Journal of Exercise Physiology(JEP)

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NSAIDS and GAIT


11

Journal of Exercise Physiology
online

(JEP
online
)


Volume 12 Number 5 October 2009



Managing Editor

Tommy Boone, PhD, MPH

Editor
-
in
-
Chief

Jon K. Linderman, PhD

Review Board

Todd Astorino, PhD

Julien Baker, PhD

Tommy Boone, PhD

Larry Birnbaum, PhD

Eric Goulet, PhD

Robert Gotshall, PhD

M. Knight
-
Maloney, PhD

Len Kravitz, PhD

James Laskin,

PhD

Derek Marks, PhD

Cristine Mermier, PhD

Chantal Vella, PhD

Ben Zhou, PhD



Official

Research Journal of


the

American Society of
Exercise Physiologists
(ASEP)


ISSN 1097
-
975









Clinical Exercise Physiology


Exercise
-
Induced Muscle Injury and Influence of N
SAID

Therapy on
Kinematics of Downhill Walking in Older Adults


ANGELA BALDWIN LANIER
1
, KATHY SIMPSON
2
, CHRIS GREGORY
3
,
SCOTT WALTER STEVENSON
4
, HENRY WANG
5
, GARY
DUDLEY
6


1
Department of Kinesiology, Berry College, Mount Berry GA, USA

2
Department
of Kinesiology, The University of Georgia, Athens GA, USA

3
Department of
Physical Therapy, University of Florida, Gainesville FL, USA

4
Tucson Fitness
and Wellness Center, T
ucson AZ, USA

5
School of Physical Education, Sport,
and Exercise Science, Muncie IN, USA

6
Deceased


ABSTRACT


Lanier AB, Simpson KJ, Gregory C
,
Stevenson SW, Wang H,
Dudley, G.
Exercise
-
Induced Muscle Injury and Influence of N
SAID

Therapy on Kinematics of

Downhill Walking in Older Adults
.

JEP
online

2009;1
2
(5
):
11
-
21.

Non
-
steroidal anti
-
inflammatory drug (NSAID) therapy
appears to be beneficial in reducing the inflammatory response to
exercise

in older individuals
. The purpose of this study is to determine i
f
NSAID

therapy is eff
ective for alleviating exercise
-
induced muscle
dysfunction

measured by gait kinematics.

In th
e

double
-
blind cross
-
over

study, 15 older adults (
60

±

8 yr) performed 8 sets of 8 unilateral
eccentric (ECC) knee extension actions at 75% o
f the maximum load
that could be lowered once, then consumed naproxen

sodium or placebo
for 10 days.

Video data of pa
rticipants' gait during decline walking were
collected.
Participants exhibited the following gait alterations:

shorter
step l
ength (p

=

0.0
4
), reduced support time (p

=

0.00), and more
posterior relat
ive center of mass positions (p

=

0.
02).

There were n
o
significant (p

<

0.05) gait changes detected for the NSAID trial. Gait
alterations were moderately correlated with indice
s
of muscle injury

(p

<

0.05).
These results suggest that

NSAID’s may protect against
alterations in downhill gait following novel ECC exercise

in older
individuals
.


Key Words
: Delayed Onset Muscle Soreness, Gait, Eccentric,
Dysfunction, Muscle Damage
.






NSAIDS and GAIT


12

INTRODUCTION


O
lder adults are increasingly encouraged to remain or become physically active thro
ugh formal
exercise programs.
Likewise, resistance exercise is often prescribed to restore strength and mobility
following imposed inactivity

(1,2).

Paradoxically, such novel

exercise can cause muscle injury,
infla
mmation, weakness, and soreness

(3,4)

among older adults who may be more susceptible to
contraction
-
induced injury than younger adults

(5).

For older adults, it could be especially desirable to
prevent these exercis
e
-
induced responses that can alter gait biomechanics during walking and
temporarily impair the
performance of daily activities (6).



