Pain and Effusion and Quadriceps Activation and Strength

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Journal of Athletic Training 2013;48(2):186–191

doi: 10.4085/1062-6050-48.2.10
Ó by the National Athletic Trainers’ Association, Inc original research
www.natajournals.org

Pain and Effusion and Quadriceps Activation and


Strength
Riann M. Palmieri-Smith, PhD, ATC*†; Mark Villwock, MS*†;
Brian Downie, PA-C, MS‡; Garin Hecht, MD§; Ron Zernicke, PhD*†
*School of Kinesiology, University of Michigan, Ann Arbor; †Bone & Joint Injury Prevention & Rehabilitation Center,
University of Michigan, Ann Arbor; ‡MedSport, University of Michigan, Ann Arbor; §University of Michigan Medical
School, Ann Arbor

Context: Quadriceps dysfunction is a common consequence Results: Quadriceps strength and activation were highest
of knee joint injury and disease, yet its causes remain elusive. under the normal knee condition and differed from the 3
Objective: To determine the effects of pain on quadriceps experimental knee conditions (P , .05). No differences were
strength and activation and to learn if simultaneous pain and knee noted among the 3 experimental knee conditions for either
joint effusion affect the magnitude of quadriceps dysfunction. variable (P . .05).
Design: Crossover study.
Setting: University research laboratory. Conclusions: Both pain and effusion led to quadriceps
Patients or Other Participants: Fourteen (8 men, 6 dysfunction, but the interaction of the 2 stimuli did not increase
women; age ¼ 23.6 6 4.8 years, height ¼ 170.3 6 9.16 cm, the magnitude of the strength or activation deficits. Therefore,
mass ¼ 72.9 6 11.84 kg) healthy volunteers. pain and effusion can be considered equally potent in eliciting
Intervention(s): All participants were tested under 4 ran- quadriceps inhibition. Given that pain and effusion accompany
domized conditions: normal knee, effused knee, painful knee, numerous knee conditions, the prevalence of quadriceps
and effused and painful knee. dysfunction is likely high.
Main Outcome Measure(s): Quadriceps strength (Nm/kg)
and activation (central activation ratio) were assessed after each Key Words: arthrogenic muscle inhibition, central activation
condition was induced. failure, voluntary activation, muscles

Key Points
 Knee pain and effusion resulted in arthrogenic muscle inhibition and weakness of the quadriceps.
 The simultaneous presence of pain and effusion did not increase the magnitude of quadriceps dysfunction.
 To reduce arthrogenic muscle inhibition and improve muscle strength, clinicians should employ interventions that
target removing both pain and effusion.

Q uadriceps weakness is a common consequence of


traumatic knee joint injury1,2 and chronic degen-
erative knee joint conditions.3,4 Arthrogenic mus-
cle inhibition (AMI), a neurologic decline in muscle
can result in AMI,10–12 the effects of pain are less
understood despite many clinicians attributing AMI to
pain. Using techniques that introduce knee pain without
accompanying injury may provide insights into the role of
activation, results in quadriceps weakness and hinders pain in eliciting AMI.
rehabilitation by preventing gains in strength.5 The inability The degree of knee joint damage may play a role in the
to reverse AMI and restore muscle function can lead to quantity of AMI that manifests. Hurley et al13,14 demon-
decreased physical abilities,6 biomechanical deficits,7 and strated that quadriceps AMI, measured using an interpolat-
possibly reinjury.5 Furthermore, researchers8,9 have sug- ed-twitch technique, was greater in patients with extensive
gested that quadriceps weakness resulting from AMI may traumatic knee injury (eg, fractured tibial plateau, ruptured
place patients at risk for developing osteoarthritis in the medial collateral ligament, and medial meniscectomy) than
knee. In light of the substantial influence of quadriceps patients with isolated joint trauma (ie, isolated anterior
AMI on these clinically relevant outcomes, we need to cruciate ligament [ACL] rupture). Similarly, patients with
improve our understanding of the factors that contribute to more knee joint symptoms (ie, greater number of symptoms
this neurologic decline in muscle activity so efforts to target and increased severity of symptoms) may present with
and reverse it can be implemented and gains in strength can greater magnitudes of quadriceps inhibition. Recently,
be achieved more easily. investigators15 have suggested that patients with more pain
Joint injury and disease are accompanied by numerous display less quadriceps strength, supporting this tenet.
sequelae (ie, pain, swelling, tissue damage, inflammation), Given that effusion and pain often present simultaneously
so ascertaining which one ultimately leads to neurologic with joint injuries and diseases, such as ACL injury and
muscle dysfunction is difficult. Whereas a joint effusion osteoarthritis, examining both the isolated and cumulative

