
times
exercise
or minus
(day
standard
of standard
de-
viation.
was made us and
between
radius,
the line of the humerthe arm hanging at side (i2).
with
rest at the subject’s MR
Imaging
Protocol
MR imaging was performed with a i.5T 64-MHz unit and a quadrature-driven, transmit/receive body coil (GE Medical Milwaukee).
Because
muscle
in-
juries
onds). listed
necessary image information was obtamed from both limbs for data analysis. The subjects were placed in a supine posi-
bers
sented in subsequent tables, figures, and text.) The subjects did not engage in any further physical activity that involved resistance training of the muscles used in this
study
during
the
ing evaluation
period
of MR imag-
(ie, for up to 80 days).
tend to be conspicuous on MR images when pulse sequences with a long echo time (TE) and repetition time (TR) are used (19,22,23), T2-weighted and proton
density,
imaging
msec);
field
ness;
pain
or soreness;
soreness; ness;
5, severe
pain
very severe pain Elbow stiffness arms ercise
average
pain
pain
or soreness;
or soreness. was assessed
quisition
tion
in
to keep
to a minimum
MR imager,
and
These data
while
images
ac-
the
were
obtained from the midforearms to the deltoids, with the subjects’ arms placed together over their heads and held in place with loosely applied cloth tape to motion
obtained and (n
=
(2i).
before i day
5),
(n
iO days
Serial
MR images (n = 5 pa5), 3 days (n 5), 5 (n = 5), 25 days (n =
exercise
i,
Data
mild
The
or
6,
the
of four of the five subjects before and on each day of MR imaging
#{149} Radiology
in the
gap.
selected
exby
correspond tables,
to those figures.
and
or brachialis
muscles,
had
inactive subject’s
depending
greater
signal
muscles middle the with
on
intensity)
and
(ie, the triceps) upper arms that
concentric special
care
of each per-
and eccentric acto avoid inclusion
of subcutaneous fat, fascia, blood vessels, or bone structures (20). T2 relaxation times were determined for these regions
of interest the
with
manufacturer T2 relaxation
forming before (days
the
provided
by
unit. biceps
per-
concentric and eccentric actions and on the days after exercise 1, 3, 5, 10, 25, 40, 50, 60, and 80)
were
compared
ance
for
with
repeated
differences
analysis
an analysis
measures
between
overall
these
of variance
of vari-
to determine values.
If the
showed
statis-
(P < .05), the data were
tical significance further analyzed ison
software
of the MR times of the
with
a multiple
compar-
test.
RESULTS Imaging
No abnormalities were observed in any of the muscles before exercise. Muscles that performed concentric actions had no changes in signal intensity, statistically significant changes in T2 relaxation times, or as-
sociated exercise
symptoms on days 1-80 after (Fig 1, Tables 2, 3). Statistically significant (P < .05) increases in T2 relaxation times ocin the biceps muscles performing eccentric actions on days 180 after exercise compared with baseline measurements (Fig 1). The highest mean T2 relaxation times occurred on days 3 and 5 and decreased toward the baseline value by day 80 curred
Analysis
after
images
times though icant,
were minimally increased, althese were statistically signifon days 40, 50, 60, and 80 com-
pared On
with days
chialis
and
were
obtained
with
stan-
dardized window settings, and the relative signal intensities of the muscles in the arms that performed concentric and eccentric actions were compared visually with those of the nonexercising muscles (ie, the triceps) (20). Regions of interest were selected in the center
numbers
subsequent
text.
MR
thick-
4), 40 days (n = 4), 50 days (n 4), 60 days (n 2), and 80 days (n 3) after exercise.
