Kinematic differences during a jump cut maneuver between individuals with and without a concussion history

Accepted Manuscript Kinematic differences during a jump cut maneuver between individuals with and without a concussion history

Andrew Lapointe, Luis Nolasco, Aniela Sosnowski, Eva Andrews, Douglas N. Martini, Riann M. Palmieri-Smith, Deanna H. Gates, Steven P. Broglio PII: DOI: Reference:

S0167-8760(17)30472-5 doi: 10.1016/j.ijpsycho.2017.08.003 INTPSY 11306

To appear in:

International Journal of Psychophysiology

Received date: Revised date: Accepted date:

16 January 2017 23 June 2017 12 August 2017

Please cite this article as: Andrew Lapointe, Luis Nolasco, Aniela Sosnowski, Eva Andrews, Douglas N. Martini, Riann M. Palmieri-Smith, Deanna H. Gates, Steven P. Broglio , Kinematic differences during a jump cut maneuver between individuals with and without a concussion history, International Journal of Psychophysiology (2017), doi: 10.1016/j.ijpsycho.2017.08.003

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ACCEPTED MANUSCRIPT

Kinematic differences during a jump cut maneuver between individuals with and without a concussion history

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Aniela Sosnowski NeuroTrauma Research Laboratory University of Michigan

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Luis Nolasco, MS Rehabilitation Biomechanics Laboratory University of Michigan

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Eva Andrews NeuroTrauma Research Laboratory University of Michigan

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Douglas N. Martini PhD Department of Neurology Oregon Health and Science University

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Riann M. Palmieri-Smith PhD, ATC Neuromuscular Research Laboratory University of Michigan

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Deanna H. Gates PhD Rehabilitation Biomechanics Laboratory University of Michigan

Corresponding Author Steven P. Broglio PhD, ATC 401 Washtenaw Ave Ann Arbor, MI 48109 [email protected]

Steven P. Broglio PhD, ATC NeuroTrauma Research Laboratory University of Michigan Injury Center University of Michigan

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Andrew Lapointe MS NeuroTrauma Research Laboratory University of Michigan

ACCEPTED MANUSCRIPT Abstract

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Recent evidence suggests that athletes are at a higher risk of lower-body injuries in the months and years following a concussion. However, little is known about how people modify their movements post-concussion. This study examined kinematics during a jump cut motion in young adults with a concussion history (n=9; 4 males, 5 females; 3.1 years’ post-injury) and 10 controls (6 males, 4 females). Peak center of mass and peak knee angles during the landing phase of a jump-cut maneuver were evaluated. Participants with a concussion history demonstrated decreased knee varus (Left: Mconc=-0.5±1.0o, Mctrl=3.6±1.0 o; Right: Mconc=5.1±1.2o, Mctrl=7.8±1.12 o) and external rotation (Left: Mconc=2.5±1.6o, Mctrl=13.0±1.5 o; Right: Mconc=7.7±1.6o, Mctrl=12.8±1.5 o) regardless of whether the cut was oriented towards to the left or right. The kinematic patterns demonstrated in individuals with a concussion history may be suggestive of increased knee injury risk. This study adds to the growing body of literature linking orthopedic injury in those no longer displaying the acute signs and symptoms of concussion.

Acknowledgements

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This project was supported by the Carl & Joan Kreager Research Fund

ACCEPTED MANUSCRIPT Introduction Concussion is a diffuse brain injury with highly variable clinical outcomes both within and between individuals. As such, the injury diagnosis remains a clinical one, supported by a multifaceted assessment battery[1-3]. To date, research has indicated symptomology as the most sensitive assessment measure[4], but as symptom reports can be minimized by the injured athlete, objective measures of

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neurocognitive function and motor control are also recommended. Neurocognitive and motor control

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evaluations have been extensively used in an acute population. These tests have shown good results in

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evaluating clinical functioning for injury assessment[4-6] and management, with resolution to pre-injury levels of performance in approximately two weeks post-injury [2][7]. Despite the broad use of these

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clinical measures, emerging research using more sophisticated motor control assessments has identified

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persistent changes to motor control[8, 9] that extend beyond the clinical recovery window.

