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INTERACTION EFFECTS OF THE STARTLE RESPONSE AND
HORMONAL CHANGES ON KNEE STIFFNESS
by
Athena DeAngelis
A thesis submitted to the Faculty of the University of Delaware in partial fulfillment of the requirements for the degree of Master of Science in Exercise Science
Approved: __________________________________________________ Charles Buz Swanik, Ph.D. Professor in charge of thesis on behalf of Advisory Committee Approved: __________________________________________________ William B. Farquhar, Ph.D. Chair of the Department of Kinesiology and Applied Physiology Approved: __________________________________________________ Kathleen S. Matt, Ph.D. Dean of the College of Health Sciences Approved: __________________________________________________ Charles G. Riordan, Ph.D. Vice Provost for Graduate and Professional Education
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ACKNOWLEDGEMENTS
I would like to say a special thank-you to several people who have been a great
support system and have provided me with everything I needed to finish this project.
First and foremost I want to thank all my lab-mates and friends that have helped as
volunteer subjects and assisting in all aspects of performing testing. These special
people include Kathy Liu, Craig Oates, Jen Halterman, Chris Clyde, Peter Braun, and
Dan Tocci. I really want to acknowledge Alan Needle for providing all his expertise,
advice, time and mentorship over the past two years. Finally, I could not do this
without awesome friendships and support that I will treasure forever with Christina
Shields, Rob Hulbert and Matt Astolfi.
The University of Delaware provided me the opportunity to work along side
some of the best researchers including my committee members: Dr. Kaminski, Dr.
Knight and Dr. Royer. I would also like to thank my advisor and chair, Dr. Swanik,
for providing me with guidance throughout this entire thesis process and giving me his
expertise in joint stiffness and neurocognitive function to assist me in completing this
degree.
Finally, I would be nothing without the love and support my family
continuously gives me everyday of my life. Even though they are not experts with my
project, they were always a phone-call away to talk to and always support everything I
was doing in order to earn my degree. Without them, I would not be the person I am
today.
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TABLE OF CONTENTS LIST OF TABLES ........................................................................................................ vi LIST OF FIGURES ...................................................................................................... vii ABSTRACT ................................................................................................................ viii Chapter
Knee injuries are commonly experienced among the physically active
population, with anterior cruciate ligament (ACL) sprains affecting over 250,000
people per year. (Adachi et al., 2008; J. T. Blackburn et al., 2009; Griffin et al., 2000)
Non-contact ACL (NC-ACL) injuries account for over 70% of all ruptures and likely
result from sudden errors in coordination during abrupt deceleration maneuvers like
landing, or cutting.(Fleming et al., 2003; Kirkendall & Garrett, 2000; Olsen et al.,
2004) Females suffer this injury 2-8 times more often than males, and most
researchers believe intrinsic factors such as knee valgus collapse, anterior tibial sheer
and knee laxity are responsible for the higher incidence. However, these prior
observations may only reflect underlying disruptions in neuromuscular control that
ultimately lead to pathological joint kinematics. (Boden et al., 2000; C.Swanik et al.,
2004; C.Swanik et al., 1999) Moreover, theories for the potential neurophysiological
source of these coordination errors have been limited, especially in males. It is
plausible that two common neurological influences, the startle response and menstrual
cycle, interact to heighten ones risk for NC-ACL injury. (Adachi et al., 2008)
Precise muscle activation strategies can help stress-shield ligamentous
structures from excessive loading by regulating joint stiffness during sport-specific
maneuvers.(Lephart et al., 1992) Both quadriceps and hamstring musculature provide
this capacity of dynamic stabilization at the knee, however, sudden unanticipated
events may interrupt the feed-forward and feedback motor control necessary for
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optimal temporal/spatial muscle recruitment levels. (Rozzi et al., 1999; C.Swanik et
al., 2004; C.Swanik et al., 1999) Recently, greater attention has been focused on
attributes of the central nervous system (CNS) that may be associated with
unintentional musculoskeletal injuries and the promise of reducing injury prone
behaviors.(C.Swanik et al., 2007; Baumeister et al., 2008, Ribot-Ciscar et al., 2009)
It is well documented that unanticipated events can provoke a universal startle
response within the CNS, which results in a brief, but widespread change in
neuromuscular activity. (Davis, 1984; Koch, 1999) When an unexpected startle
response is provoked, neuromuscular changes to preparatory (feed-forward) and
reactive (feedback) muscle contractions in the extremities can be observed, potentially
altering the stiffness regulation necessary for energy absorption and dynamic joint
stabilization. (LaCroix, 1981; Freeman, 1966; Davis, 1984; Koch, 1999) The most
common startle research model uses an unexpected acoustic stimulus, which during
ordinary physical activities and real-world settings may be synonymous with any
sudden extraneous events, noises, or interpersonal communications. (Leumann et al.,
2001) While much of the previous research has focused on NC-ACL injury
mechanisms in women, the startle response may help explain why males too suffer a
loss of coordination and high incidence of this unintentional musculoskeletal injury.