measuring the angle of elbow flexion with a goniometer (i2). The measurement 660
time
section
intersection
were
in
of inaxial
80 (TR msec/TE two excitations;
10-mm
subject
155 155 109 100 142
were
and of ion
or soreand
2-mm
parameters
tients)
3, moderate
4, above
and
of view;
images
the presence parameters:
44-cm
days
The subjective perceptions of pain soreness were determined on a scale 6 in each subject before exercise and each day of MR imaging, as follows: normal, no pain or soreness; 2, very
(SE)
plane; 2,000/20, 128 X 256 matrix;
inhibit
of Symptoms
spin-echo
obtained to determine jury with the following
were Assessment
These
formed tions,
loads. Therefore, the concentric and eccentric actions were performed at the same relative work levels. This exercise protocol was similar to those used by othera to study concentric versus eccentric actions (12,20) and was also designed to simulate resistive training techniques frequently used by body builders and strength trainers (2i). The estimated total work performed by each arm was calculated by measurement of power, as follows: power = mass (kilograms) X distance (meters)/time (secresults numpre-
S
Male Male Female Female Male
presented
which
at the top of each range
1 2 3 4 5
80
of the muscles before (day 0) and after (days 1, 3, 5, 10, 25, 40, 50, 60 and 80) the subjects performed exercise involving eccentric actions. A statistically significant (P < .05) increase in T2 relaxation times existed for each post-exercise imaging interval compared
Systems,
comparable
work
This calculation yielded the in Table 1. (Note that subject in Table 1 correspond to those
Sex
Subject*
This was accom-
actions.
Power (kg.m-sect)
20
concentric
by
Power
01
plished with strict form by bending the arm at the elbow and raising the dumb-
(ie, shortening)
Total Work Performed Calculated by
Arm,
of the
active
muscles
(ie, the
biceps
exercise.
The
T2 relaxation
the baseline level. 1-80 after exercise, biceps
muscles
formed creased
eccentric actions signal intensity
amount
and
spatial
bra-
that
per-
showed inthat varied in
distribution
(Figs
June
1991
Table 2 Subjective
Perceptions
of Pain Day
Associated
with
Ecc
Muscular Day
Ecc
Conc
Actions 5
Day
Conc
10
Conc
Ecc
Ecc
Conc
1 2 3 4 5
1 1 1 1 1
1 i 1 1 1
1 1 1 1 1
4 2 3 3 1
1 1 1 1 1
4 2 3 4 5
1 1 i 1 1
4 1 3 3 3
1 1 1 1 1
1 1 1 1 1
Mean
1
1
1
2.6
1
3.6
1
2.8
1
1
further changes occurred action, Day 0 pre-exercise,
after day 5. The scale for assessment Ecc eccentric action.
of subjective
perceptions
of symptoms
is described
in Subjects
and
Methods.
Conc
-
3 Elbow
in
Flexion
Angles
Associated
with
Concentric
and Eccentric
Muscular
Day 3
Actions
Day 5
Day 10
Subject
Conc
Ecc
Conc
Ecc
Conc
Ecc
Conc
Ecc
i 2 3
0 0 NA
0 5 NA
0 0 NA
10 5 NA
0 0 NA
10 5 NA
0 0 NA
0 0 NA
4
0
20
0
30
0
30
0
0
5
0
20
0
20
0
20
0
0
Mean
0
11.2
0
16.2
0
16.2
0
0
Note-Numbers concentric action,
2, 3). After
in columns 2-9 represent Ecc eccentric action, NA
careful
inspection
increase in angle not available.
in the exthat all intensity
changes,
found
at the
of the biceps
insertion muscles,
primarily
day
of se-
quential images obtained tremities, it was determined of the subjects had signal
site
of the brachialis and on the distal aspect of
the elbow joint, slightly higher Subject 1 had signal intensity
and up to a region than the middle arm. the least amount of changes that were fo-
cal in small areas of the brachialis muscle and somewhat diffuse in the biceps (Fig 3). Subjects 2 and 4 had marked increases in signal intensity that affected the entire brachialis and deep biceps muscles, with a diffuse distribution
in the
biceps (Fig increased
approximately
peripheral
aspects
3). Subject 3 had signal changes in
50%
of the
the biceps (Fig marked increased
3). Subject signal
5 had changes
that
affected the entire brachialis muscle and a significant portion of the biceps, with the exception of the lateral aspect of the The onset, the increased
biceps peak, signal
(Fig 3). and persistence intensity
were apparent eccentric-action
179
#{149} Number
in all muscles
3
subjects on
1 after
with
exercise.
pro-exercise
The
value
peak
in degrees.
signal
ish
for
four
three subjects was performed centric action, nal
intensity
of the
subjects.
