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Exertion and pain do not alter coordination variability in runners with iliotibial band syndrome
Clinical Biomechanics 47 (2017) 73–78
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Exertion and pain do not alter coordination variability in runners with iliotibial band syndrome
MARK
Jocelyn F. Hafera,⁎, Allison M. Brownb, Katherine A. Boyera a b
Department of Kinesiology, University of Massachusetts Amherst, USA Department of Rehabilitation & Movement Sciences, School of Health Professions, Rutgers, The State University of New Jersey, USA
A R T I C L E I N F O
A B S T R A C T
Keywords: Dynamical systems analysis Vector coding Running injury
Background: Iliotibial band syndrome is a common overuse running injury which results in altered mechanics. While injuries alter discrete mechanics, they may also cause a change in coordination variability, the stride-tostride organization of runners' movement patterns. Uninjured and injured runners may experience a change in coordination variability during a run to exertion due to fatigue, pain, or a combination of these factors. The aim of the current study was to determine if runners with iliotibial band syndrome and uninjured runners display different segment coordination variability across the course of a run to exertion. Methods: 3D kinematics were collected as 13 uninjured runners and 12 runners with iliotibial band syndrome ran on a treadmill. A modified vector coding technique was used to calculate coordination variability during stance for segment couples of interest. Coordination variability was compared between uninjured and injured runners at the beginning and end of the run. The influence of pain on coordination variability was also examined. Findings: There were no differences in coordination variability at the beginning or end of the run between uninjured runners and those with iliotibial band syndrome. The change in coordination variability due to the run was not different between uninjured runners, injured runners who experienced no change in pain, and injured runners who did experience a change in pain. Interpretation: Runners do not constrain the patterns of segment motion they use in response to exertion nor does it appear that occurrence of pain during running results in a differential change in coordination variability.
1. Introduction Running is a popular form of exercise which results in overuse injury in as many as 79% of participants (van Gent et al., 2007). One of the most common overuse running injuries is iliotibial band syndrome (ITBS) (Taunton et al., 2002) which is characterized by pain in the lateral aspect of the knee that often worsens progressively throughout a run. The mechanism for ITBS injury is thought to be altered joint mechanics. Previous studies have demonstrated that runners with a history of (Ferber et al., 2010; Miller et al., 2007), those who go on to develop (Noehren et al., 2007) and those currently experiencing (Grau et al., 2011) ITBS display altered joint mechanics in comparison to healthy runners (Foch et al., 2015). Runners with a history of ITBS also have a different mechanical response to a run to exertion than that of uninjured runners (Miller et al., 2007). This differential response to an extended duration run in runners with a history of or current ITBS has been suggested to be a result of the onset or avoidance of pain. However, recent studies have found that, in comparison to uninjured ⁎
runners, those with a history of ITBS or currently symptomatic ITBS display few (Brown et al., 2016) or none (Foch and Milner, 2014; Foch et al., 2015) of these specific differences in joint mechanics. Thus, studies of discrete kinematic variables fail to provide a clear picture of the role of both exertion and pain in the alteration of movement patterns with ITBS. It has been proposed that as a consequence of altered muscle activity in response to or to avoid a painful stimulus, variability in the coordination of movement may decrease (Hamill et al., 1999; Hodges and Tucker, 2011). Overuse running injuries in general, and ITBS specifically, have been associated with decreased coordination variability (as assessed through various methods; (Heiderscheit et al., 2002, Miller et al., 2008)). Lower coordination variability suggests decreased flexibility of the motor system as an individual uses fewer patterns of joint or segment motion to produce a complex task, such as locomotion (Newell, 1985). As a consequence of using fewer patterns of segment motion, lower segment coordination variability may also be suggestive of mechanics that are restricted to a narrow area or range of tissues.
Corresponding author at: 30 Eastman Lane, 110 Totman Building, University of Massachusetts Amherst, Amherst, MA 01003, USA. E-mail address: [email protected] (J.F. Hafer).
http://dx.doi.org/10.1016/j.clinbiomech.2017.06.006 Received 2 January 2017; Accepted 7 June 2017 0268-0033/ © 2017 Published by Elsevier Ltd.
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2.3. Experimental protocol
Thus, decreased segment coordination variability in runners may be a manifestation of an individual's attempt to avoid pain during a run or an inability to access their full range of movement patterns due to an injury (Hamill et al., 2012). In uninjured runners and those with a history of injury, segment coordination variability appears to change over the course of a run, perhaps as a consequence of exertion or muscle fatigue (MacLean et al., 2010). Thus, the onset or presence of muscle fatigue during a run may compound the effects of injury on segment coordination variability. For runners with current ITBS, there is currently a lack of data on segment coordination variability, and it is unknown how this coordination variability may change during an extended run or in response to an increase in pain throughout a run. The aim of the current study was to determine if runners with ITBS and uninjured runners display different segment coordination variability over the course of a run to high exertion. It was hypothesized that there would be differences in coordination variability between groups (uninjured coordination variability > ITBS coordination variability) and across time (beginning vs. end of run), and that the uninjured and ITBS groups would display a different change in coordination variability in response to the run (group × time interaction). While ITBS pain typically presents in response to running, our previous work with an ITBS population suggests there is significant inter-individual variance in this pain increase. If the current study participants displayed varied pain responses, we sought to explore whether different levels of induced pain altered the uninjured vs. ITBS comparisons.