186 Volume 48  Number 2  April 2013


effects of these sequelae appears warranted to determine if for the other conditions, we quantified quadriceps strength
they influence the magnitude of muscle inhibition. and activation after the induction of an experimental knee
Experimental joint-effusion and pain models are safe and joint effusion (effused knee), experimental knee pain
effective experimental methods that allow for the isolated (painful knee), or experimental knee effusion and pain
examination of their effects on muscle function. The (effused and painful knee). Furthermore, to assess the
effusion model, whereby sterile saline is injected directly reliability of our dependent measures between days,
into the knee joint capsule,7 produces a clinically relevant baseline or normal knee testing occurred each day before
magnitude of the joint effusion that may be present with any injections. Each of the 4 conditions was tested on a
traumatic injury. Effusion is thought to activate group II separate day, and testing sessions were separated by 5 to 7
afferents responding to stretch or pressure,16–18 which in days. Randomization was completed using an online
turn may facilitate group Ib interneurons and result in research randomization Web site (http://www.randomizer.
quadriceps AMI.5 The pain model involves injecting com). The investigators were not blinded to condition, and
hypertonic saline into the infrapatellar fat pad to produce order allocation was not concealed. Data collection
anteromedial knee pain similar to that described in patients occurred around the same time of day (morning, afternoon,
with patellofemoral pain syndrome.19 Pain is considered to evening) for each condition for every participant.
initiate AMI through activation of group III and IV
afferents that act as nocioceptors to signal damage or Quadriceps Strength and Activation Procedures
potential damage to joint structures.16–18 The firing of these
afferents then may lead to facilitation of group Ib Participants were seated on an isokinetic dynamometer
interneurons, the flexion reflex, or the gamma loop, (Biodex System 3; Biodex Medical Systems, Inc, Shirley,
ultimately resulting in quadriceps inhibition.20 Thus, these NY) with their hips and knees flexed to 908 and their backs
models allow us to create symptoms that are associated supported. Their dominant lower extremities were secured
with knee injury and have the added benefit of providing a to the arm of the dynamometer with straps at both the
way to examine their effects in isolation. thighs and ankles, and their trunks were fixed to the chair
Therefore, the purpose of our study was to determine the with hook-and-loop straps. Self-adhesive, 5-cm 3 9-cm
effects of pain on quadriceps strength and activation and to electrodes (Dura-Stick II; Chattanooga Group, Hixson, TN)
learn if simultaneous pain and knee joint effusion would were placed proximally over the rectus femoris and distally
affect the magnitude of quadriceps dysfunction. We over the vastus medialis to deliver the stimuli for
hypothesized that pain alone would result in quadriceps quadriceps activation testing.
inhibition and that the magnitude of inhibition would be On each testing day and before any injections, partici-
greater when effusion and pain were present simultaneously. pants were instructed to perform 3 10-second maximal
voluntary isometric contractions (MVICs) for knee exten-
METHODS sion to familiarize them with the task. During all MVICs,
an investigator (M.V.) provided constant spoken encour-
Participants agement to promote the participant to extend the knee as
hard as he or she could. After the practice trials, 1 of the 4
Fifteen healthy individuals originally volunteered to conditions was induced. In the case of the normal knee
participate, but after receiving a knee-effusion injection, 1 condition, participants rested for 5 minutes and then
participant fainted and subsequently was removed from the performed the remaining MVICs for knee extension.
study at the discretion of the investigators. Therefore, 14 After the experimental condition was achieved, partici-
healthy participants (8 men, 6 women; age ¼ 23.6 6 4.8 pants were instructed to perform 3 additional MVICs for
years, height ¼ 170.3 6 9.16 cm, mass ¼ 72.9 6 11.84 kg) knee extension. These contractions were initiated within 2
were included in the study. Participants were excluded if minutes after the experimental condition was induced. In
they had a history of knee injury or surgery, had knee pain at addition to spoken feedback from the investigators, visual
the time of the study, had an allergy to lidocaine, had any feedback was provided whereby they were encouraged to
orthopaedic or rheumatologic disorder that affected the reach a target line on a computer screen that was set to a
lower extremity, or reported being pregnant. All participants torque value 10% above that of their MVICs recorded
provided written informed consent, and the study was during the familiarization trials. 22 A 2-minute rest was
approved by the Institutional Review Boards of the provided between contractions to minimize the effects of
University of Michigan Medical School. We recorded the fatigue. The torque signal generated from the dynamometer
age, height, weight, and dominant lower extremity of the was exported to a separate data-acquisition unit (MP100;
participants. The dominant lower extremity was defined as
BIOPAC Systems, Inc, Goleta, CA) for real-time data
the limb with which the participant would kick a ball.21
acquisition. The average torque value calculated over the 3
Activity level at the time of the study was not documented,
repetitions was normalized to the participant’s body mass
but participants were instructed to refrain from any training
or physical activity for 24 hours before reporting for testing. (kg) and used to quantify quadriceps strength (Nm/kg).
During the performance of the MVICs, we also assessed
quadriceps activation, which is a measure used to quantify
Testing Procedures AMI. Using the burst-superimposition technique, we
We quantified the quadriceps strength and activation of delivered a supramaximal electrical stimulus (GRASS
all participants under 4 randomized conditions: normal S88 and SIU8T; Astro-Med, Inc, West Warwick, RI) with
knee, effused knee, painful knee, and effused and painful a train of 100 pulses per second, pulse duration of 600
knee. For the normal knee condition, we quantified strength milliseconds, train duration of 100 milliseconds, and
and activation without manipulating the knee joint, whereas maximal voltage of 130 V23,24 to the participants while