Some research suggests that females may have different reactions to
unanticipated startle events than males. (Hausmann et al., 2000; McCormick &
Teillon, 2001) In response to an auditory stimulus, females have shown faster
responses and higher lower-limb muscle activation. (Kofler et al., 2001) The
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differences in female startle response have been suggested to result from hormonal
changes. (Braff et al., 2001; Kofler et al., 2001)
The female menstrual cycle and hormone concentration level change is one
remarkable difference between males and females and may be linked to variations in
female neuromuscular control and dynamic stability. (Adachi et al., 2008) Previous
studies tend to focus on ACL characteristics such as laxity and collagen formation;
however, Zazuluk (2006) reported that these results are inconclusive. There is limited
research linking the idea of hormonal alterations to neuromuscular control and joint
stability. Although some debate exists, ACL injuries appear more prevalent during the
ovulation stage of the menstrual cycle, when estrogen is at its peak. (Deie et al., 2002;
Eiling et al., 2007; Park et al., 2009) This hormonal change, along with dysmenorrhea
seen around day 14 of the cycle, may contribute to alterations in sensorimotor
characteristics and athletic performance leading to increased risk of injury. (Adachi et
al., 2008; Eiling et al., 2007) Estrogen levels also cause increased synthesis of the
neurotransmitter dopamine, creating a more responsive effect to the acoustic
startle.(Braff et al., 2001; Jovanovic, 2004) Since estrogen peaks during ovulation, this
would suggest that with an increase of dopamine the reflex would be most affected
during this phase of the cycle. (Jovanovic, 2004) Therefore, changes in hormonal
levels during the menstrual cycle may contribute to differences in both the startle
response and joint stiffness regulations, but these interactions have not been observed.
The purpose of this study was to determine if gender and menstrual cycle
differences occur with an acoustic startle, and whether these alterations influence the
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quadriceps and hamstring muscle activation strategies responsible for knee joint
stiffness regulation. By combining measures of muscle stiffness and acoustic startle
trials, more information may be found on this potential source for heightened risk of
non-contact ACL injuries. In this study we tested the hypothesis that (1) there is
altered muscle activation and stiffness occurring when the acoustic startle trials occur
compared to the control conditions, (2) males react to the acoustic startle with quicker
muscle activation leading to an increase in stiffness compared to females and (3) the
female menstrual cycle interacts with the startle response leading to a change in
muscle activation and joint stiffness.
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Chapter 2
METHODS
2.1 Experimental Design
This study utilized a post-test only design with repeated measures. The
independent variables are gender (male and female), menstrual cycle phase (Follicular
(FF), and Ovulation (FO)) and condition (no startle and acoustic startle). The
dependent variables are measurements of short-range and total knee stiffness and
muscle activity (timing and amplitude).
2.2 Participants Eighteen male and eighteen female (tested twice) healthy volunteer
participants within the 18-25 years age range were recruited from the University of
Delaware population. The number of participants is determined through an a priori
power analysis using G*Power v3.1.2 (Heinrich-Heine-Universitat, Dusseldorf) with
parameters set at α = .05, 1- β = 0.80. Prior to testing, participants were provided
university-approved informed consent (UD IRB 231022-1) as well as a Physical
Activity Readiness Questionnaire (PAR-Q) and Demographic and Health History to
determine participation eligibility. If the participant answered, “Yes” to questions
pertaining to pains in the heart or chest, faintness or dizziness, bone or joint problems,
or low back problems; he/she were not included in the study. Participants were tested
on their dominant leg. This is defined by which leg the subject would use to single-leg
jump for distance. (Croce 2004, Russell 2007) Exclusion criteria for all participants
includes: (1) any fractures to the test leg within the previous year, (2) history of injury
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to the leg within the previous 6 months (3) other knee injuries requiring surgery, (4)
any current bone, muscular, or joint injuries to the hip, knee, and ankle, (5) any
cardiovascular, metabolic or neurological that limits moderate physical activity, (6)
any hearing impairment or complications, and (7) any females taking oral
contraceptive medications or having irregular menstrual cycles.
2.3 Instrumentation 2.3.1 Stiffness and Proprioception Device (SPAD)
Stiffness testing was performed using a custom-built stiffness and
proprioception assessment device (SPAD). The SPAD is a device capable of
providing a perturbation to the knee at a controlled acceleration, deceleration , velocity
and range of motion. The SPAD is a brushless Danaher/Kollmorgen servomotor (B-
404-B-B4) that is fitted into a gearbox (UT018-050, 50:1) and connected to an
amplifier/controller (Copley Xenus driver XSL-12-36-R). The mated servomotor and
gearbox are mounted in a cast aluminum pedestal that is offset from the subject’s
chair. An adaptor arm and torque reaction sensor (Model # T5400, Futek Advanced
Sensor Technology, Irvine, CA) with a 565 N capacity and 1.43 X 105 ft-lb/rad
torsional stiffness is coupled to the gearbox. The signal conditioner digitally displays
torque values and also sends an analog torque signal through an A-D board (NI DAQ
6009, National Instruments, Austin, TX) that can be recorded and displayed in
LabVIEW software. For safety purposes, internal motor settings cannot exceed preset
speeds and there are three emergency stop switches that can disable the motor during
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testing. The SPAD device is operated using a personal computer with a customized
LabVIEW virtual instrument and motor control software program.