Data collection began with the collection of a static calibration trial used to calculate segment characteristics and knee and ankle joint centers. In addition, a dynamic calibration trial was captured and used to calculate a functionally determined hip joint center (Schwartz and Rozumalski, 2005). Next, participants ran on a treadmill at a self-reported 5-kilometer race pace for a 3 minute acclimatization period at which time 30 s of pre-exertion ‘beginning of run’ data were collected. Participants then continued their treadmill run at their self-selected race pace until volitional exhaustion with data captured every 3 min. Level of exertion and pain were also monitored every 3 min throughout the run to exertion. Exertion was quantified using the Borg Rating of Perceived Exertion (RPE) scale (Borg, 1982). Pain symptoms were monitored using the Borg CR-10 verbal numerical rating scale (vNRS). Once participants reached an RPE of 17/20 or a vNRS rating of 6/10, a final 30 s of post-exertion ‘end of run’ data were collected. An increase in vNRS pain of 2 points was considered a clinically significant change (Farrar et al., 2001). 2.4. Data processing Ten strides of data were extracted for runners' dominant (uninjured participants) or injured (ITBS participants) limb from their pre- and post-exertion data collection (Hafer and Boyer, 2016). Data were processed with custom code written in LabView (National Instruments, Austin, TX) and Visual 3D (C-Motion, Inc., Rockville, MD). Bi-directional second-order low-pass Butterworth filters achieving fourth-order attenuation were used to smooth kinematic data at 8 Hz. Segment angles for the pelvis, thigh, shank, and rearfoot with respect to the global coordinate system were calculated and normalized to 100% of the gait cycle for each trial. Segment coordination was calculated using a custom MATLAB (MathWorks, Natick, MA) program. Angle-angle plots of the couplings of interest were created and coupling angles (Θ) were calculated as the angle with respect to the right horizontal created by the vector connecting two consecutive time points (Chang et al., 2008):
2. Methods 2.1. Participants Two groups of female runners were recruited for this study: those who were free from neuromuscular and musculoskeletal injury in the previous 6 months, and those who had iliotibial band syndrome. Based on previous studies, at least 10 participants per group were needed for between-group comparisons (Cunningham et al., 2014) and at least 4 participants per group were needed for repeated measures comparisons (Hafer et al., 2016) to achieve a power level of 0.8 with an alpha level of 0.05. Iliotibial band syndrome status was verified by a physician or a physical therapist based off of reported symptoms of lateral knee pain during a run and positive Noble Compression test. Individuals qualified for the study if they were currently running at least 15 miles/week, were able to run at least one 9-minute mile and were a rearfoot striker. A study investigator (AB) visually verified that each individual was a rearfoot striker prior to enrollment in the study. This was confirmed by inspection of kinematics after data were collected. All procedures were approved by the institutional review board for human subjects research. All participants provided written informed consent prior to completing any study procedures.
Θi,j = tan−1 [(yi,j + 1 − yi,j) (xi,j + 1 − xi,j)] where 0 ≤ Θ ≤ 360° and j is a percent gait cycle of the ith trial. Coupling angles were calculated using circular statistics (Batschelet, 1981). Coordination variability was calculated as the circular standard deviation of the coupling angle at each individual point of the gait cycle across ten strides of data (Batschelet, 1981). This circular standard deviation was averaged across the stance phase for each subject. Couplings of interest included frontal pelvis rotation vs. frontal thigh rotation, sagittal thigh rotation vs. sagittal shank rotation, sagittal thigh rotation vs. transverse shank rotation, and transverse shank rotation vs. frontal rearfoot rotation couples. These couplings were selected as they contribute to joint kinematics which are thought to increase iliotibial band strain (Hamill et al., 2008; Miller et al., 2007).
2.2. Instrumentation Twelve motion analysis cameras (Motion Analysis Corporation, Santa Rosa, CA, USA) were used to collect 3-dimensional kinematic data. Retroreflective markers were placed on designated locations to define the trunk (right and left acromioclavicular joints and sacrolumbar joint), pelvis (left and right ASIS and sacro-lumbar joint), thigh (functionally-determined hip joint center and medial and lateral femoral epicondyles), shank (medial and lateral femoral epicondyles, tibial tuberosity, and medial and lateral malleoli), foot (heel and first and fifth metatarsal heads), and rearfoot (superior and inferior, lateral and medial aspects of the proximal calcaneus). Additional array clusters were placed on the thigh and shank for segment tracking purposes. All participants wore standard, lab-provided footwear (New Balance 1062, Boston, MA, USA) and rearfoot markers were attached to participants' feet through windows cut in the shoes. Kinematic data were sampled at 120 Hz.