Journal of Athletic Training 187


Table 1. Effect Sizes (95% Confidence Intervals) for Quadriceps Strength and Activation Between the Normal Knee Condition and Each
Experimental Knee Condition
Knee Condition
Measure Effused Painful Effused and Painful
Torque 0.49 (0.28, 1.22) 0.46 (0.30, 1.20) 0.71 (0.05, 1.47)
Central activation ratio 0.64 (0.29, 1.21) 0.48 (0.14, 1.38) 0.73 (0.06, 1.47)
Pain rating 1.32 (2.09, 0.47) 3.05 (4.03, 1.89) 2.92 (3.89, 1.79)

they performed the previously described MVICs for knee effusion always preceded the injection for pain because the
extension. The central activation ratio (CAR) was calcu- pain resolved more quickly than the effusion.
lated for each repetition using the following equation:
  Pain Ratings
MVIC torque
CAR ¼ ; After each experimental condition, participants were
superimposed burst torque
instructed to complete a short-form McGill Pain Question-
where MVIC torque was the peak torque recorded before naire. The visual analog scale (10-cm line) included on this
the delivery of the electrical stimulus, and superimposed- form was used to estimate the overall intensity of pain
burst torque was the maximal torque value elicited via the participants experienced in their knees due to the injection
electrical stimulus. A CAR equal to 1.0 represents maximal or injections. The pain rating was taken approximately 1
voluntary activation, but a CAR equal to 0.95 represents minute after the injection, which was before the completion
complete or normal activation.25 The average CAR over the of the quadriceps strength and activation assessment.
3 repetitions was used to quantify quadriceps AMI.
Statistical Analysis
Experimental Knee-Effusion Procedures
We used 2 separate 1 3 4 repeated-measures analyses of
To induce the experimental knee-joint effusion, the area variance to compare quadriceps strength and activation
superolateral to the patella of the dominant lower extremity across the 4 conditions. Similarly, we used a repeated-
was cleaned with alcohol and povidone-iodine. All measures analysis of variance to compare the pain ratings
participants’ lower extremities were placed in extension across the 4 conditions. Bonferroni multiple-comparisons
while they lay supine in the dynamometer chair, which was procedures were employed post hoc. The a level was set at
fully reclined. We used a sterile syringe with a 25-gauge, equal to or less than .05 for all tests. Effect sizes (95%
1.5-inch needle to inject 3 mL of 1% lidocaine subcutane- confidence intervals [CIs]) were quantified for each
ously to anesthetize the skin. After the lidocaine was condition between the normal knee condition and the
released from the syringe, the needle was guided into the experimental knee condition (effused, painful, or effused
knee joint capsule, a 60-mL syringe was attached, and 60 and painful) using the Cohen d ([group mean normal 
mL of sterile saline was injected into the subcapsular group mean at experimental condition]/the pooled standard
synovial cavity.7,26 After the injection, we performed a deviation). To establish between-sessions reliability of our
sweep test to confirm the saline was in the knee joint dependent measurements, intraclass correlation coefficients
capsule. All injections were performed by the same (ICC) (2,1) 6 standard error of the mean were calculated
investigator (B.D.), a certified physician assistant. using the torque and CAR data recorded at each session
before the delivery of any injections.
Experimental Knee-Pain Procedures
To induce experimental knee pain, participants were RESULTS
positioned as described for the knee-effusion injection. An Effect sizes and their 95% CIs for quadriceps strength and
area inferior and medial to the patella was cleaned with activation are presented in Table 1. The between-sessions
alcohol and povidone-iodine. We used a sterile syringe with reliability for our measurements was high (MVIC ¼ 0.924 6
a 25-gauge, 1.5-inch needle to inject 0.3 mL of 5% 0.192; CAR ¼ 0.91 6 0.027), suggesting that our comparison
hypertonic saline into the medial infrapatellar fat pad. After across days can be considered with confidence.
being injected with the hypertonic saline, participants were
instructed verbally to rate their pain on a scale of 0 (no
Strength and Activation
pain) to 10 (worst pain). Participants who rated their pain
as 5 or more did not receive a second injection of We noted differences between conditions for both
hypertonic saline. Participants who rated their pain as less quadriceps strength (F3,39 ¼ 7.56, P , .001) and activation
than 5 on the scale were injected with another 0.3-mL bolus (F3,39 ¼ 6.21, P ¼ .001; Figures 1 and 2). The quadriceps
of 5% hypertonic saline. Nine of 14 volunteers required the strength recorded during the normal knee condition (2.49 6
second injection of hypertonic saline. The described 0.70 Nm/kg) differed from the other 3 knee conditions
procedures were similar to those used in previous (effused: 2.16 6 0.69 Nm/kg, P ¼ .04; painful: 2.15 6
investigations.19,27,28 Participants were not informed in 0.71, P ¼ .01; effused and painful: 1.96 6 0.77, P ¼ .009)
advance of the criterion used to determine the need for and was greatest under the normal knee condition.
administration of a second injection. Similarly, the CAR was highest under the normal knee
For the effused and painful condition, we followed the condition (0.88 6 0.09) and differed from the 3
procedures described for both conditions. The injection for experimental knee conditions (effused: 0.81 6 0.11, P ¼

188 Volume 48  Number 2  April 2013


a
Figure 1. Quadriceps peak torque for each knee condition. Indicates difference from the other 3 knee conditions (P , .05).