Downhill walking kinematics may be especially affected by knee extensor muscle soreness, as
greater eccentric knee extenso
r torque occurs during
downhill compared to level gait (7).
It has been
suggested that for downhill compared to level walking, increased duration of eccentric activity of the
knee extensor muscles helps lower the body in a controlled manner and to stabiliz
e the knee joint

(7,8).

We hypothesized that if novel eccentric exercise induced muscle
-
related
responses in the knee
extensors

(e.g., muscle injury), the downhill gait kinematics would also be affected.


Additionally, whether the use of a NSAID by older

adults can diminish or prevent any potential gait
alterations that may be associated with the muscle injury responses to novel eccentric exer
cise has
not been ascertained.
The effect of NSAIDs on preventing neuromuscular dysfunction has been
controversial
. While some studies suggest that NSAIDS may be beneficial for reducing muscle
soreness and/or dysfuncti
on following eccentric exercise
(9
-
15)
,

other studies do not support those
findings

(16
-
19).

The goals of this study of healthy, older adults were to d
etermine
:

1)
if
performing a
single bout of novel eccentric exercise that induces muscle
-
related responses (i.e., loss of muscle
strength, inflammation and soreness) also alters gait kinematics; 2)
if the

gait alterations are
associated with muscle
-
related

responses; and 3)
if
NSAID therapy attenuates these alterations in
gait during downhill walking.


METHODS


Research Design

A double
-
blind crossover design (different lower limb for each drug trial) was employed

(
4,9).

Unilateral limb exercise was performe
d to avoid the protective effect of eccentric exercise

(20,21).

The protective effect, or repeated bout effect, is an adaptation to eccentric exercise that increases
resistance to muscle injury and reduces the severity of soreness and neuromuscular dysfunc
tion.


After attending four familiarization sessions to practice performing maximal effort unilateral concentric
actions using each

quadriceps femoris, the following pre
-
exercise data were obtained:
1)
concentric
one
-
repetition maximum (1RM),
2)
maximal i
sometric force, and
3)
resting magnetic resonance
images of both thighs

(
4,9,21,22
).
Additionally, participants were videotaped while wal
king down a
16% declined ramp.
One week after pre
-
exercise data were obtained, novel eccentric exercise of the
right or

left quadriceps femoris

was performed (Day 1).
Drug or placebo was administered for 10
days, beginni
ng immediately after exercise.

Magnetic resonance images of each quadriceps femoris,
video of downhill walking, and isometric and concentric strength data

were again gathered

on Days 3
and 10 of recovery.
Quadriceps soreness was recorded on these day
s using a visual analog scale.
After a three
-
week washout, the protocol was repeated with the contralateral limb, and the drug or
placebo crossed
-
over.


Subject
s

Fifteen healthy, but not resistance
-
trained
male (n =
10
) and post
-
menopausal female (n =
5)

NSAIDS and GAIT


13

participants (mean ± SD; 60 ±
8 yr, 176 ± 8 cm, 80 ± 16

kg) with no history of neuromuscular
problems/inju
ries participated in the study.

Many persons beyond thi
s age (> 70 years) have a history
of chronic NSAID use that could increase the participants’ risk for gastrointestinal problems duri
ng
participation of this study.

Thus, we felt that recreationally active older, but not elderly subjects were
appropriate pa
rticipants for this investigation.


Procedures, risks
,

and benefits were explained and
an
informed written consent
was
obtained after
approval by the Institutional R
eview Board of the university.
No subjects reported taking NSAIDs
during

the month prior to

the study.
The only drugs that the participants were allowed to ingest were
the p
rescribed NSAID or placebo.

Additionally, participants were asked to refrain from any form of
resistance training during the duration of the study.


Procedures

Gait Analysis

Fifteen healt
hy but not
res
istance
-
trained

male (n = 10) and post
-
menopausal female (n = 5)

participants
were videotaped (120 Hz) from a sagittal view of the involved limb while walking down a
16% grade at a self
-
selected pace for five trials.
Two photocel
ls 4 m apart were used to de
termine
average walking speed.
Spatial locations of the body were captured with fourteen markers placed
over anatomical landmarks; two markers were placed on the 16% declined ramp

(
7
).