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Recent studies have explored the long-term effects of concussion on motor performance in a

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variety of tasks. Advanced non-linear analytical techniques (i.e. Approximate Entropy) implemented by Cavanaugh et al[10] identified alterations in postural control that extended beyond day four post-injury

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when all participants had returned to normal clinical levels of functioning[10]. Similarly, collegiate athletes who were 44 months post-injury, continued to demonstrate less complex balance maintenance [11].

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Implementation of a more complex motor task with an increased cognitive load (i.e. gait during a dual task) demonstrated ongoing changes in gait velocity and center of mass (COM) displacement and velocity

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at four weeks post-injury [12]. In another dual-task study, differences between concussed and control groups were more prominent during dual-task vs single-task[13] . Howell et al[14] observed that dual-task differences between concussed and controls remained significant two months post-injury with Fino et al[15]’s mixed model predicting that some of these difference may persist one-year post-injury. A metaanalysis evaluating gait changes up to seven months post-injury demonstrated decreased gait velocity and greater medial-lateral sway[16, 17]. Additionally, an investigation of previously concussed individuals 6.3 years post-injury revealed increased time in double support during single and dual-task conditions[8].

ACCEPTED MANUSCRIPT In additional to these subtle, ongoing changes in motor control, emerging epidemiological research has most recently demonstrated an association between concussion and lower extremity injuries in the months and years following injury[18, 19] with a link drawn between concussion and anterior cruciate ligament (ACL) injuries[20]. The underlying biomechanical differences that may result in increased injury risk however, are not clear. One recent study by DuBose et al[21] compared Division I football players

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completing a drop-landing task before and after the competitive season. Those athletes with a diagnosed

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concussion during the season demonstrated significantly greater changes in hip, knee and leg stiffness at

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the post-season assessment, providing some evidence to suggest that there are biomechanical changes that can be associated with concussion. However, there has yet to be a study evaluating kinematic differences

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in those with and without a concussion history during a complex dynamic motor task (e.g. cutting maneuver) that more closely resembles the demands of sport. This knowledge is critical in our

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understanding of motor differences following concussion as it has been estimated that up to 70% of

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anterior cruciate ligament (ACL) injuries occur during the planting and cutting movements[22]. Thus, the purpose of this investigation was to evaluate differences between concussed individuals and matched

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controls during a jump cut maneuver with a dual cognitive task. We hypothesize that those with a concussion history will demonstrate differences in lower extremity kinematics that are consistent with

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increased risk of knee injury.

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Materials and Methods Participants

This investigation included control (n=10; 6 males, 4 females) and previously concussed (n=9; 4 males, 5 females) participants. Participants’ self-reported concussion history was determined via prescreening questionnaire. All participants also completed a brief health history questionnaire to determine eligibility. Participants were included if they were between the ages of 18 and 26, capable of engaging in a jump cut motion, and played a varsity level high school sport. Participants were excluded if they were taking medications or had an orthopedic or neurological condition that may affect balance,

ACCEPTED MANUSCRIPT ability to jump, land, or walk. Participants were also excluded if they had sustained a concussion after the age of 19 or the previous 6 months. Additional exclusion criteria included a history of hip, knee or ankle injuries that required medical attention within the past 6 months, or were pregnant or thought they may be pregnant. Information on limb dominance was also collected. The dominant leg was defined as the leg

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used to kick a ball. All participants were right leg dominant.

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Concussion history was obtained via self-report by asking each participant two questions in a

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manner similar to previous reports [8, 11, 23]. The question first asked if the individual had sustained a concussion that was diagnosed by a medical professional (e.g. physician, athletic trainer, nurse). The

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second question asked if the individual had sustained a blow to the head that resulted in concussion related symptoms provided on a list, but was not evaluated by a medical professional. Those placed in the

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concussed group must have indicated at least one diagnosed concussion and those in the control group

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must have indicated no to both questions. Time from injury was also collected and the concussed participants were evaluated on average 3.1 years (Median=1.7 years; SD=2.8 years, Range=0.9 to 6.5

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years) after their most recent concussion. A detailed description of the participant demographics (i.e. mean and standard deviation) are provided in Table 1. Participants provided informed consent before

--Insert Table 1 here--

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data collection by signing an Institutional Review Board approved document.