2.3.2 Electromyography (EMG)
Surface electromyography (EMG) were collected from the vastus medialis,
vastus lateralis, medial hamstrings, and lateral hamstrings to determine stiffness
regulation strategies by analyzing the amplitude and timing of the muscular
contractions. There was also one electrooculography (EOG) self-adhesive Ag/AgCl
snap dual electrode (Noraxon USA Inc, Scottsdale, AZ) placed on obicularis oculi to
record EOG activity of the eye blinking and confirm a startle response. Self-adhesive
Ag/AgCl bipolar surface electrodes (Phillips Medical Systems, Andover, MA) were
used to collect EMG data of the leg musculature, and an EMG unit (Bortec AMT-8,
Bortec Biomedical, Calgary, Alberta, Canada) was used to record EMG with a real-
time visual display on the monitor. Electrode placement was identified by bony
landmarks and through palpation of the mid-belly of the contractile component of the
muscle during an isometric contraction. The reference electrode was placed on the
patella. Except for the eye muscle, each electrode is 10mm in diameter and was
placed 25mm apart. Electrode placement site was shaven, abraded, and cleansed with
an alcohol swab (70% ethanol solution) to decrease the impedance from the skin. The
EMG signal was converted from analog to digital data (NI DAQ 6009, National
Instruments, Austin, TX), and then passed to a computer where the raw EMG data was
sampled at 2,400 Hz and further analyzed with LABVIEW software (National
Instruments, Austin, TX). The EMG signal was bandpass filtered at 20-400Hz,
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rectified, and low-pass filtered at 5Hz to create a linear envelope. EMG is normalized
to maximum voluntary isometric contractions (MVICs) for the muscles of the
quadriceps and hamstrings. All data collected with EMG equipment is used to
determine the timing, sequence, amplitude (area & peak), and pattern of the
quadriceps/hamstrings muscle groups during preparatory and reactive phases of the
stiffness testing.
2.4 Procedures
Participants were asked to report to the Human Performance Lab for a 90-
minute testing procedure. Females were asked to participate twice in the study: once
during the follicular phase and once during ovulation phase of the menstrual cycle.
After providing consent, completing all questionnaires, and satisfying the inclusion
criteria, participants then rode a stationary bike for a 5-minute warm-up followed by 5
minutes of stretching of their quadriceps and hamstrings as instructed with a handout
and verbal direction.
The participant was positioned on the SPAD with the dominant knee flexed to
30 degrees and the trunk positioned at 90 degrees of flexion. The axis of rotation of
the adapter arm attached to the servomotor was in line with the lateral knee joint line.
In order to ensure that all torque responses result from movement at the knee and not
the lower leg, a vacuum splint was secured to the lower leg below the knee to maintain
the ankle in a neutral position. A thigh pad was also used for stability so that
movement occurred only at the knee joint. All electrodes for EMG activity recordings
were attached to the same side determined as the dominant leg. Three maximum
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voluntary isometric contractions (MVIC) were collected for the quadriceps and
hamstrings to determine an overall average and 30% of their maximum contraction.
The parameters of the perturbations for each testing condition remained the
same for each perturbation with a quick acceleration of 1000 deg/sec2 to a velocity of
100o/sec and a flexion arc of 40o going from knee extension to flexion. The various
testing conditions of reactive stiffening included both control trials and acoustic startle
trials. The five perturbation techniques were passive-nonreactive, active-nonreactive,
passive reactive, active reactive and active deactivate. (Figure 1) For the acoustic
startle condition, a high-pitched 100 dB tone, lasting 50ms at a frequency of 1000 Hz
sounded 100ms before perturbation. (Braff et al., 2001) Throughout all conditions, the
knee perturbation was randomly applied within a 10-second time span. Also, the
subjects were wearing headphones for all conditions to mute potential noisy
distractions. Resistance to the perturbation is detected by the torque sensor and
recorded by a computer. Joint stiffness is calculated as the Δ force (Nm) / Δ
displacement (degrees) / body mass (kg). There were six trials of each, and during the
passive reactive trials the acoustic startle was applied three times. We calculated
electromechanical delay (EMD) as the difference of when torque and EMG went
above 5 percent of peak.
2.5 Data/Statistical Analysis
A custom-written software program using LabVIEW was used to analyze
position and torque data, calculate stiffness and analyze all EMG signals. Stiffness
10
values were calculated from the position data at 3° and 40° of the flexion
perturbations. The EMG was averaged over the six trials for each of the five
perturbations. EMG was analyzed from a window of 150ms prior to perturbation and
600ms after the start of perturbation. The normalized stiffness values were obtained
by dividing each volunteer’s stiffness values by their body mass(kg). The significance
for all data is set a priori at p<.05. A repeated-measures ANOVA with one between-
subject factor (group, 3 levels), and one within-subjects factor (condition, 5 levels)
was used primarily to determine the differences in gender (cycle) and knee stiffness
and when the startle is applied. To determine mean statistical differences, pairwise
comparisons were used to assess changes in stiffness while the startle was applied
between males and females, as well as changes in muscle activation strategies post
hoc. This was also used to compare females during the two periods of their menstrual
cycle.
Figure 1: Five Perturbation Techniques and Instructions
Condition Instructions Passive Stiffness (PS) “Remain completely relaxed throughout the entire perturbation”
Active Stiffness (AS) “Push out to [30% MVIC] prior to the move. When you feel the perturbation, hold that amount of contraction without pushing more or less.”
Reactive Stiffness (RS) “Push out to [30% MVIC] prior to the move. When you feel the perturbation, resist it as hard and as fast as possible as if you are stopping your knee from bending.