Indelible ink was
used to identify anatomic
al locations to ensure consistent placement of mark
ers on subsequent
testing days.

Each participant wore his/her same footwear for all days of data collection.


For each participant, reflective markers locations were digitized (Peak Motus Motion Measuremen
t
System
TM
, vl.1) for 1 stride initiated by the involved limb. Kinematic data were filtered using a fourth
-
order Butterworth fil
ter (cutoff frequency = 5 Hz).
Kinematic variables

(n = 6)

of the
involved limb were
calculated.
Temporal variables (e.g., tota
l support time), were expressed relative to the total stride
time. For the instant of touchdown of the involved limb, trunk inclination (relative to horizontal axis),
horizontal distance between the line of gravity and the heel of the involved limb (relat
ive to the
horizontal length of the base of support) and step length (%
of leg length) were generated.
During the
single stance phase, maximum vertical velocity of the center of mass of t
he body was calculated.
For
each
of the 15 participants

and
six
varia
ble
s
, the mean of the five trials was analyzed.


Strength Tests a
nd Eccentric Exercise

The unilateral

quadriceps femoris concentric 1RM test and the eccentric exercise were performed on
an isotonic knee extension machine (Badger
-
Magnum; Milwaukee, WI)

(
4,
9,21
-
23
).

The participants
completed a 4
-
week familiarization in order to
establish a best voluntary 1RM.

Two efforts during
each familiarization session were performed so as to avoid a training effect. For determining the
maximal voluntary isometric stren
gth, the contractions were performed at a 45° knee angle on a Kin
-
Com
TM

knee extension dynamometer (Chattanooga Group, Inc., Chattanooga, TN).


During the eccentric exercise session (
D
ay 1), the participant's goal was to perform 8 sets of 7
-

10
eccentric

repetitions (90 s rest between sets)

(
4,9,21
-
23
).

The load (75% of the eccentric 1RM) was
reduced if necessary so the partic
ipant could complete the task.
The eccentric load was estimated
from the concentric 1RM for two reasons: 1) The eccentric 1RM is ap
proximately 1.4 times concentric
1RM

(
24
)
; and 2) concentric
-
only familiarization and strength testing avoided eliciting a "protective
effect" before the eccentric bout

(
21
).


Pharmacology

Participants consumed one capsule of naproxen sodium (220 mg) or su
crose placebo three times
daily (every 8 hours) for 10 days, beginning immediately after the eccentric

bout.
Randomly assigned

NSAIDS and GAIT


14

0
1
2
3
4
Pre
3
10
Day
Walking Velocity (m/s)
Drug Trial
Placebo Trial
prepackaged capsules blinded the investigators and participants. All capsule containers
were
returned
empty
after the study, sugg
esting 100% compliance.


Magnetic Resonance Imaging and Analysis

Muscle injury was assessed with MR imaging

(
4,9,21
-
23
).

Transaxial images (TR/TE 2000/30 60, 256
by 256 matrix, 40 cm FOV, 1 NEX) 1.0 cm thick with a 0.5 cm gap between slices were obtained f
rom
the knee joint to the head of the femur. Magnetic resonance images were analyzed for determination
of muscle cross
-
sectional area and muscle injury (T
2
) using National Institute of Health Image
software. Shifts in transverse (spin
-
spin) relaxation tim
es as indicated by T
2

values have been used
as an objective m
ethod to quantify muscle injury (
4,9,21
-
23
).


For each participant, data were averaged over the 12 contiguous images immediately inferior to the
gluteus maximus
.

The reliability (squared intracla
ss correlation coefficient [R
2
]) of a CSA measure on
different days was 0.98.


Soreness Ratings

The s
ubjects rated soreness in each quadriceps femoris on a visual analog scale when seated (hips
and knees at approximately 90°) and while sitting down withou
t upper body assistance

(
9,25
).

The
100 mm visual analog scale was anchored with "no pain" and "extremely painful"

(
26
-
28
).



Statistical Analysis

Variables were analyzed with a
two
-
way repeated measures
(drug/placebo trial x time) analysis
of variance

(
ANOVA).