Of
the
in whom MR imaging up to 80 days after econe had increased sigchanges
that
persisted
for 60 days (subject 4) and two had increased signal intensity changes that persisted for 80 days (subjects 3 and 5). In subjects 4 and 5, signal intensity changes were also localized to the subcutaneous tissue that extended to the middle portion of the forearm, to the
site
of muscle
injury
(Fig
4). Images obtained from each subject also demonstrated apparent (although not quantified) increases in the circumferences of the muscles affected by eccentric action that were predominantly seen on days 3, 5, and 10 (Fig 2). Symptoms
of
changes were slightly varied among the subjects. Small signal intensity
compared
intensity changes occurred on day 3 for subjects 3 and 4, on day 5 for subjects 1 and 5, and on day 10 for subject 2. On or after day 10, the signal intensity changes appeared to dimin-
distal
brachialis
muscle and a portion of the deep biceps, with no apparent signal intensity changes in the peripheral aspect of
Volume
Eccentric
3
Ecc
Day 1
changes in the
and
Day
Conc
Increase
of the marked
Concentric
1
Day
Subject
Note-No concentric
Table
and Soreness 0
Subjective perceptions of muscle pain and soreness occurred to varying degrees in each subject and only affected the arms that performed eccentric actions (Table 2). Four of the five subjects had symptoms on day i
No further
changes
occurred
after
day 5. Conc
-
after eccentric-action exercise. Mean peak symptoms occurred on day 3, and each subject was asymptomatic by day 10 after exercise involving eccentric actions (Table 2). Each subject reported that the primary site of pain and soreness was localized to the insertion sites of the biceps and brachialis muscles. Elbow flexion indicative of joint stiffness also occurred to varying degrees in each subject and only affected the arms that performed eccentric actions (Table 3). The largest mean increase in elbow flexion angles occurred on days 3 and 5 after exercise. The elbow flexion angles returned to the
preexercise
values
by
day
10 after
exercise. All
subjects
(particularly
subjects
4
and 5) had grossly apparent swelling and distention of the arms that performed eccentric action compared with the concentric-action arms; this swelling and distention was noted on days 3 and 5 after exercise and slightly decreased ecchymosis
on was
day 10. No associated noted in any of the
extremities. DISCUSSION Eccentric muscular actions produce a higher specific muscle tension than concentric actions and are therefore more likely to cause exertional musRadiology
#{149} 661
Figure
2.
mance
of eccentric
Axial
T2-weighted
SE (2,000/80) images obtained from the middle upper arm of subject 5 before (day 0) and serially The slight peripheral shading of the image obtained on day 0 was caused by slight contact of the magnet during MR imaging. Anatomy is best depicted on the day 1 image (biceps, solid arrows;
muscular
ject’s arm with the bore muscle, bordered by open arrows; triceps tendon, arrowhead). A subtle increase in signal intensity des on day 1 image after exercise. Day 3 image shows a more diffuse pattern of greater increased and almost the entire biceps muscles (with the exception of the lateral aspect of the biceps, which out
the
time
of the
MR
anatomy
of the affected
minishes
on
days
40,
imaging
evaluation).
muscles. 50,
and
The
60.
The
increased
Note
also
the
peak
increased
signal
intensity
on days
increase
in circumference
marked
obtained on days 3, 5, 10, and 25. The image obtained of the affected muscles. This subject had the severest actions.
‘j’
10 and
T2-weighted
SE (2,000/80)
signal
in the
biceps
intensity,
and
observed
brachialis
brachialis
mus-
in the brachialis
appears to have been unaffected through5, along with the greatest distortion in the compared with that on day 5 and further dimuscles, which is most apparent on images with regard to signal intensity as well as the size
is seen on day 25 is diminished of the affected
stiffness
associated
with
eccentric
muscular
#{149}
.‘
.--‘
-, ..,‘.
.
-
a,, -.,
,.
---
.‘
..
,,
j.,,
...,,
4.
5
4
aU)
exercise involving eccentric muscles. Anatomy is best depicted
chialis
“,,-
1)
‘1
intensity
is seen
:
.-
Axial-plane,
.
-“
\±: 3. day 5 after
signal
on day 80 shows a return to baseline symptoms of pain, soreness, and joint
A’’
Figure
after perforof the sub-
actions.
images
obtained
actions. Note the variability in subject 2 (biceps, solid
from
the middle
upper
in the arrow;
pattern brachialis
of increased muscle,
arms
of five subjects
signal bordered
changes by open
(numbered affecting arrows;
at bottom) the biceps and triceps tendon,
on braar-
rowhead).
cle injuries of muscle
(5-7). In fact, the majority strain injuries encountered
in sports-related
settings
are
believed
to be the result of eccentric actions (1-4). Muscles that cross two joints (such as the biceps, gastrocnemius, or rectus femoris) and that are used in the control of movement are most hable to this type of injury (i,5,6), as was seen in the muscles injured in our
study.