Passive Reactive Stiffness (PRS)
“Remain completely relaxed prior to move. When you feel the perturbation, resist is as hard and as fast as possible as if you are stopping your knee from bending”
Deactivating Stiffness (DS) “Push out to [30% MVIC] prior to the move. When you feel the perturbation, turn off all your muscles and relax as quickly as possible.”
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Chapter 3
RESULTS
3.1 Demographics and Maximum Voluntary Isometric Contractions
Demographic data for age, height, mass, and peak MVIC torque are displayed
in Table 1. Females and males ages ranged from 18-25 and were not significantly
different (p=.563). Males displayed significantly greater height, mass, and leg length
compared to female participants (p<.001). Peak torques during MVIC for quadriceps
and hamstrings MVICs also were significantly greater in male participants (p<.05).
3.2 Startle Effects on Stiffness and EMG Variables 3.2.1 Stiffness & Startle Results for normalized short-range (0 to 4°) and total (0 to 40°) stiffness from
PR trials are displayed in Tables 2 & 3, respectively. The startle was observed to
significantly affect both short-range (p=0.037) and total (p<0.001) stiffness. For short-
range stiffness, both the first (FST) startle trial (p=0.003) and the average of the startle
trials (AST) (p=0.005) displayed significantly greater stiffness than control (CON)
trials. However, for total stiffness, FST trials demonstrated significantly less total
stiffness than both CON (p=0.004) and AST (p<0.001) trials.
3.2.2 EMG & Startle EMG variables used for analysis during PR trials include peak EMG (table 5),
TTP for leg musculature (table 6), TTP for obicularis oculi (table 7), onset values
(table 8), areas for EMG activation 250 prior-to (table 9), 250ms following (table 10)
and 250-500ms following (table 11) the perturbation.
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A significant muscle by condition interaction effect was observed for all
variables (p<.05), with the exception of EMG area 250-500ms following the
perturbation, which was approaching significance (p=.055). The VM displayed
significantly lower peak EMG during FST trials compared to CON and AST trials
(p=0.040 and p=0.017). VM and VL revealed significantly shorter TTP for FST and
AST trials (p<.05) than CON and MH displayed significantly shorter TTP in FST in
relation to CON (p=.046). The VM and MH demonstrated significantly shorter onset
for both FST and AST than CON (p<.05). VM and VL showed a significant increase
in pre-perturbation area with FST and AST compared to CON (p<.05) and LH
presented significant increase in FST trials than CON (p=.037). Post-perturbation area
had a significant decrease for VL in AST trials compared to CON (p<.001).
The muscles also differed from each other within each startle condition.
During CON, FST and AST the quadriceps had significantly increased peak EMG
values than hamstrings (p<.001). CON trials showed a significant delay TTP for the
quadriceps compared to the hamstrings (p<.05). FST and AST had significant longer
TTP in quadriceps than hamstrings (p<.05) with AST also showing slower TTP in
lateral hamstrings than medial hamstrings (p=.048). CON and FST displayed longer
onset of VM compared to VL, MH and LH (p<.001) as well as MH delays to LH
(p<.05). CON also demonstrated decreased onset in VL than MH (p=.026) and AST
had longer onset in VM compared to VL and LH (p=.036 and p=.005). CON showed
increase in VM pre-perturbation activity than VL (p=.041) while FST and AST
displayed decrease in MH activity than VM (p<.05). All trials had an increase in post-
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perturbation VM activity than the hamstrings (p<.05) with FST and AST also showing
increase in VL than MH (p<.05).
3.3 Startle Effects on Group Differences No significant group differences were observed for stiffness values. No
significant group by trial interaction effects was observed for either stiffness value.
No significant group differences were observed for any EMG variables. A significant
group by muscle interaction was only found for areas 250ms and 250-500ms
following the perturbation (p<.05). For the post-perturbation area, the FF and FO
groups has significantly higher EMG activity in VM compared to LH (p=.008 and
p=.027). Additionally, the FO group showed significantly less activity in MH than
both VM and VL (p<.001 and p=.011). In post-post perturbation area, both female
groups had significantly higher VM and VL activity compared to MH and LH
(p<.001) while ML demonstrated significant less activity in MH than both VM and
VL (p=.003 and p=.004). Furthermore, the VM had significantly decreased activity in
ML than FO (p=.024). No significant group by startle interaction effect for any EMG
variable was observed.
Results for electromechanical delay (EMD) are presented in Table 4. No
significant differences were observed between groups; however, differences were
detected between muscles, p<.001. Post-hoc analysis indicated MH had a significant
higher EMD than VM, VL and LH (p<.001).
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Chapter 4
DISCUSSION
The purpose of the present study was to determine how stiffness of the knee
joint is affected by an acoustic startle, as well as hormonal differences associated with
gender and the menstrual cycle. Neuromuscular, neurocognitive, and mechanical
differences are thought to play a significant role in the high incidence (70%) of non-
contact joint injury mechanisms (Boden et al., 2000; Fleming et al., 2003), and even
greater factor among females who suffer a disproportionate number (2-8x greater) of
ACL tears compared to males. (Arendt & Dick, 1995; Eiling et al., 2007; Griffin et al.,
2000; C. Swanik et al., 2007) However, few studies have investigated the influence of
extrinsic factors, such as startling events, on the neuromuscular control and joint
stiffness regulation needed for knee stability. The primary finding of this study was
that joint stiffness and muscle activation patterns were significantly affected by an
acoustic startle in both males and females, while differences between groups were not
observed. These findings suggest that startling events may negatively influence the
normal stiffness regulation strategies needed for functional joint stability regardless of
gender, and attenuation of this startle response should be considered in future knee
injury mechanism and prevention studies.