Experimental Protocol

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Participants were positioned a distance of 120% of their leg length from the front edge of a force platform. A box was placed between the participant and force platform at a distance of 85% of leg length for the participant to jump over. On their own volition, the participant was instructed jump forward, over the box using both feet, to land on their dominant (right) leg, then cut to either the left or right. The testing protocol consisted of three conditions: During the first condition (i.e. Anticipated jump) participants were informed the direction they would be cutting after landing on the force platform before initiating the jump. The second and third condition, (i.e. Congruent and Incongruent jumps), were tested concurrently.

ACCEPTED MANUSCRIPT During these trials participants were to direct their cut in response to the center arrow of the Flanker Task (for review see[24]). Congruent and Incongruent trials consisted of arrow displays in which the target (i.e. center) arrow was flanked by arrows of the same (<<<<<) or opposing (>><>>) directions, respectively (Figure 1). The arrows were displayed on a computer screen approximately 4.5m away from the force plate. Presentation of the Flanker Task arrows was triggered when the participant broke a beam of light

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immediately after jumping. The trigger occurred approximately 0.5 s prior to contact with the ground. All

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conditions were repeated randomly until a total of five successful trials were performed for each of the

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Anticipated, Congruent and Incongruent condition to the left and right, or 6 total conditions. Data Analysis

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During all trials, kinematic data were captured at 120 Hz using a 16-camera motion capture system (Motion Analysis, Santa Rosa, CA, USA)[25]. Forty reflective markers were placed on the trunk

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and lower limbs to track motion of the trunk and lower body. Marker position data were filtered using a

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4th-order low-pass Butterworth filter with cutoff frequency at 6 Hz in Visual3D (CMotion, Germantown, MA). Markers placed on the segments and bony landmarks were used to create an 8-segment model

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consisting of the trunk, pelvis, thighs, shanks, and feet in Visual3D. The trunk segment was tracked using markers placed on the 7th cervical vertebrae, sternal notch, 8th thoracic vertebrae, and xiphoid process.

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The pelvis segment was defined proximally by markers on the right and left iliac crests and distally by the

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right and left greater trochanter[26]. The knee and ankle joint centers were estimated using markers placed over the following bony landmarks: medial and lateral femoral condyles, medial and lateral malleoli.

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Three markers (1 lateral and 2 medial) were placed on each of the thigh and shank segments for 3D motion tracking. Joint angles were defined as the three dimensional motion of the distal segment relative to the proximal segment using Euler angle decomposition with motion in the sagittal plane as the first rotation, motion in the frontal plane as the second rotation, and motion in the transverse plane as the third rotation[27]. Ground reaction forces were collected at 1200 Hz using an AMTI force platform (AMTI, Watertown, MA, USA).

ACCEPTED MANUSCRIPT --Insert Figure 1 here--

The location of the whole body center of mass (COM) was computed as the weighted sum of each body segment’s COM. Vertical COM position was normalized to each participant’s height for comparison across individuals. Trials were deleted from the analyses if it was determined that a single legged, rather than two-

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legged, jump was performed during the initial (loading) stage of the jumping maneuver. In the end, 563 of 570 possible trials were used for statistical analysis. This investigation centered on the landing phase of

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the maneuver, which began the instance data from the force plate exceeded 1 Newton and ended once it

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had returned to zero (foot on to foot off). Data was time normalized to 0 to 100% of the landing movement (101 points) in Visual3D and subsequently exported into Matlab (Mathworks, Natick, MA,

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USA) where peak joint angles and COM displacement were obtained.

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Statistical Analyses

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The primary dependent measures were relative vertical center-of-mass (COM) and knee valgus/varus, internal/external rotation and flexion/extension peak angles for the dominant (right) leg.