Previous trastructural centric and 662
studies that evaluated ulchanges related to coneccentric actions per-
#{149} Radiology
formed at comparable work levels have shown that concentric actions did not affect the muscles, while eccentric actions caused muscle damage (5,6,9,10,12,14). The immediate, postexercise muscle damage produced by the eccentric actions was considered mechanically
induced
and
was
rela-
tively minor (10,12,14). Muscle damage was seen to progressively increase over the subsequent few days because of mechanical and/or biochemical factors (iO,i2,i4). Therefore, the extent of muscle damage
produced by eccentric solely that of the initial strain; an even greater
actions is not mechanical amount of
damage occurs during cise period (5,6,10,12,14).
the
postexerThis, in
turn, causes other additional abnormal morphologic alterations of the muscle (ie, edema, distortion of anatomic features) and the associated symptoms (5,6,9,iO-i4,24). The symptoms related to exertional muscle injury follow a distinct pattern, referred to as delayed onset muscle soreness (5,6). Muscle pain,
June
1991
I
Figure
4.
Axial-plane, 12-weighted images obtained from
(2,000/80)
upper before
arm and middle forearm (a, c) and on day 5 after
involving
creased
V
0
O
eccentric
d.
cle,
soreness (5,6,12,19). These are usually localized to the or attachment of the mus-
that
is, the
deep creased signal intensity localized to the subcutaneous tissue of the forearm (b) that is distal to the site of the muscle injury. Anatomy is best depicted on d (biceps, solid arrow; brachialis muscle, open arrows; triceps
junction. In addition, gradually increase in the first 24 hours
peak
2-5
days
the symptoms in intensity withafter exercise,
after
exercise,
and
de-
crease until they disappear 7-10 days after exercise (5,6). The severity and duration of each component of the symptom pattern in delayed onset muscle soreness are varied and de-
pend
on the
training muscle amount
relative
level
of the muscles, the specific group injured, and the of muscle damaged, as well
as a myriad of other (5,6,9,12,14-17,25).
The quence torns injury
of our
previously of muscle
factors
mentioned changes
described in exertional are compatible with
study.
Muscles
eccentric actions with symptoms apparent swelling,
postulated intramuscular
that
seand sympthe
muscle results
performed
were associated of pain, soreness, and as well as measur-
able joint stiffness. of these symptoms
Volume
of prior
The precise is unknown
origin but is
to be related to increased fluid pressure, inflam-
179
#{149} Number
3
arrowhead).
Joint subject’s mation,
and/or
damage
to the
corre-
sponding connective tissues (5-8, 12,14,24). According to our data, it is possible that damaged connective tissue is one of the main sites responsible for symptoms,
musculotendinous
actions.
cumference and distortion of the normal shape of the involved muscles (Fig 2). In a study of eccentric actioninduced muscle injury, Frid#{233}net al (iO) hypothesized that disruption of the myofibrillar Z bands causes the development of degraded protein components and the release of protein-bound ions that, in turn, cause a buildup of edema that results in swelling (iO). Pain and soreness during delayed onset muscle soreness may be partially related to the tension that swelling from edema causes in the fibers of intramuscular connective tissue (10,12). However, it appears that the symptoms may disappear before the swelling is totally gone (12).
b.
muscle symptoms insertion
of subject 4 (b, d) exercise There is in-
signal intensity of the brachialis and biceps muscles (d) as well as an in-
tendon,
soreness, joint stiffness (if a joint is involved), and swelling are the cornmon symptoms of delayed onset
SE middle
the
the
most
because
pain
was
musculotendinous
in each
subject
localized junctions
to the of the
biceps and brachialis muscles, which were also seen to have the greatest spatial distribution of increased signal intensity site of soreness also correlates site of soreness
on
the and with and
MR images. This tissue damage the maximum muscle damage
produced by eccentric ed by others (9,10,12,13).
actions Pain
tors are known to be prevalent gions of the tendons and related
reportrecepin mecon-
nective tissues (26-28). Therefore, the musculotendinous junction should be carefully inspected when one evaluates exertional muscle damage with MR imaging (i9). Swelling of the involved extremity from edema accumulating in the damaged muscle typically develops shortly after severe exertional muscle injuries (5,6,10,12,24,29). This symptom was present in each subject and
involved the eccentric-action arm. Swelling could be appreciated on the MR images as an increase in the cir-
stiffness, manifested by unwillingness to extend
the the
affected limb so that it is held in a slight flexion (12), was observed to varying degrees in each subject in this
study.