2.5. Statistics Statistical tests were carried out to compare the mean stance phase coordination variability between groups for each of the four coupling angle comparisons of interest. In accordance with the hypotheses that coordination variability would be different between 1) uninjured runners and those with ITBS and 2) the beginning and end of the run, coordination variability was compared by group (uninjured vs. ITBS) and across time (beginning vs. end of run) using 2-way ANOVAs with time as a within-subjects variable. If significant interactions were found, paired t-tests were used to examine main effects within the interaction. As it was discovered post-hoc that ITBS runners had varied pain responses to the run to exertion, exploratory statistics were 74
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course of a run to exertion. Contrary to our hypotheses, there were no significant differences in segment coordination variability between ITBS and uninjured runners and for the most part runners with ITBS did not respond differently to the run to exertion compared to uninjured runners. One exception was the thigh vs. shank sagittal plane couple where a trend for a significant time by group interaction was found. Post-hoc simple main effects test of time found no significant change in coordination variability over time for either group. In our exploration of the impact of pain induced by a run to exertion, we did not observe significant differences in the magnitude of change in segment coordination variability between groups (uninjured, ITBS with no pain, ITBS with pain). To date, few studies have examined the effect of a run to high exertion on coordination variability in runners with ITBS (Miller et al., 2008). In their work, Miller and colleagues examined coordination variability assessed by continuous relative phase (CRP) over the course of a treadmill run in uninjured runners and runners with a history of ITBS (Miller et al., 2008). Similar to our findings, the authors reported no significant interactions between group and time with respect to coordination variability. While Miller et al. employed a different variability measure, together, our findings suggest that runners with a history of, or currently symptomatic ITBS, do not respond differently to exertion than do their healthy counterparts in these measures of variability. In addition to testing for an interaction between group and time, we also examined for the main effects of group and/or time. Our study did not show a main effect of group. At the start of the run, without possible interaction of fatigue, runners with ITBS did not demonstrate any differences in coordination variability compared to the uninjured cohort. The lack of difference in coordination variability between injured and uninjured runners is in contrast to previous studies which observed lower coordination variability in injured runners (Heiderscheit et al., 2002; Seay et al., 2011). These studies examined segment coordination variability via a vector coding technique similar to the current study in runners with alternate diagnoses such as low back pain (Seay et al., 2011) or patellofemoral pain syndrome (Heiderscheit et al., 2002). The mechanism of injury and kinematic variables of interest for these diagnoses are unique to that of the patient with ITBS and therefore may need to be considered independently of our work. In work by Miller and colleagues, the authors did report less CRP coordination variability with respect to some couplings and greater variability with respect to others in runners with a history of ITBS as compared to uninjured runners (Miller et al., 2008). In contrast, Hein and colleagues present similar findings to ours with respect to ITBS injury status when examining CRP coordination variability whereby no significant between-group differences were noted (Hein et al., 2012). It is important to note that measures of coordination variability may differ when calculated using modified vector coding or CRP methods (DeLeo et al., 2004; Miller et al., 2010). Thus, the impact of injury on coordination variability remains unclear. In patients with ITBS, endurance, as tested by the ability to maintain kinematic patterns in a setting of fatigue, is often considered a critical
Table 1 Participant characteristics. Pain was assessed using a 0–10 verbal numerical rating scale.
N Age (years) Height (m) Body mass (kg) Run speed (m/s) Run duration (min) Change in pain
Uninjured
ITBS
Mean
SD
Mean
13 30.23 1.63 56.22 3.33 25.15
7.01 0.11 5.74 0.15 6.54
12 32.67 1.70 60.36 3.01 25.25
ITBS pain
ITBS no pain
SD
Mean
SD
Mean
SD
7.73 0.06 5.37 0.35 8.34
5 33.20 1.68 59.50 3.10 22.80 4.80
4.76 0.06 4.06 0.45 5.45 1.25
6 33.50 1.72 61.43 2.88 27.00 0.67
10.01 0.05 6.87 0.26 10.90 0.61
performed to examine the effect of pain on coordination variability. 1way ANOVAs were used to compare the change in coordination variability between uninjured runners, ITBS runners who had an increase in pain during the run, and ITBS runners who did not have an increase in pain during the run. Significance was set at P < 0.05 for all comparisons with a trend operationally defined as P < 0.10. Where significant main effects were found, post-hoc comparisons were made using Tukey's test. 3. Results Participants who completed the protocol included 13 uninjured runners and 12 runners with iliotibial band syndrome. Average run duration for the entire cohort was 25.13 min. Run duration was not significantly different between uninjured runners and ITBS runners or between pain and no pain ITBS groups (Table 1). Participant characteristics are detailed in Table 1. Over the course of the run, 5 runners with iliotibial band syndrome developed clinically significant pain and 6 did not (pain data were incomplete for one runner). Two ITBS runners discontinued the run due to pain (vNRS ≥ 6) at an RPE of 15. When comparing uninjured and injured runners as well as the beginning and the end of the run, there were no significant differences by group or by time in any segment couples (Table 2). At the sagittal thigh vs. sagittal shank rotation couple there was a trend towards a significant group by time interaction (P = 0.06) where uninjured runners had a decrease and runners with iliotibial band syndrome had an increase in coordination variability from the beginning to the end of the run. This pattern, while not significant, also appeared in the frontal pelvis vs. thigh frontal rotation couple as well as the sagittal thigh vs. transverse shank rotation couples (Fig. 1). The comparison of the change in coordination variability across uninjured, ITBS with pain, and ITBS without pain revealed no significant differences between groups (Fig. 2, Table 3). 4. Discussion The purpose of this study was to determine if symptomatic runners with ITBS display different segment coordination variability compared to uninjured runners and if this difference is exacerbated over the
Table 2 Average stance phase coordination variability at the beginning and end of a run to exertion in uninjured runners and those with iliotibial band syndrome for four segment couples of interest. Uninjured
ITBS
Beginning
Pelvis frontal vs. thigh frontal (°) Thigh sagittal vs. shank sagittal (°) Thigh sagittal vs. shank transverse (°) Shank transverse vs. rearfoot frontal (°)
End
P-value
Beginning
End
Mean
SD
Mean
SD
Mean
SD
Mean
SD
13.37 2.85 6.93 11.61
7.54 1.18 2.80 3.53
11.29 2.52 6.45 11.00
4.19 0.61 1.91 4.06
12.90 2.82 7.50 13.39
4.46 0.51 2.40 4.19
14.13 3.43 7.82 11.91
6.92 1.45 2.66 2.72
75
Group
Time
Group × time
0.55 0.19 0.25 0.32
0.76 0.59 0.89 0.12
0.24 0.06 0.46 0.51
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J.F. Hafer et al.