If the
sphericity assumption was not
met, the Huyne
-
Feldt adjustment
was made so that the F ratio was
not positively biased

(
30
).


Specific differences were
analyzed by the least squares
means tes
t.

To determine the
relationships between gait
alte
rations and neuromuscular
responses to eccentric exercise,
Pearson product correlations were
per
formed using difference
scores.

For a given variable, the
mean difference score was
calculated for the placebo and
drug trials on day 3 or 10 by
subtracting the

trial mean from
the pre
-
exercise mean. The level of statistical significance was set at
p

< 0.05.

Data are presented as
mean ± standard deviation (M ± SD).


RESULTS


For average walking velocity, there were no main effects for trial and time (
p

>
0.05) a
s shown in
Figure 1.
Therefore, it was concluded that walking velocity was unlikely to have affecte
d the observed
gait variables.
For step length, the results of the ANOVA for the involved leg showed a trial x time
Figure 1
.
Walking velocity (m/s) down a 16% ramp Pre
-
exercise, 3 and 10 d
ays after eccentric exercise. Walking
velocity was not statistically significant during both trials
(
p

> 0.05 for all). Mean ± SD; n = 15.


NSAIDS and GAIT


15

20
25
30
35
40
Pre
3
10
Day
Step Length
(% of leg length)
Drug Trial
Placebo Trial
*
Table 1.
Correlations between the difference scores of selected kinematic a
nd
neuromuscular response variables. (*
p

< 0.05).



Gait Variables


Neuromuscular
Responses


LnGravDist

(% of base
of support)

Step Length
(involved leg)

Relative Support
Time (involved leg)

1RM

-
0.22

0.52*

0.46

Maximum Isometric Force

-
0.23

0.38

0.57*

Cross Sectional Area of
Thigh Muscle

0.34

-
0.28

-
0.28

MRI T
2
(injured muscle)

0.38

-
0.34

-
0.59*

% CSA with Elevated T
2

0.32

-
0.32

-
0.48

Pain/Soreness Scale
During Movement

0.37

-
0.60*

-
0.39


interaction (
p

= 0.05).
The placebo trial

dis
played a significant
decrease
of 9%

for step length (
p

=
0.00) on day 3 compared to pre
-
exercise, whereas the drug trial displayed a
non
-
significant
increase
(
p

= 0.23; Figure 2). On day 10 of recovery compared to pre
-
exercise values, for the placebo t
rial,
step length f
or the involved leg
was still 5% less (
p

= 0.00).

For
step length of the uninvolved
leg, there were no significant
main effects (
p

= 0.75).

For
maximum vertical velocity of the
body's center of mass and trunk
inclination during touchdow
n for
the involved l
eg, there were no
significant different main effects
(
p

≥ 0.35).


The relative total support time
that the participants spent on the
involved leg also showed a trial
x time interaction (
p

= 0.00) due
to the placebo trial leg
exhibiting a 9% less (
p

= 0.04)
support time than the drug trial
limb on day 3 afte
r exercise
(Figure 3). Support time for the
placebo trial returned to pre
-
exercise by day 10 of recovery (p =
0.15).
The drug trial did not show any
significant differences in relative total support time on any day (p > 0.05).


As reflected by the trial
x
time interaction (
p

=
.02),
the relative distance
between the line of
gravity and the heel of
the involved limb at
touchdown increased
approximately 20% for
the placebo trial on
D
ay 3
compared to the pre
-
exercise value. The
relative distance between
the

line of gravity and the
heel of the involved limb
at touchdown did not
exhibit any statistical
differences across days
for the drug trials (
p

= 0.20) (Figure 4).


There were moderate (
r


≥ 0.50) correlations between changes in classical neuromuscular re
sponses
(9) and changes in gait responses between pre
-
exercise and placebo trials that were statistically
significant. Concentric 1RM strength decrements and muscle soreness were inversely related to
involved step length (
r



-
0.60;
p

≤ 0.02) on
D
ay 3.