4.1 Stiffness Regulation and the Acoustic Startle
A measure of the resistance provided by a joint to external loading is crucial
for understanding functional stability and injurious mechanisms, as one’s failure to
optimally regulate joint stiffness can lead to excessive loading in capsuloligamentous
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structures and potential damage. Furthermore, since joint stiffness is largely dependent
on muscle recruitment, including measures of muscle activity can allow greater
understanding of where failures in stiffness regulation may be occurring beyond that
provided by passive connective tissue structures. Muscular contraction can increase
joint stiffness 10-fold, however an optimal level of stiffness is task dependent, and
based on both performance and stability needs (Swanik 1997; Nichols & Houk 1976;
Rack & Westbury, 1974). In order to maintain proper biomechanical alignment the
joint must undergo a controlled, columnar buckling, with the majority of energy being
absorbed and dissipated in the eccentric lengthening of surrounding musculature rather
than capsuloligamentous tissue (Hewett & Torg, 2009). These highly coordinated
muscle activation strategies include pre-programmed preparatory contractions, pre-
planned reflexes and involuntary reactions developed from within the central nervous
system (CNS) and therefore susceptible to strong stimuli and unanticipated events.
The acoustic startle is one example frequently used as a research model to assess the
effects of sensory stimuli on the CNS.
Startle events have been hypothesized to alter neuromuscular control by
disturbing both preparatory and reactive neuronal circuitry at the level of the
brainstem. (Ghez & Krakauer, 1991, Koch, 1999) These planned reflexes can help
explain how people will react to an event when anticipating certain proprioceptive
circumstances during activity (Nieuwenhuijzen et al, 2000). While studies have
investigated the effect of a startle on these neuronal circuits, and involuntary muscular
responses (Yeomans 1995; Koch 1999; Moffit et al. 2012), no research has
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investigated its potential secondary effect on a measure of joint stability such as
stiffness.
Our results found an increase in short-range stiffness following the startle, but
then a decrease in total stiffness, which encompasses and larger, functional range of
motion. Limited research is available with the startle and biomechanics, but a study
by Nieuwenhuijzen et al showed decreases in leg musculature range-of-motion during
a gait analysis (2000) and Moffit et al displayed changes in neuromuscular activation
with an applied startle (2012). Short-range stiffness is typically associated with the
passive components of the joint, a reverse pivot of bound actin-myosin cross-bridges,
as well as the series and parallel elastic components of the muscle. (Sinkjaer et al.,
1988, Crago et al, 1976; Nichols & Houk 1976; Houk et al, 1967) Our startle response
was purposely initiated in a brief period of time before the external knee perturbation,
in an attempt to replicate a potential unanticipated sensory disturbance just prior to
joint loading, which may occur during physical activity. The higher short-range
stiffness likely reflects a disturbance in neuromuscular control as we found earlier
quadriceps muscle activation during these trials. Quadriceps activation is important for
maintaining knee stability because this group is among the primary antigravity
muscles (Bellew, 2002). However, when contracting earlier that anticipated during
the joint range of motion, the quadriceps may contribute to increased anterior shear
forces and a knee hyperextension moment. This combination would potentially place
the knee in a more vulnerable position for ACL injury (Rozzi et al, 1999; Griffin et al,
2000).
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In addition to altered short-range stiffness, our results also supported
decreased stiffness for the entire 40-degree perturbation. The total-stiffness is largely
dependent on the ability to regulate the reverse cross-bridge cycling of an eccentric
contraction as the knee is forced into flexion (Sinkjaer et al, 1998). Our results showed
that the startle caused an initial, early heightening of joint stiffness that then was
attenuated throughout the remainder of the perturbation; a potentially detrimental
combination for avoiding knee injury. Previous studies have also linked alterations in
muscle stiffness to knee injury. (Swanik 2007; Blackburn et al 2009; Boden et al
2000) The inability to sufficiently stiffen the knee, as one would normally accomplish
through muscle activation, could expose capsuloligamentous structures to excessive
loads that would otherwise be absorbed through controlled muscle lengthening.
When considering these muscle activation patterns, nearly all variables were
affected by the acoustic startle. While the quadriceps muscles were observed to have
greater EMG activity than the hamstring muscles throughout all trials, the startle
prolonged the onset and time-to-peak (TTP) activity of the vastus medialis muscle.
Furthermore, the startling event before the perturbation caused an early increase in
EMG activity but decreased muscle activity when compared to control trials during
and after the perturbation (Tables 10 & 11). We hypothesize that this overall
decreased EMG activity, in conjunction with our findings of decreased total joint
stiffness, may be related to an “uncontrolled buckling” observed in a jump landing
where absorption of ground reaction forces occurs with the joint in a more vulnerable
position. (Boden et al., 2000; Fleming et al., 2003; Hewett & Torg, 2009) If an
18
unanticipated event occurs just prior to joint loading, a startle reflex may be initiated.