Thigh sagittal vs. Shank sagittal 8
30
7
Coordination Variability (°)
Coordination Variability (°)
Pelvis frontal vs. Thigh frontal 35
25 20 15 10
6
Uninjured - beginning
5
Uninjured - end ITBS - beginning
4
ITBS - end 3 2
5
1
0
0
Thigh sagittal vs. Shank transverse
Shank transverse vs. Rearfoot frontal 25
16
Coordination Variability (°)
Coordination Variability (°)
14 12 10 8 6 4
20
15
10
5
2 0
0
Fig. 1. Coordination variability during stance at the beginning and end of the run for uninjured runners and runners with iliotibial band syndrome. Dark horizontal lines indicate group mean, grey horizontal lines indicate ± SD. Values detailed in Table 2.
this study do not refute this point nor suggest that exertion does not play a critical role in running injuries. Rather, our results suggest that any increased susceptibility to running injury during high exertion is not likely due to alterations in coordination variability. The lack of significant differences by group or time of run could
component of a rehabilitation program. When examining the main effect of time on coordination variability, our results suggest that a run to exertion does not affect coordination variability. There are several studies suggesting that fatigue may relate to running injuries (Dierks et al., 2010; Meardon et al., 2011; Voloshin et al., 1998). The results of
Thigh Sagittal vs. Shank sagittal 4
10
3
Coordination Variability (°)
Coordination Variability (°)
Pelvis frontal vs. Thigh frontal 15
5 0 -5 -10 -15 -20
2 1
-30
-4
Shank transverse vs. Rearfoot frontal 8
6
6
-2 -4
Coordination Variability (°)
Coordination Variability (°)
Thigh Sagittal vs. Shank transverse 8
0
ITBS - Pain
-2 -3
2
ITBS - No Pain
-1
-25
4
Uninjured
0
4 2 0 -2 -4 -6 -8
-6
-10
-8
-12
Fig. 2. Change in coordination variability during stance from beginning to end of run in uninjured runners, runners with iliotibial band syndrome who experienced pain in response to the run, and runners with iliotibial band syndrome who did not experience pain in response to the run. Dark horizontal lines indicate group mean, grey horizontal lines indicate ± SD. Values detailed in Table 3.
76
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Conflict of interest
Table 3 Change in average stance phase coordination variability in response to a run to exertion in uninjured runners and runners who did not or did experience pain during the run. Pvalues are reported for the comparison across all three groups. As there were no significant group differences, no post-hoc comparisons were made.
The authors declare no conflicts of interest. Acknowledgements
Pelvis frontal vs. thigh frontal (°) Thigh sagittal vs. shank sagittal (°) Thigh sagittal vs. shank transverse (°) Shank transverse vs. rearfoot frontal (°)
Uninjured
ITBS pain
ITBS no pain
Mean
SD
Mean
SD
Mean
SD
P-value
− 2.09
7.33
3.96
6.92
0.30
6.98
0.29
The authors wish to thank Dr. Howard Hillstrom and the Leon Root, MD Motion Analysis Laboratory at the Hospital for Special Surgery for support during the collection of data for this study.
− 0.34
0.97
1.04
2.11
0.36
0.72
0.11
References
− 0.48
1.85
0.14
4.13
0.86
3.24
0.62
− 0.61
1.89
−2.12
4.63
− 0.74
4.53
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potentially be explained by the fact that our injured group may actually have been made up of two subsets of runners: those who experienced pain and those who did not during their run to exertion. There may be a differential impact of injury and injury symptoms on coordination variability. The majority of studies reporting decreased coordination variability in ITBS compared to uninjured runners have examined an injured population that is not in pain (MacLean et al., 2010; Miller et al., 2008). Runners with currently symptomatic patellofemoral pain have displayed decreased coordination variability in comparison to uninjured runners in some studies (Hamill et al., 1999; Heiderscheit et al., 2002), while at least one study showed that runners with symptomatic patellofemoral pain had greater coordination variability in comparison to uninjured runners (Cunningham et al., 2014). We found there were no differences in the change in coordination variability by pain level. In the current study, it is evident that within the ITBS pain and ITBS no pain groups there was substantial inter-participant variation in response to the run to exertion (Fig. 2). Future studies should further examine the interaction between pain and coordination variability during a run to high exertion or fatigue. Nevertheless, when looking across a sample of runners who currently have ITBS, there does not appear to be a difference in coordination variability, nor does exertion affect them differently from healthy runners. In addition to the small sample size in the ITBS pain and ITBS no pain groups, the current study has a few limitations. First, data were collected as participants ran on a treadmill and coordination variability may differ between treadmill and overground running. The impact of this limitation on the findings of this study is likely minimal as all participants were exposed to the same running conditions and so any difference from overground running would be systematic. Additionally the use of treadmills in the study of running gait, especially for methods requiring at least 10 strides of input data, is increasingly common. Finally, while participants ran until they reached a standard level of subjective fatigue and the length of this run was not different between groups, it is possible that an objective measure of fatigue (e.g., change in muscle power) would reveal that not all participants were fatigued to the same extent.