.01; painful: 0.83 6 0.11, P ¼ .03; effused and painful: 0.79 quadriceps muscle strength and activation. Both the effused
6 0.11, P ¼ .02). We did not note differences among the 3 knee and painful knee groups demonstrated quadriceps
experimental knee conditions for either quadriceps strength muscle dysfunction, but the amounts of quadriceps
or activation (P . .05). activation and strength deficits were not magnified when
these 2 stimuli were present simultaneously.
Pain Reports are conflicting about whether the presence of
pain results in quadriceps dysfunction. Shakespeare29 noted
We found differences between conditions for intensity of
that quadriceps inhibition can occur in the absence of
pain (F3,39 ¼ 35.16, P , .001; Table 2). The intensity of
perceived pain in patients after meniscectomy, whereas
pain was lower under the normal knee condition than under
Arvidsson et al30 found that reducing pain via epidural
the 3 experimental knee conditions (effused: P ¼ .02;
injections of lidocaine can increase quadriceps electromyo-
painful: P , .001; effused and painful: P , .001). The
graphic activity in patients after ACL reconstruction.
intensity of pain was greater during the painful condition
than the effused condition (P ¼ .005) but not the effused Similarly, pain has been shown to be both related31 and
and painful condition (P ¼ .98). In addition, the intensity of unrelated32 to quadriceps strength and activation in patients
pain was lower during the effused condition than the undergoing total knee arthroplasty. Our study was different
effused and painful condition (P ¼ .001). from those earlier reports because we examined a cause-
and-effect relationship between pain and quadriceps
activation and strength. We showed that moderate amounts
DISCUSSION of pain created a small magnitude of quadriceps AMI (5.7%
We used experimental knee pain and effusion models to change from the normal knee condition) and also resulted in
examine the effects that pain and effusion may have on a decline in quadriceps strength (13.7% change from the

Figure 2. Quadriceps central activation ratio (CAR) for each knee conditions. a Indicates difference from the other 3 knee conditions (P ,
.05).