The involuntary startle causes an early quadriceps activation and knee extension
moment, appearing to us as heightened short-range stiffness. Under real-world
conditions such as landing or cutting, this effect may cause the knee joint to move
towards a hyper-extended position, which is associated with ACL tears. Furthermore,
as the startle response subsides, less muscle activity was observed and subsequently
less total stiffness of the joint resulted. The level of total joint stiffness that resulted
from the startle event was less than under normal conditions, suggesting that the
optimal stiffness regulation strategy for dynamic stability was significantly disrupted.
The inability to maintain normal stiffness regulation throughout the total range of
motion could result in uncontrolled columnar buckling during functional activities
(Hewett & Torg, 2009).
For further analysis, we compared the average of 3 applied startles to the initial
startle. Previous research has suggested that following the initial startle, the effect of
subsequent startles would be diminished and therefore may make differences more
difficult to detect. (Blumenthal et al., 2005) Our results supported this finding as the
greatest differences in joint stiffness were observed in the initial trial, and several
EMG differences were observed as well (Tables 3, 5–8). The first startle had
significantly decreased total stiffness when compared to the control and average trials.
A decreased peak EMG was observed during initial trials as well as increased time-to-
peak and decreased onset times. This demonstrates that there is an attenuation of the
startle for both stiffness and muscle activation after the initial startle is introduced. It
19
is unclear how long the attenuation of a startle response may last, but these changes do
show promise for future research into prevention and rehabilitation approaches that
can minimize the potentially disruptive neuromuscular effects of sudden unanticipated
events.
4.2 Group Effects
No group differences were observed for any stiffness or EMG measures.
Throughout the literature, females are observed to tear their ACL more frequently than
males.(Huston & Wojtys, 1996; Rozzi et al., 1999) However, the reasons behind this
common phenomenon are inconclusive, often attributing differences to
neuromuscular, strength, stiffness and the female menstrual cycle characteristics.
Moreover, little attention has been directed toward explaining why males also suffer
NC-ACL injuries. (Wojtys et al., 1998; Blackburn et al., 2009; Griffin et al., 2000; C.
Swanik et al., 2007) The menstrual cycle tends to show the most hormonal changes
during the ovulation phase with some data showing increases in laxity and stiffness.
(Van Lunen et al., 2003; Wojtys et al., 1998) This study did not support the claim that
the menstrual cycle causes significant changes in neuromuscular control or stiffness.
Some theories also blame quadriceps dominance in females, leading to knee joint
hyperextension and improper mechanics; however, our study observed that all groups
recruited these muscles similarly. Previous studies tend to show a decrease in stiffness
in females compared to males, which leads to a decrease in joint stabilization and
increases in ACL injuries, however, many of these studies do not account for
normalized body weight between genders as our study did. (Blackburn et al., 2009;
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Granata et al., 2002) Unlike other stiffness studies comparing genders, our study did
not use dynamic tasks such as jumping rather than a controlled seated dynamic
movement in order to minimize other joint axial loads and to concentrate specifically
on the knee joint.
Males tend to have greater strength, a more balanced muscle contribution,
greater muscle mass, and higher muscle fiber recruitment than females. (Blackburn et
al., 2009; Wojtys et al., 2002) In our study, females showed a decrease in MVIC for
quadriceps and hamstrings than males, supporting that females have less over-all
quadriceps and hamstring strength. The reason for females having a higher injury rate
is often contributed to the neuromuscular control strategy and their lack of control
during dynamic tasks (Rozzi et al., 1999, Griffin et al., 2000; C. Swanik et al., 2007)
Currently there is conflicting evidence, however, supporting the claims of why males
and females both suffer from a higher incidence of non-contact ACL injury. In fact,
the mechanism explaining why males also suffer from non-contact injuries has not
been offered. This study showed similar activation strategies with no significant
difference between groups. Although, from the results, female groups did have data
that was trending towards slower TTP, lower peak EMG, and slower muscle onsets. A
larger subject pool would provide more data to see if this effect continues to lead
towards significance. A group-muscle significant difference was seen with both
female groups following the 40-degree perturbation where the VM had higher EMG
activity compared to the other three muscles measured during the first startle. This
could lead towards a quad-dominance effect following startling perturbation
21
maneuvers, and this dominance could support the incidence of higher injuries. It is
possible that our startle response main effect size was large enough to conceal
potential interaction effects between groups. However, more research, with larger
subject pools is needed to provide additional evidence on whether there could be
group and gender differences with a startle event.
4.3 Limitations
One of the largest limitations to this study was that the subject pool was small
and larger groups could potentially lead to overall group differences. In future studies,
more participants are warranted to have a better understanding of how gender groups
could have altered stiffness and muscle activation patterns. In this study we measured
body weight (kg) to normalize stiffness values, however, it may be prudent to use lean
body mass due to the variations in body types that were included in this study. Lean
body mass is a more accurate portrayal of a person’s body composition. Another
limitation was that females faced the acoustic startle in more than one sitting, which
could lead to some suspicion of a habituation effect; however, prior research shows
that there is a minimal learning effect when a startle stimulus is tested on two separate
days making this limitation unlikely. The females also self-reported the accuracy of
their menstrual cycle, which is difficult to assess how honest these reports were for the
precision of our study. In future studies, ovulation kits and hormonal level testing can
improve the accuracy of the menstrual cycle timeline, which may give a better
understanding of how the 28-day cycle can alter muscle stiffness and activation.