5. Conclusions The results of this study suggest that segment coordination variability does not change from the beginning to the end of a run to exertion in either uninjured runners or runners who currently have ITBS. This finding indicates that, while joint kinematics or kinetics may change, runners do not constrain the patterns of segment motion they use in response to exertion. Additionally, it appears that the absence or occurrence of pain during a run does not result in a differential change in coordination variability. 77
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572–578. Taunton, J.E., Ryan, M.B., Clement, D.B., McKenzie, D.C., Lloyd-Smith, D.R., Zumbo, B.D., 2002. A retrospective case-control analysis of 2002 running injuries. Br. J. Sports Med. 36 (2), 95–101. Voloshin, A.S., Mizrahi, J., Verbitsky, O., Isakov, E., 1998. Dynamic loading on the human musculoskeletal system — effect of fatigue. Clin. Biomech. 13 (7), 515–520.
prospective study of the biomechanical factors associated with iliotibial band syndrome. Clin. Biomech. 22 (9), 951–956. Schwartz, M.H., Rozumalski, A., 2005. A new method for estimating joint parameters from motion data. J. Biomech. 38 (1), 107–116. Seay, J.F., Van Emmerik, R.E., Hamill, J., 2011. Low back pain status affects pelvis-trunk coordination and variability during walking and running. Clin. Biomech. 26 (6),
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Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Exertion and pain do not alter coordination variability in runners with iliotibial band syndrome
MARK
Jocelyn F. Hafera,⁎, Allison M. Brownb, Katherine A. Boyera a b
Department of Kinesiology, University of Massachusetts Amherst, USA Department of Rehabilitation & Movement Sciences, School of Health Professions, Rutgers, The State University of New Jersey, USA
A R T I C L E I N F O
A B S T R A C T
Keywords: Dynamical systems analysis Vector coding Running injury
Background: Iliotibial band syndrome is a common overuse running injury which results in altered mechanics. While injuries alter discrete mechanics, they may also cause a change in coordination variability, the stride-tostride organization of runners' movement patterns. Uninjured and injured runners may experience a change in coordination variability during a run to exertion due to fatigue, pain, or a combination of these factors. The aim of the current study was to determine if runners with iliotibial band syndrome and uninjured runners display different segment coordination variability across the course of a run to exertion. Methods: 3D kinematics were collected as 13 uninjured runners and 12 runners with iliotibial band syndrome ran on a treadmill. A modified vector coding technique was used to calculate coordination variability during stance for segment couples of interest. Coordination variability was compared between uninjured and injured runners at the beginning and end of the run. The influence of pain on coordination variability was also examined. Findings: There were no differences in coordination variability at the beginning or end of the run between uninjured runners and those with iliotibial band syndrome. The change in coordination variability due to the run was not different between uninjured runners, injured runners who experienced no change in pain, and injured runners who did experience a change in pain. Interpretation: Runners do not constrain the patterns of segment motion they use in response to exertion nor does it appear that occurrence of pain during running results in a differential change in coordination variability.
1. Introduction Running is a popular form of exercise which results in overuse injury in as many as 79% of participants (van Gent et al., 2007). One of the most common overuse running injuries is iliotibial band syndrome (ITBS) (Taunton et al., 2002) which is characterized by pain in the lateral aspect of the knee that often worsens progressively throughout a run. The mechanism for ITBS injury is thought to be altered joint mechanics. Previous studies have demonstrated that runners with a history of (Ferber et al., 2010; Miller et al., 2007), those who go on to develop (Noehren et al., 2007) and those currently experiencing (Grau et al., 2011) ITBS display altered joint mechanics in comparison to healthy runners (Foch et al., 2015). Runners with a history of ITBS also have a different mechanical response to a run to exertion than that of uninjured runners (Miller et al., 2007). This differential response to an extended duration run in runners with a history of or current ITBS has been suggested to be a result of the onset or avoidance of pain. However, recent studies have found that, in comparison to uninjured ⁎
runners, those with a history of ITBS or currently symptomatic ITBS display few (Brown et al., 2016) or none (Foch and Milner, 2014; Foch et al., 2015) of these specific differences in joint mechanics. Thus, studies of discrete kinematic variables fail to provide a clear picture of the role of both exertion and pain in the alteration of movement patterns with ITBS. It has been proposed that as a consequence of altered muscle activity in response to or to avoid a painful stimulus, variability in the coordination of movement may decrease (Hamill et al., 1999; Hodges and Tucker, 2011). Overuse running injuries in general, and ITBS specifically, have been associated with decreased coordination variability (as assessed through various methods; (Heiderscheit et al., 2002, Miller et al., 2008)). Lower coordination variability suggests decreased flexibility of the motor system as an individual uses fewer patterns of joint or segment motion to produce a complex task, such as locomotion (Newell, 1985). As a consequence of using fewer patterns of segment motion, lower segment coordination variability may also be suggestive of mechanics that are restricted to a narrow area or range of tissues.