Journal of Athletic Training 189


Table 2. Overall Pain Rating for Each Conditiona may have contributed to this outcome.34 Thus, the presence
Knee Condition Mean 6 SD of pain in both the effused and painful condition and the
Normal 0.00 6 0.00
effused condition may help explain why quadriceps
Effused 2.17 6 2.33b strength and activation did not differ between these groups.
Painful 5.22 6 2.42c Although not a main purpose of our study, knee joint
Effused and painful 5.46 6 2.64c effusion led to declines in quadriceps strength and
a
0 ¼ no pain, 10 ¼ worst pain.
activation. This result was not novel; many investiga-
b
Indicates different from the normal knee condition only. tors10–12,33 have noted that effusion leads to AMI. However,
c
Indicates different from the normal and effused knee conditions. AMI in these previous investigations was quantified using
the H reflex. We quantified AMI in our study using the
CAR, which was recorded while volunteers performed
normal knee condition). Henriksen et al15 noted decrements
muscle contraction, rather than the H reflex, which is
in isometric and isokinetic knee-extension strength ranging measured under static conditions. Thus, the finding that
from 5% to 15% after the induction of experimental knee effusion leads to quadriceps inhibition during a quadriceps
pain, which was consistent with our data. Considering that contraction is worth highlighting.
pain accompanies numerous knee joint injuries and Our participants presented with an average CAR of 0.89,
conditions, the prevalence of AMI and quadriceps strength which is lower than the 0.95 considered to be complete
deficits with joint trauma is likely high. Our finding that the activation for healthy adults.25 Therefore, before experi-
magnitude of inhibition resulting from pain was not large mentally altering their knees, some of our participants
agrees with data suggesting that pain contributes to a small would be considered to have incomplete quadriceps
but substantial portion of the AMI present after total knee activation. The reason behind this is unclear, but it could
arthroplasty.31 Notably, the relationship between pain and be due to not truly completing a maximal quadriceps
AMI may be mediated by the severity of the pain isometric contraction during testing. We encouraged
experienced, but that connection requires future study. maximal contraction by providing both visual and oral
Knee-extension strength has been positively correlated with feedback during testing and thus had to assume participants
pain intensity, so we would hypothesize a similar relation were completing the MVICs to the best of their abilities.
between AMI and pain.15 Given that we used a crossover design and all participants
Contrary to our hypothesis, the interaction of pain and completed all conditions, we suggest our results comparing
effusion did not result in different magnitudes of AMI the conditions are not hindered. Although not reported as
(change from the normal knee condition was 5.7% in the part of this study, we collected data for each participant in a
painful condition, 7.6% in the effused condition, and 10% normal knee condition each day before inducing any
in the effused and painful condition) or quadriceps strength experimental condition and found that the baselines were
declines (change from the normal knee condition was not different from each other (P ¼ .96 for quadriceps CAR).
13.7% in the painful condition, 13.6% in the effused Thus, whereas the magnitude of CAR of the normal knee
condition, and 21.8% in the effused and painful condition), was lower than expected for healthy adults, we are
suggesting that the 2 stimuli did not have an additive effect. confident that the change resulting from the effusion or
Given that severity of injury can influence the degree of pain or both models was accurate.
AMI,13 we expected that a more noxious stimuli provided The computed effect sizes listed in Table 1 suggest that the