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Statistical comparisons were performed in SPSS (version 24) with a significance level of p<0.05. To improve statistical power, knee angles and COM position were evaluated in separate analyses for

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differences between landing on the dominant (i.e. right) leg and cutting to the right or left and within

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Flanker Task conditions. Seeing no differences within individual trials (p’s>0.05), trials were collapsed within a given condition and each variable of interest was evaluated using a mixed model ANOVA where Group was used as a between-subjects factor (Concussed and Control) and Flanker condition was used as a within-subjects factor (Anticipated, Congruent, Incongruent) for each direction of the cutting maneuver. Degrees of freedom were corrected using Greenhouse-Geisser estimates of sphericity when the assumption of sphericity was violated.

ACCEPTED MANUSCRIPT Results The analyses for COM indicated a significant Group×Condition effect for both cutting directions [Left: F(1.81, 162.55)=7.73, p=0.001; Right: F(1.86, 159.92)=4.81, p=0.011] . To assess this interaction, contrasts were performed which revealed that as Flanker Conditions increased in cognitive demand (i.e. Anticipated to Congruent to Incongruent), the concussed group demonstrated significant increases in

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COM displacement relative to controls (Figure 2) for both directions of the cutting maneuver (Table 2) as

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cognitive load increased.

Analyses of knee external rotation during left-sided trials did not indicate a Group×Condition

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interaction (p=0.629) but there was a significant Group effect, F(1,90)=24.16, p<0.001. The Group

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analysis of external rotation indicated significantly less external rotation among the concussed group (Table 2). During right-sided trials, a significant Group×Condition effect was observed F(1.81,

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152.46)=6.82, p=0.003. Contrasts revealed that participants showed less external rotation during the

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Congruent and Incongruent conditions in comparison to the Anticipated trials (p’s<0.05). There was no significant difference between the Congruent and Incongruent conditions (Figure 2). Moreover, controls

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demonstrated lower levels of external rotation as cognitive load increased, whereas the same trend was

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not present in concussed participants.

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Analyses for knee varus indicated no Group×Condition interaction for either direction (Left: p=0.073; Right: p=0.166), nor Condition main effect (p=0.178) for right-sided trials. However, in left-sided trials a significant main effect of Condition was noted, F(1.84, 156.61)=7.98, p=0.001. The Group main effect was significant (Table 2) whereby the concussed group showed less varus when compared to the controls. Moreover, the peak measures of valgus/varus in concussed participants performed the left-sided cutting maneuver resulted in valgus during unanticipated trials, whereas peak measures in anticipated trials were in varus. Peak measures of this kinematic variable resulted in varus for all conditions in control participants.

ACCEPTED MANUSCRIPT Analysis of peak knee flexion indicated a significant Group×Condition interaction for both cutting directions [Left: F(2, 180)=4.22, p=0.016; Right: F(2, 172)=5.32, p=0.006]. Further analyses revealed a Condition effect, with contrasts showing more flexion during both the Congruent and Incongruent conditions in comparison to the Anticipated trials (p’s>0.05). There was no significant difference between the Congruent and Incongruent conditions (Figure 2) for flexion. Group differences

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demonstrated a trend for concussed participants to show less peak knee flexion as cognitive load

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increased in comparison to controls (Left: F(2,179.62)=4.22, p=.016; Right: F(1.946,167.33)=13.57,

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p=.006) (Table 2). --Insert Table 2 here--

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--Insert Figure 2 here--

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Discussion

Concussion has been linked to gross differences in cognitive and motor processes that typically

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resolve within two weeks of injury[7, 28, 29]. A growing body of literature is now showing persistent sub-

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clinical alterations to motor function such as balance[30-32] and gait[8, 33] that are present years after acute injury resolution. These differences have been associated with increased rates of knee [18, 19] and ACL

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injury[19] at the epidemiological level, but the biomechanical differences that may lead to these injuries is not understood. To our knowledge this study was the first investigation to evaluate jump cut kinematics

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in a previously concussed group of participants while simultaneously responding to a cognitive task (i.e.

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Flanker Task). This methodology was selected in an attempt to replicate ‘real world’ scenarios that require both planned and reactionary actions with variable levels of decision making. In our investigation, those participants with a concussion history demonstrated less knee varus and knee external rotation, ultimately placing them into valgus and internal rotation during a portion of the cutting maneuver (Figure 2). Alterations in frontal plane mechanics[34], specifically, increased knee abduction (valgus) angles[34, 35] and internal rotation of the knee[36, 37] are thought to increase ACL injury risk[38-41].