Corresponding author at: 30 Eastman Lane, 110 Totman Building, University of Massachusetts Amherst, Amherst, MA 01003, USA. E-mail address: [email protected] (J.F. Hafer).
http://dx.doi.org/10.1016/j.clinbiomech.2017.06.006 Received 2 January 2017; Accepted 7 June 2017 0268-0033/ © 2017 Published by Elsevier Ltd.
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2.3. Experimental protocol
Thus, decreased segment coordination variability in runners may be a manifestation of an individual's attempt to avoid pain during a run or an inability to access their full range of movement patterns due to an injury (Hamill et al., 2012). In uninjured runners and those with a history of injury, segment coordination variability appears to change over the course of a run, perhaps as a consequence of exertion or muscle fatigue (MacLean et al., 2010). Thus, the onset or presence of muscle fatigue during a run may compound the effects of injury on segment coordination variability. For runners with current ITBS, there is currently a lack of data on segment coordination variability, and it is unknown how this coordination variability may change during an extended run or in response to an increase in pain throughout a run. The aim of the current study was to determine if runners with ITBS and uninjured runners display different segment coordination variability over the course of a run to high exertion. It was hypothesized that there would be differences in coordination variability between groups (uninjured coordination variability > ITBS coordination variability) and across time (beginning vs. end of run), and that the uninjured and ITBS groups would display a different change in coordination variability in response to the run (group × time interaction). While ITBS pain typically presents in response to running, our previous work with an ITBS population suggests there is significant inter-individual variance in this pain increase. If the current study participants displayed varied pain responses, we sought to explore whether different levels of induced pain altered the uninjured vs. ITBS comparisons.
Data collection began with the collection of a static calibration trial used to calculate segment characteristics and knee and ankle joint centers. In addition, a dynamic calibration trial was captured and used to calculate a functionally determined hip joint center (Schwartz and Rozumalski, 2005). Next, participants ran on a treadmill at a self-reported 5-kilometer race pace for a 3 minute acclimatization period at which time 30 s of pre-exertion ‘beginning of run’ data were collected. Participants then continued their treadmill run at their self-selected race pace until volitional exhaustion with data captured every 3 min. Level of exertion and pain were also monitored every 3 min throughout the run to exertion. Exertion was quantified using the Borg Rating of Perceived Exertion (RPE) scale (Borg, 1982). Pain symptoms were monitored using the Borg CR-10 verbal numerical rating scale (vNRS). Once participants reached an RPE of 17/20 or a vNRS rating of 6/10, a final 30 s of post-exertion ‘end of run’ data were collected. An increase in vNRS pain of 2 points was considered a clinically significant change (Farrar et al., 2001). 2.4. Data processing Ten strides of data were extracted for runners' dominant (uninjured participants) or injured (ITBS participants) limb from their pre- and post-exertion data collection (Hafer and Boyer, 2016). Data were processed with custom code written in LabView (National Instruments, Austin, TX) and Visual 3D (C-Motion, Inc., Rockville, MD). Bi-directional second-order low-pass Butterworth filters achieving fourth-order attenuation were used to smooth kinematic data at 8 Hz. Segment angles for the pelvis, thigh, shank, and rearfoot with respect to the global coordinate system were calculated and normalized to 100% of the gait cycle for each trial. Segment coordination was calculated using a custom MATLAB (MathWorks, Natick, MA) program. Angle-angle plots of the couplings of interest were created and coupling angles (Θ) were calculated as the angle with respect to the right horizontal created by the vector connecting two consecutive time points (Chang et al., 2008):
2. Methods 2.1. Participants Two groups of female runners were recruited for this study: those who were free from neuromuscular and musculoskeletal injury in the previous 6 months, and those who had iliotibial band syndrome. Based on previous studies, at least 10 participants per group were needed for between-group comparisons (Cunningham et al., 2014) and at least 4 participants per group were needed for repeated measures comparisons (Hafer et al., 2016) to achieve a power level of 0.8 with an alpha level of 0.05. Iliotibial band syndrome status was verified by a physician or a physical therapist based off of reported symptoms of lateral knee pain during a run and positive Noble Compression test. Individuals qualified for the study if they were currently running at least 15 miles/week, were able to run at least one 9-minute mile and were a rearfoot striker. A study investigator (AB) visually verified that each individual was a rearfoot striker prior to enrollment in the study. This was confirmed by inspection of kinematics after data were collected. All procedures were approved by the institutional review board for human subjects research. All participants provided written informed consent prior to completing any study procedures.