22
4.4 Conclusion
The results from this study indicate that startle events can significantly alter
neuromuscular control and stiffness regulation strategies at the knee joint. Regardless
of gender, this event caused alterations in preparatory and reactive muscle recruitment
strategies necessary for dynamic restraint and joint stability. Overall, the first startle
caused the greatest significant differences in the measures investigated. This suggests
a single, uniquely timed startling event could expose both males and females to a
failure of the dynamic restraint mechanism and non-contact related ACL injuries.
More-over, startle events could be used in prevention and rehabilitation exercises,
however, from this study’s results, proper care should be taken due to the significant
disruption in neuromuscular control that the startle is found to have on unanticipated
As a motor response to stimuli, the startle elicits a flexor and extensor reaction,
(Davis, 1984; Landis & Hunt, 1939) and was reported to show similar results in a
study by Nieuwenhuijzen et al (2000). These flexor and extensor co-activation
reactions were seen during the early/mid-stance of gait in the leg musculature while a
startle was applied and caused a decrease in range of motion. This study was
performed to develop a better understanding of how a startle could disrupt functional
movements. Nieuwenhuijzen et al found that the startle affected locomotion through
co-contraction and showed increases in muscle activation strategies. Unanticipated
events such as startles have shown to alter functions in previous literature. (Braff et
al., 2001; Swerdlow et al., 1993b) In studies focused on neuropsychiatric disordered
patients, the startle is showing impairment to sensorimotor and cognitive reaction due
to its effect on PPI. When the PPI is inhibited, this can cause delays in functional tasks
and muscle activation creating possible deficits in stabilization. (Braff et al., 2001)
The relationship between auditory stimulus and changes to joint stability specifically
51
at the knee is not highlighted in current literature which could add further knowledge
to the ACL injury occurrences in sport.
Summary
ACL injuries affect many athletes every year, but more females than males.
Quadriceps and hamstring stiffness contributes to muscle firing and activation
differently in males and females. Decreased stiffness values are often seen as a
contributing factor to ACL injuries, which can be preventable with better dynamic
stabilization. The female menstrual cycle has continuing estrogen hormonal fluxes
during the 28-day period, which shows alterations in neuromuscular control and joint
stability. When these processes are altered, the risk of injury increases in the female
population. The acoustic startle response can also disrupt muscular stiffness, dynamic
joint stability, and may interact with the menstrual cycle to cause variations in
neuromuscular control. Studying gender differences combined with a startle stimulus
may lead to further insight to causes of ACL injury.
52
Chapter 7
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APPENDIX A
Stiffness and Proprioception Assessment Device
Stiffness testing will be performed using a custom-built stiffness and
proprioception assessment device (SPAD) (Appendix 2). The SPAD is a brushless
Danaher/Kollmorgen servomotor (B-404-B-B4) that is fitted into a gearbox (UT018-
050, 50:1) that is connected to an amplifier/controller (Copley Xenus driver XSL-12-
36-R). The amplifier (input: 230 VAC, 3PH, output: 18 FLA, 50/60 Hz) is mounted
~4ft above the ground and connected to the motor with a 12-foot long feedback cable
(Model # CEF-RO- 006-900, Pacific Scientific, Rockford, IL) and also connected to a
personal computer through a Kvasar CAN cable. The controller receives a three-
phase, 240-volt, 30-amp enclosed I-T-E switch power supply through a power cable
(Model # CEP-A6-006-904, Pacific Scientific, Rockford, IL). The mated servomotor
and gearbox are mounted in a cast aluminum pedestal that is offset from the subject’s
chair. An adaptor arm and torque reaction sensor (Model # T5400, Futek Advanced
Sensor Technology, Irvine, CA) with a 565 N capacity and 1.43 X 105 ft-lb/rad
torsional stiffness is coupled to the gearbox. Signals from the torque reaction sensor
pass through a conditioner (Model # D502, Futek Advanced Sensor Technology,
Irvine, CA) at 60 Hz and have a 0 to 10 Vdc analog output range. The signal
conditioner digitally displays torque values and also sends an analog torque signal
through a BNC box so that is can be recorded and displayed in LabVIEW software.
For safety purposes, internal motor settings cannot exceed preset speeds and there are
three emergency stop switches that can disable the motor during testing. The operator
59
and test participant will each hold an emergency stop button. When depressed, the
motor is disabled. Also, if the adaptor arm moves within the last 5% of the
participant’s end range of motion a proximity sensor (#S4602896, Turck Inc. USA,
Minneapolis, MN) will disable the motor. When the motor is disabled, the operator
must re-start the power supply to continue tests. The LabVIEW motor control
software also has “soft limits” which will disable the motor amplifier if motion
exceeds individualized motion limits. The SPAD is also fitted mechanical stops to
limit motion through an adjustable range and brass screws in the adapter arm flange
connected to the gear box which will fail under excessive torque. The SPAD device is
operated using a personal computer with a customized LabVIEW virtual instrument
and motor control software program.
60
Figure A.1: Subject Positioning on the SPAD for testing protocols
Motor Amplifier
Torque Sensor
Motor & Gear Box
Subject Emergency Stop Switch
Proximity (stop) Sensors & Mechanical Stops
Adapter Arm
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APPENDIX B
PAR-Q Form
1. Has your doctor ever said that you have a heart condition and that you should only do physical activity recommended by a doctor?