Jones
In a previous
et al (12),
joint
study
by
stiffness
was
found 1-4 days after an eccentric-action exercise similar to the one used in our study. Joint stiffness related to
eccentric jury
action-induced
is believed
creased amassed pansion
and tive
muscle
to be caused
intramuscular edema that of the
pressure produces
muscle
in-
by in-
from an ex-
compartment
ensuing damage to the connectissue parallel to the affected
muscle
(10,12).
A previous muscle
study
injury
of exertional
caused
by
unaccus-
tomed exercise showed that damaged muscles are depicted on T2-weighted MR images as increased signal intensity
abnormalities
and
corresponding
increased T2 relaxation times that may persist without symptoms long after the physical event that caused the damage (19). These abnormal changes on MR images are considered to be predominantly the result of accumulated edema, with a minor contribution from hemorrhage that is produced in response to muscle injury(20).
In our tensity
study, and
increases
T2 relaxation
in signal times
Radiology
in-
were
.
663
observed only on the MR images of the muscles that performed eccentric actions. Normally, muscle damage that involves eccentric actions is not associated with bleeding (6,8), and therefore we suspect that the various MR imaging changes seen in the muscles in this study were primarily due to edema. However, we did not obtain images with Ti-weighted or gradient echo techniques during thin study to demonstrate the lack of intramuscular hemorrhage. Furthermore, the MR imaging abnormalities
seen
in this
study
fol-
lowed a consistent pattern: Signal intensity gradually increased over a few days after the initial exercise, peaked after several days, and slowly decreased toward normal after a penod as long as 80 days. These changes are compatible with the previously described course of exertional muscle injury (5,6). It should be noted that the length of time required for recovcry
of exertional
muscle
damage
is
variable and may be considerably long under certain circumstances (57,12,14,16,25). The increase in signal intensity and increased T2 relaxation times of the muscles that performed eccentric actions lasted up to 75 days longer than the symptoms in two of the subjects in this study. The significant delay between the disappearance of symptoms observed previously
and the on serial reported
abnormal
changes
MR images by
was
Fleckenstein
et al (19), who reported changes, observed with MR imaging, that persisted for up to 21 days after symptoms in subjects with exertional musdc injuries. Our subjects had an even longer period for a return to baseline MR imaging values, most likely because the muscle injuries induced by isolated eccentric actions were more severe. These data also support the study of Fleckenstein et al (19), which shows that the clinical assessment of muscle injuries may be insufficient to demonstrate the total recovcry of damaged tion-induced
muscles damage.
after
aging is performed only immediately after the initial injury (ie, within 24 hours), when there may be moderate to severe symptoms, the amount and distribution of muscle damage is unlikely to be fully recognized. The onset of symptoms does not correlate with the greatest appearance of musdc abnormalities seen with MR imaging. Peak abnormalities may appear 3, 5 or even 10 days after the muscle injury. Jones et al (12,14) also indicated that a poor correlation cxists between pain and muscle fiber damage, regardless of whether one considers the time course or extent of the damage. Therefore, because of the disparity between symptoms and MR imaging abnormalities, it is recommended that serial MR imaging be used to best characterize exertional muscle injuries. In two subjects with severe symptoms of pain, soreness, and joint stiffness and with the largest degree of increased signal changes in the affected muscles, increased signal intensity was localized in the subcutaneous fat around the forearm, distal to the site of muscle injury (Fig 4). This apparent exudate likely originated from the site of muscle damage and collected at this remote site because of a gravistatic movement of the fluid. Because of the intense symptoms and extent of MR imaging abnormalities, the finding of fluid removed from the area of muscle damage may indicate a more serious injury. Because the pattern of exertional muscle injury is somewhat variable among subjects (Fig 3), it is recommended that MR imaging be used to guide evaluations of eccentric action-induced injury with spectroscopy or biopsy to ensure that only the affected muscle is assessed (30). 0therwise, it is possible that the sample site may not include the injured musdc or that an admixture of normal and injured muscle may be sampled
8.
9.
10. 11.
12.
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15. 16. 17. i8.
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20.
21.
22.
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#{149} Radiology
7.
exer-
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June
1991