Θi,j = tan−1 [(yi,j + 1 − yi,j) (xi,j + 1 − xi,j)] where 0 ≤ Θ ≤ 360° and j is a percent gait cycle of the ith trial. Coupling angles were calculated using circular statistics (Batschelet, 1981). Coordination variability was calculated as the circular standard deviation of the coupling angle at each individual point of the gait cycle across ten strides of data (Batschelet, 1981). This circular standard deviation was averaged across the stance phase for each subject. Couplings of interest included frontal pelvis rotation vs. frontal thigh rotation, sagittal thigh rotation vs. sagittal shank rotation, sagittal thigh rotation vs. transverse shank rotation, and transverse shank rotation vs. frontal rearfoot rotation couples. These couplings were selected as they contribute to joint kinematics which are thought to increase iliotibial band strain (Hamill et al., 2008; Miller et al., 2007).
2.2. Instrumentation Twelve motion analysis cameras (Motion Analysis Corporation, Santa Rosa, CA, USA) were used to collect 3-dimensional kinematic data. Retroreflective markers were placed on designated locations to define the trunk (right and left acromioclavicular joints and sacrolumbar joint), pelvis (left and right ASIS and sacro-lumbar joint), thigh (functionally-determined hip joint center and medial and lateral femoral epicondyles), shank (medial and lateral femoral epicondyles, tibial tuberosity, and medial and lateral malleoli), foot (heel and first and fifth metatarsal heads), and rearfoot (superior and inferior, lateral and medial aspects of the proximal calcaneus). Additional array clusters were placed on the thigh and shank for segment tracking purposes. All participants wore standard, lab-provided footwear (New Balance 1062, Boston, MA, USA) and rearfoot markers were attached to participants' feet through windows cut in the shoes. Kinematic data were sampled at 120 Hz.
2.5. Statistics Statistical tests were carried out to compare the mean stance phase coordination variability between groups for each of the four coupling angle comparisons of interest. In accordance with the hypotheses that coordination variability would be different between 1) uninjured runners and those with ITBS and 2) the beginning and end of the run, coordination variability was compared by group (uninjured vs. ITBS) and across time (beginning vs. end of run) using 2-way ANOVAs with time as a within-subjects variable. If significant interactions were found, paired t-tests were used to examine main effects within the interaction. As it was discovered post-hoc that ITBS runners had varied pain responses to the run to exertion, exploratory statistics were 74
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course of a run to exertion. Contrary to our hypotheses, there were no significant differences in segment coordination variability between ITBS and uninjured runners and for the most part runners with ITBS did not respond differently to the run to exertion compared to uninjured runners. One exception was the thigh vs. shank sagittal plane couple where a trend for a significant time by group interaction was found. Post-hoc simple main effects test of time found no significant change in coordination variability over time for either group. In our exploration of the impact of pain induced by a run to exertion, we did not observe significant differences in the magnitude of change in segment coordination variability between groups (uninjured, ITBS with no pain, ITBS with pain). To date, few studies have examined the effect of a run to high exertion on coordination variability in runners with ITBS (Miller et al., 2008). In their work, Miller and colleagues examined coordination variability assessed by continuous relative phase (CRP) over the course of a treadmill run in uninjured runners and runners with a history of ITBS (Miller et al., 2008). Similar to our findings, the authors reported no significant interactions between group and time with respect to coordination variability. While Miller et al. employed a different variability measure, together, our findings suggest that runners with a history of, or currently symptomatic ITBS, do not respond differently to exertion than do their healthy counterparts in these measures of variability. In addition to testing for an interaction between group and time, we also examined for the main effects of group and/or time. Our study did not show a main effect of group. At the start of the run, without possible interaction of fatigue, runners with ITBS did not demonstrate any differences in coordination variability compared to the uninjured cohort. The lack of difference in coordination variability between injured and uninjured runners is in contrast to previous studies which observed lower coordination variability in injured runners (Heiderscheit et al., 2002; Seay et al., 2011). These studies examined segment coordination variability via a vector coding technique similar to the current study in runners with alternate diagnoses such as low back pain (Seay et al., 2011) or patellofemoral pain syndrome (Heiderscheit et al., 2002). The mechanism of injury and kinematic variables of interest for these diagnoses are unique to that of the patient with ITBS and therefore may need to be considered independently of our work. In work by Miller and colleagues, the authors did report less CRP coordination variability with respect to some couplings and greater variability with respect to others in runners with a history of ITBS as compared to uninjured runners (Miller et al., 2008). In contrast, Hein and colleagues present similar findings to ours with respect to ITBS injury status when examining CRP coordination variability whereby no significant between-group differences were noted (Hein et al., 2012). It is important to note that measures of coordination variability may differ when calculated using modified vector coding or CRP methods (DeLeo et al., 2004; Miller et al., 2010). Thus, the impact of injury on coordination variability remains unclear. In patients with ITBS, endurance, as tested by the ability to maintain kinematic patterns in a setting of fatigue, is often considered a critical
Table 1 Participant characteristics. Pain was assessed using a 0–10 verbal numerical rating scale.