________ NO _______ YES 2. Do you frequently feel pain in your chest when you do physical activity? ________ NO ________YES 3. Do you often feel faint or have spells of severe dizziness? ________ NO ________ YES 4. Has a doctor ever said your blood pressure was too high ________ NO ________ YES 5. Has your doctor told you that you have a bone or joint problem such as arthritis
that could be aggravated or made worse by a change in your physical activity? ________ NO ________ YES 6. Do you know of any other reason why you should not do physical activity? ________ NO _________ YES 7. Are you over the age of 65 and not accustomed to vigorous exercise? ________ NO _________ YES If you answer YES to one or more of these questions please answer the following questions: 8. Have you recently consulted your physician about increasing your physical activity
and/or participating in a fitness evaluation? ________ NO _________ YES 9. If you answered “NO” to question 8, will you agree to consult your physician prior
to increasing your physical activity and/or participating in a fitness evaluation? ________ NO _________ YES Signature of PARTICIPANT _____________________ Date ________________ Signature of Investigator __________________________ Date ________________
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APPENDIX C
Demographic and Health History Questionnaire
Participant ID: ______________ Date: ___________ Gender: M F Cycle: L F N/A Age: _______ Sport: _______ PLEASE ANSWER THE FOLLOWING CONDITIONS TO THE BEST OF YOUR ABILITY. 1. Are you currently unable to participate in lower extremity activities due to injury? NO___ YES___ (if so, explain)_______________________________ 2. Have you injured either knee within the last 6 months? NO___ YES___ (if so, explain)_______________________________ 3. Have you injured either ankle within the last 6 months? NO___ YES___ (if so, explain)_______________________________ 4. If yes to any of the above, please answer: Have you ever seen a doctor for your injury (s)? NO___ YES___ (if so, explain)_______________________________ 5. Do you have any other muscle or skeletal disorders that the researcher should be aware of? NO___ YES___ (if so, explain)_______________________________ 6. Are you presently taking any medications? (including prescribed and over the counter) NO___ YES___ (if so, explain)_______________________________ 7. Have you ever had any type of surgery that may prevent your participation in this study? NO___ YES___ (if so, explain)_______________________________ 8. Do you have any hearing deficits? NO___ YES___ (if so, explain)______________________________ 9. Do you have a history of neurological disorders that may prevent your participation in this study? NO___
63
YES___ (if so, explain)_______________________________ 10. Have you ingested any caffeine in the past 12 hours? NO___ YES___ (if so, explain)_______________________________ 11. Have you taken any over-‐the-‐counter medications in the past 12 hours? NO___ YES___ (if so, explain)_______________________________ 12. FEMALES: Have you had a regular menstrual cycle (lasting 26-‐32 days) during the past 6 months? NO____ YES____ Please indicate any medical and/or health concerns you may have which have not been addressed by the previous items on this form. If there are any questions please feel free to contact one of the investigators at the following: Athena DeAngelis, BS, ATC 541 South College Avenue, University of Delaware Newark, DE, 19716 (856)-‐816-‐7286 -‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐ Signature of participant Date -‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐ Signature of investigator Date
Stand and touch the wall for support. Bend your heel towards your back and pull your ankle and forefoot to your rear end. Hold for 30 seconds and repeat 3 times.
HAMSTRINGS:
Stand and slightly bend your knees. Bend at the waist and reach towards your toes or floor and hold for 30 seconds. Repeat 3 times.
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APPENDIX E
IRB Approval Letter
RESEARCH OFFICE 210 Hullihen Hall University of Delaware
DATE: May 6, 2011 TO: Athena DeAngelis FROM: University of Delaware IRB STUDY TITLE: [231022-1] The Effects of an Acoustic Startle and Hormonal Changes on Knee Joint Stiffness SUBMISSION TYPE: New Project ACTION: APPROVED (E. Peloso, W. Farquhar) APPROVAL DATE: May 6, 2011 EXPIRATION DATE: May 5, 2012 REVIEW TYPE: Expedited Review REVIEW CATEGORY: Expedited review category # 4 Thank you for your submission of New Project materials for this research study. The University of Delaware IRB has APPROVED your submission. This approval is based on an appropriate risk/benefit ratio and a study design wherein the risks have been minimized. All research must be conducted in accordance with this approved submission. This submission has received Expedited Review based on the applicable federal regulation. Please remember that informed consent is a process beginning with a description of the study and insurance of participant understanding followed by a signed consent form. Informed consent must continue throughout the study via a dialogue between the researcher and research participant. Federal regulations require each participant receive a copy of the signed consent document. Please note that any revision to previously approved materials must be approved by this office prior to initiation. Please use the appropriate revision forms for this procedure. All SERIOUS and UNEXPECTED adverse events must be reported to this office. Please use the appropriate adverse event forms for this procedure. All sponsor reporting requirements should also be followed. Please report all NON-COMPLIANCE issues or COMPLAINTS regarding this study to this office. Please note that all research records must be retained for a minimum of three years. Based on the risks, this project requires Continuing Review by this office on an annual basis. Please use the appropriate renewal forms for this procedure. If you have any questions, please contact Jody-Lynn Berg at (302) 831-1119 or [email protected]. Please include your study title and reference number in all correspondence with this office.