ACCEPTED MANUSCRIPT Additionally, the kinematic differences observed here were moderated by the increasing cognitive demands, in that the concussed participants demonstrated increasing relative vertical COM and knee flexion with greater cognitive load (see Figure 2). Our findings demonstrating changes over increasingly complex conditions, align with other studies that have also evaluated differences between anticipated and unanticipated maneuvers[42-44]. McLean[45] observed greater peak knee abduction in unanticipated

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conditions in comparison to anticipated conditions, an observation that was inconsistent in our

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experiments. Differences in COM displacement have been reported among concussed individuals during

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a gait assessment [12] and higher COM vertical position during impact has been associated with ACL injury[46]. In addition, previous research has reported that the direction of the cutting maneuver relative to

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the plant and cut leg significantly influenced peak knee valgus (i.e. knee abduction) angle during landing[47], our results confirmed these findings however the direction of the effect between groups

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remained consistent for both left and right sided conditions.

Others have investigated altered motor performance in those with a concussion history. Several

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studies[17, 48] have suggested that motor function differences remain present months following concussion, a much larger recovery time than observed on neuropsychological which typically recover within two

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weeks post-injury[49]. Rochefort et al[30] demonstrated balance deficits remained prominent one month

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postconcussion. Our findings resulted from a much larger post-injury window (Range=0.9-6.5 years; Mean=3.1 years; Median=1.7 years; SD=2.3 years), but are consistent with work from Sosnoff et al[11]

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showing ongoing differences in balance at four years post-injury and Martini et al[8] showing discrepancies in gait 6.3 years following injury. Furthermore, motor cortex excitability, an underlying process to motor control, was significantly prolonged among a group of 60 year olds approximately 25 years following their last injury[50]. Lastly, differences in outcome variables evaluated in this assessment can neither confirm nor deny results reported by DuBose et al[21] as the nature of the tasks between experiments (jump cutting vs jump landing), in addition to the kinematics explored, would render any comparison questionable. Regardless, each of these investigations indicate unresolved differences in

ACCEPTED MANUSCRIPT motor patterns among those with a concussion history. Our findings add to these works and support the hypothesis that motor/kinematic changes following concussion remain long after neuropsychological symptoms have returned to clinically normal levels.

Future Directions

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Our findings are consistent with the hypothesis suggesting a link between concussion and lower

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extremity injury by identifying kinematic changes in the previously concussed cohort [18] [19]. Although

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the underpinnings of these findings cannot be fully elucidated from the current investigation, we propose the following paradigm to explain the relationship. Previous works have indicated that concussed

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individuals have impaired transcallosal inhibition[51], cerebrocerebellar dysfunctions at the level of the cerebellum[52], and demonstrate suppressed motor learning[53]. These differences suggest that concussed

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participants may fail to properly integrate afferent information into pre-planned motor patterns to execute

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a jump cut maneuver in safest and most efficient manner. By not learning from the previous action and failing to fully integrate proprioceptive and exteroreceptive feedback in subsequent movement planning

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(Figure 3 - A), the executed movement remains flawed, again placing the individual at increased injury risk when executed (Figure 3 - B). These flawed landing patterns maneuvers may lead to repeated micro

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trauma to knee ligaments (e.g. ACL) and reducing the force required to produce the initial knee injury

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shown in Figure 3. An alternative to this theory may be taken from two recent studies [54, 55] suggesting that concussion does not alter biomechanics in manner consistent with increased injury risk, rather these

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individuals had irregular kinematic patters prior to the concussive injury. --Insert Figure 3 here--

This study has several limitations. First, there was an uneven distribution of genders between groups. This may limit our ability to detect differences as prior work which has shown clear gender differences in kinematics[56, 57]. To address this limitation analysis of covariance was initially performed in order to assess any potential interactions of gender on the main effect reported in this text. Although no gender effects were found in this sample this may be due to insufficient sample size. With a larger

ACCEPTED MANUSCRIPT sample size optimal parametric statistics could be implemented to assess this relationship in greater detail. Our original experiment also collected variables during the loading and air time portion of the jump cut task, however we chose to evaluate peak kinematics solely during the landing phase. Future research should seek to replicate our findings using a prospective design and evaluate these other phases. Lastly, additional variables quantifying kinematics of the hip and ankle, along with moment and power kinetics

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were not evaluated in this investigation, but should be included in future works.