Greater decreases in maximum isometric force

Figure 2. Step length as a % of limb length for the involved
limb du
ring decline walking down a 16% ramp Pre
-
exercise,
3 and 10 days after eccentric exercise. *Trial x time
interaction, due to a decrease for placebo (
p

= 0.00). Mean ±
SD; n = 15.


NSAIDS and GAIT


16

30
40
50
60
Pre
3
10
Day
Support Time
(% stride time)
Drug Trial
Placebo Trial
§
(
-
24 ± 4 %; p = 0.02) and muscle injury were associated with less relative time spent on the involved
leg (
r


-
0.59;
p

≤ 0.03) on
D
ay 3.


DISCUSSION


The objectives of this study were to determine for hea
lthy older adults, if a) a single bout of novel
eccentric exercise would elicit kinematic gait alterations; b) there would be any relationship between
changes in muscle
-
related responses and changes in gait responses following novel eccentric
exercise and,

c) NSAID therapy
would attenuate gait alterations.
In summary, from these data it is
suggested that novel eccentric
exercise affects t
he kinematics
of downhill gait.


Also, t
hese gait
alterations
are
likely

to

reflect
adaptations to compensate for
the bi
omechanical functions of
the muscles affected by the
neuromuscular responses to the
eccentric exercise.


The knee extensors are required
to produce eccentric force to
control knee flexion and to
stabilize the knee joint while
lowering the body either into

a
chair or during downhill walking

(
8,30,31
).
Th
erefore
, it seemed
likely that the muscle
-
induced
alterations of quadriceps femoris following eccentric exercise would be exacerbated during downhill
gait, while NSAIDs might limit
the potential gait alterat
ions.

As eccentric muscle actions of the knee
extensors control the forward and downward momentum of the body during the single support phase
of walking

(
32
),

we expected that after performing the eccentric bout, the step length and support time
of the inv
olved limb of the placebo would decrease while the values of the NSAID limb would be less
affected.


Indeed, for the involved limb during the placebo trial, after novel eccentric exercise was performed,
decreased step length and relative support time, and
increased relative distance between the line of
gravity and the heel of the invol
ved limb at touchdown occurred.

Relative to pre
-
exercise values, the
gait alterations were most notable on
D
ay 3 following eccentric exercise (Figures 1
-
4) as were the

classic
al muscular responses.
These findings suggest that participants were attempting to reduce the
demands on the involved limb knee extensors during downhill gait for the placebo trial, particularly for
D
ay 3 in contrast to

the pre
-
exercise trial.

Decreased in
volved limb step length served to minimize the
vertical distance that the body dropped during the involved limb swing phase.


Furthermore, the increased relative distance between the line of gravity and the heel of the involved
limb at touchdown combined
with shorter relative step length and relative total support time may
indicate that the participants were maintaining relatively more of their weight on the noninvolved limb
during th
e initial weight
-
bearing phase.

If so, the noninvolved limb during the pl
acebo trial versus the
pre
-
exercise trial would provide greater proportions of eccentric forces to reduce the downward
Figure 3. Relative support time on the involved limb Pre
-
e
xercise, Day 3 and Day 10 after eccentric exercise under
both trials. §Trial x time interaction (
p

= 0.00) due to a 7%
decrease during placebo trial (
p

= 0.04) relative to baseline.
Mean ± SD; n = 15.


NSAIDS and GAIT


17

0
10
20
30
40
50
Pre
3
10
Day
LnGravDist
(% of base of support)
Drug Trial
Placebo Trial
*
*
momentum of the body during the initial weight
-
bear
ing phase of the involved limb.


This may explain partly why no
significant difference
s for
maximum downward vertical
velocity were detected between
the placebo and pre
-
exercise
values.


Last, as the trunk inclination
values did not significantly vary
between pre
-
exercise and
placebo, trunk mass shifts are
unlikely to explain the poster
ior
shift of the body's line of gravity.
However, due to the reduced
knee extensor strength, this
posterior shift likely served to
help the participants maintain
balance while walking downhill.

The association between
muscle soreness and step
length also s
uggests that the
pain perceived when the knee
extensors act eccentrically during the gait cycle may
also influence gait kinematics.