to the knee would increase quadriceps AMI and decrease injections resulting in pain or effusion or both led to small to
quadriceps strength. Although the pain and effusion in our moderate changes in quadriceps torque and CAR when
study were both experimentally induced and may account compared with the normal knee condition. These findings led
for the lack of difference, the degree of pain (5/10 on a us to conclude that pain or effusion or both resulted in
visual analog scale) and the size of the effusion (60-mL statistical differences and potentially clinically meaningful
joint effusion) were moderate. Thus, we suggest our differences in our dependent measures. However, the wide
findings have meaning for clinical populations with knee 95% CIs suggest that we cannot rule out a large increase or
injury. The lack of difference between the effused and decrease in torque or CAR due to the injections. This wide
painful condition and each of the other 2 conditions also variation likely can be attributed to our small sample size. In
could be attributed to a lack of statistical power. However, future investigations, using a larger sample may be necessary
the effects were small when we examined effect sizes for to definitively conclude the effects of pain or effusion or both
comparisons between the effused and painful condition and on quadriceps torque and the CAR.
the painful condition (CAR ¼ 0.16, MVIC ¼ 0.27) and the A limitation of our study was that pain was only
effused and painful condition and the effused condition quantified directly after the experimental conditions were
(CAR ¼ 0.28, MVIC ¼ 0.27). Therefore, based on our induced. Pain levels likely decreased from when the pain
results, we suggest that pain and effusion have no additive rating was quantified to the time when the last MVIC took
effect on quadriceps strength and activation. Unexpectedly, place. Researchers19 using methods to induce pain similar
our results indicated that our participants experienced some to those we described found knee pain peaked (5.8/11 on a
pain during the effused condition, but this level of pain was visual analog scale) approximately 3 minutes after injection
less than that during the painful and the effused and painful of hypertonic saline and declined (2/11 on a visual analog
conditions. Researchers33 using the effusion model have scale) approximately 10 minutes postinjection. Given that
indicated that the effusion is painless, and we were testing took about 10 minutes to complete from the time of
anticipating similar outcomes. Group III and IV afferents the injection to the last MVIC, the pain rating likely had
(nocioceptors) have been found to respond to local declined by the time we recorded the last MVIC or CAR,
mechanical stimulation of the joint, and their stimulation which may have influenced our results. However, our

190 Volume 48  Number 2  April 2013


findings still illustrate that the pain produced by the model 15. Henriksen M, Rosager S, Aaboe J, Graven-Nielsen T, Bliddal H.
employed resulted in quadriceps weakness and activation Experimental knee pain reduces muscle strength. J Pain. 2011;12(4):
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19. Bennell K, Hodges P, Mellor R, Bexander C, Souvlis T. The nature
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and effusion did not appear to increase the magnitude of infrapatellar fat pad. J Orthop Res. 2004;22(1):116–121.
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that clinicians who want to reduce AMI and improve neural mechanisms and treatment perspectives. Semin Arthritis
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Address correspondence to Riann M. Palmieri-Smith, PhD, ATC, School of Kinesiology, University of Michigan, 4745G CCRB, 401
Washtenaw Avenue, Ann Arbor, MI 48109-2214. Address e-mail to [email protected].

Journal of Athletic Training 191

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