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Conclusion

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This investigation identified kinematic differences during a jump-cut maneuver at the knee and COM in those with a concussion history years’ after injury. This finding adds to a growing body of

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literature demonstrating ongoing motor control differences following concussion and are likely associated with epidemiological reports of increased lower extremity injury risk following concussion. How these

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changes relate to reported differences in cognitive functioning are not clear, but as concussion is a diffuse

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brain injury, the two are likely linked. Future work should evaluate kinematic changes rather than kinetic observations as described in this study in order to ascertain a more direct link with the mechanisms of

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lower-body injury that are present postconcussion.

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Figure 1. (A,B) Participants jumped forward, with both feet a distance of 120% of their leg length. They landed on a force platform with their dominant leg (C). The cut was directed in response to the center arrow of the Flanker task.

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Figure 2. Differences in center-of-mass and knee kinematics based on each Flanker condition. Concussed group scores are light grey and Control group scores are dark grey. Significant group differences were noted for knee varus and external rotation when collapsed across condition (Column 1). In the knee varus and external rotation figures shown on the right, negative values indicate valgus and internal rotation respectively. Error bars are denoted using the standard error of the mean

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Figure 3. Conceptual framework leading to increases in lower-body injury in concussion. Sensory integration failure is hypothesized to occur in the cerebellum. Figure adapted from Barrack and Munn[58]. By not learning from the previous action and failing to fully integrate proprioceptive and exteroreceptive feedback in subsequent movement planning (Figure 3 - A), the executed movement remains flawed, again placing the individual at increased injury risk when executed (Figure 3 - B). These flawed landing patterns maneuvers may lead to repeated micro trauma to knee ligaments (e.g. ACL) and reducing the force required to produce the initial knee injury shown in Figure 3.

ACCEPTED MANUSCRIPT Table 1. Participant Demographics. Metrics are presented as Means (standard deviations)

M ED PT CE AC

Weight (kg) 61.2 54.4 74.8 56.7 55.3 72.6 90.7 71.0 83.9 70.5 (13.0) 71.7 (10.3)

Number of Concussions 1 3 5 1 10 3 2 5 2 4 (3) 0

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Height (m) 1.62 1.70 1.80 1.57 1.47 1.75 1.85 1.75 1.82 1.72 (0.13) 1.75 (0.11)

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Age 20 18 18 21 20 21 22 24 20 20 (2) 20 (2)

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ID 1 2 3 4 5 6 7 8 9 Mean (SD) Mean (SD)

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Times since last Concussion (years) 5.83 0.87 1.08 3.67 1.58 1.25 6.5 5.75 1.66 3.1 (2.3) 0

ACCEPTED MANUSCRIPT Table 2. Center of Mass and Knee Kinematic Differences Among Concussed and Control Participants Across all Flanker Conditions

Knee Varus Left Knee External Rotation Knee Flexion Relative Vertical COM Knee Varus Right Knee External Rotation Knee Flexion

.428 .433 3.585 -.505 13.010 2.489 77.484 75.070 .435 .436 7.795 5.056 12.774 7.729 74.139 71.544

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.002 .002 .973 1.016 1.480 1.546 1.143 1.194 .002 .002 1.115 1.167 1.498 1.568 1.308 1.369

95% Confidence Interval Lower Bound Upper Bound .424 .431 .429 .436 1.652 5.518 -2.523 1.514 15.951 10.069 5.561 -.582 79.756 75.213 77.443 72.698 .431 .438 .432 .440 5.578 10.011 2.736 7.375 15.752 9.796 10.846 4.613 76.740 71.538 74.266 68.822

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Highlights  A retrospective 3D motion capture evaluation of kinematic changes postconcussion  Participants with a concussion history showed motor differences compared to controls years post injury  These differences parallel the most common mechanism of ACL injury