Most likely, the
participants took shorter steps to reduce the leg extensor activation and soreness associated with
walking
downhill.


Although associations do not presume causality, the associations between neuromuscular responses
to eccentric exercise (e.g., strength decrements, and muscle injury) and relative support time and
step length support the surmised reasons for the

observed gait alterations. Quadriceps strength is
important in the ability to prevent a fall after a gait perturbation
, and in recovery from slipping (
33,34
).
To prevent functional loss and age
-
related gait changes, older adults are frequently encouraged

to
increase physical activity.

However, the initial novel bout of exercise following a period of disuse may
induce muscle injury, strength loss and soreness

(
5,23,35
),

and thereby further impair performance of
daily
-
living activ
ities (
36
), such as walking.

Although our participants were not old enough to be at
high risk for falling, research indicates that falls are not uncommon among healthy, 60
-
year
-
olds,
oftentimes increasing the fear of falling

(
1,37
).



Another interesting finding of this study was th
e effect of naproxen sodium on exe
rcise
-
induced gait
alterations.

It was expected that the effectiveness of the NSAID therapy in attenuating muscle
dysfunction and injury would reduce gait alterations, if indeed they a
re related.

Interestingly,
comparisons

between pre
-
exercise and NSAID treatment were not detected for any gait variables.
As maintaining dynamic strength and balance is important for preventing falls

(
2
),

particularly for
downhill or stair descent, naproxen sodium’s potential efficacy may hav
e particular importance for
older adults who may be at risk for falling, and/or at risk for reduced functional capacity due to
muscle
-
associated weakness.


Previously reviewed studies are inconsistent but suggest that some NSAIDs may be beneficial for
shor
t
-
term attenuation of the neuromuscular responses to eccentric exercise for younger and older
individuals

(
4,9,12
-
14
).

However, Mishra et al.

(
38
)

reported that while NSAID therapy attenuated
Figure 4. Horizontal distance between the line of g
ravity
and the heel of the involved limb at touchdown (relative to
the horizontal length of the base of support) (LnGravDist).
*Trial x time interaction, due to an increase for placebo

(
p

= 0.00). Mean ± SD; n = 15.


NSAIDS and GAIT


18

muscle dysfunction and the inflammatory response of rabbits for
the short term, it augmented the
long
-
term muscle dysfunction, suggesting that inflammation may play an integral role in the
adaptation of muscle to exercise. As we did not examine the participants beyond 10 days, our
findings only suggest that if an over
-
the
-
counter NSAID is taken on the day of exercise initiation and
is continued during the early stages of recovery, gait changes that are moderately related to typical
neuromuscular responses may be prevented in older individuals. Further investigation is w
arranted to
determine whether the gait changes following novel eccentric exercise adversely affect older adults.

Additionally, it is unknown whether NSAIDs would benefit a much older population, and/or individuals
with a history of falls. Other potential l
imitations of this study include, but are not limited to the lack of
follow
-
up on individuals’ long
-
term responses to NSAID use, and inability to determine gender
differences due to few female participants.


CONCLUSION


In conclusion, it is suggested that
novel eccentric exercise affects downhill gait by eliciting shorter
steps and decreased relative support time spent on the involved leg, and maintenance of the absolute
distance between the line of gravity and touchdown foot. Furthermore, these gait change
s may be
attenuated by NSAID therapy during the initial stages of a novel exercise program in older adults.



ACKNOWLEDGMENTS

We thank St. Mary's Hospital of Athens, GA (Debbie Eliopulos) for use of the MRI.


Address for Correspondence:
Lanier AB
, EdD
.

Berry College,
Department of Kinesiology
,
2277
Martha Berry Hwy
,
Box 5026
,
Mount Berry, GA 30149
, TEL 706
-
238
-
7807, FAX 706
-
802
-
6735
,
Email:
alanier@berry.edu
.


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Paschalis V, Giakas G, Baltzopoulos V, et al.
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NSAIDS and GAIT


19

8.


Tokuhir
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