N Age (years) Height (m) Body mass (kg) Run speed (m/s) Run duration (min) Change in pain
Uninjured
ITBS
Mean
SD
Mean
13 30.23 1.63 56.22 3.33 25.15
7.01 0.11 5.74 0.15 6.54
12 32.67 1.70 60.36 3.01 25.25
ITBS pain
ITBS no pain
SD
Mean
SD
Mean
SD
7.73 0.06 5.37 0.35 8.34
5 33.20 1.68 59.50 3.10 22.80 4.80
4.76 0.06 4.06 0.45 5.45 1.25
6 33.50 1.72 61.43 2.88 27.00 0.67
10.01 0.05 6.87 0.26 10.90 0.61
performed to examine the effect of pain on coordination variability. 1way ANOVAs were used to compare the change in coordination variability between uninjured runners, ITBS runners who had an increase in pain during the run, and ITBS runners who did not have an increase in pain during the run. Significance was set at P < 0.05 for all comparisons with a trend operationally defined as P < 0.10. Where significant main effects were found, post-hoc comparisons were made using Tukey's test. 3. Results Participants who completed the protocol included 13 uninjured runners and 12 runners with iliotibial band syndrome. Average run duration for the entire cohort was 25.13 min. Run duration was not significantly different between uninjured runners and ITBS runners or between pain and no pain ITBS groups (Table 1). Participant characteristics are detailed in Table 1. Over the course of the run, 5 runners with iliotibial band syndrome developed clinically significant pain and 6 did not (pain data were incomplete for one runner). Two ITBS runners discontinued the run due to pain (vNRS ≥ 6) at an RPE of 15. When comparing uninjured and injured runners as well as the beginning and the end of the run, there were no significant differences by group or by time in any segment couples (Table 2). At the sagittal thigh vs. sagittal shank rotation couple there was a trend towards a significant group by time interaction (P = 0.06) where uninjured runners had a decrease and runners with iliotibial band syndrome had an increase in coordination variability from the beginning to the end of the run. This pattern, while not significant, also appeared in the frontal pelvis vs. thigh frontal rotation couple as well as the sagittal thigh vs. transverse shank rotation couples (Fig. 1). The comparison of the change in coordination variability across uninjured, ITBS with pain, and ITBS without pain revealed no significant differences between groups (Fig. 2, Table 3). 4. Discussion The purpose of this study was to determine if symptomatic runners with ITBS display different segment coordination variability compared to uninjured runners and if this difference is exacerbated over the
Table 2 Average stance phase coordination variability at the beginning and end of a run to exertion in uninjured runners and those with iliotibial band syndrome for four segment couples of interest. Uninjured
ITBS
Beginning
Pelvis frontal vs. thigh frontal (°) Thigh sagittal vs. shank sagittal (°) Thigh sagittal vs. shank transverse (°) Shank transverse vs. rearfoot frontal (°)
End
P-value
Beginning
End
Mean
SD
Mean
SD
Mean
SD
Mean
SD
13.37 2.85 6.93 11.61
7.54 1.18 2.80 3.53
11.29 2.52 6.45 11.00
4.19 0.61 1.91 4.06
12.90 2.82 7.50 13.39
4.46 0.51 2.40 4.19
14.13 3.43 7.82 11.91
6.92 1.45 2.66 2.72
75
Group
Time
Group × time
0.55 0.19 0.25 0.32
0.76 0.59 0.89 0.12
0.24 0.06 0.46 0.51
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Thigh sagittal vs. Shank sagittal 8
30
7
Coordination Variability (°)
Coordination Variability (°)
Pelvis frontal vs. Thigh frontal 35
25 20 15 10
6
Uninjured - beginning
5
Uninjured - end ITBS - beginning
4
ITBS - end 3 2
5
1
0
0
Thigh sagittal vs. Shank transverse
Shank transverse vs. Rearfoot frontal 25
16
Coordination Variability (°)
Coordination Variability (°)
14 12 10 8 6 4
20
15
10
5
2 0
0
Fig. 1. Coordination variability during stance at the beginning and end of the run for uninjured runners and runners with iliotibial band syndrome. Dark horizontal lines indicate group mean, grey horizontal lines indicate ± SD. Values detailed in Table 2.
this study do not refute this point nor suggest that exertion does not play a critical role in running injuries. Rather, our results suggest that any increased susceptibility to running injury during high exertion is not likely due to alterations in coordination variability. The lack of significant differences by group or time of run could
component of a rehabilitation program. When examining the main effect of time on coordination variability, our results suggest that a run to exertion does not affect coordination variability. There are several studies suggesting that fatigue may relate to running injuries (Dierks et al., 2010; Meardon et al., 2011; Voloshin et al., 1998). The results of
Thigh Sagittal vs. Shank sagittal 4
10
3
Coordination Variability (°)
Coordination Variability (°)
Pelvis frontal vs. Thigh frontal 15
5 0 -5 -10 -15 -20
2 1
-30
-4
Shank transverse vs. Rearfoot frontal 8
6
6
-2 -4
Coordination Variability (°)
Coordination Variability (°)
Thigh Sagittal vs. Shank transverse 8
0
ITBS - Pain
-2 -3
2
ITBS - No Pain
-1
-25
4
Uninjured
0
4 2 0 -2 -4 -6 -8
-6
-10
-8
-12
Fig. 2. Change in coordination variability during stance from beginning to end of run in uninjured runners, runners with iliotibial band syndrome who experienced pain in response to the run, and runners with iliotibial band syndrome who did not experience pain in response to the run. Dark horizontal lines indicate group mean, grey horizontal lines indicate ± SD. Values detailed in Table 3.
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Conflict of interest
Table 3 Change in average stance phase coordination variability in response to a run to exertion in uninjured runners and runners who did not or did experience pain during the run. Pvalues are reported for the comparison across all three groups. As there were no significant group differences, no post-hoc comparisons were made.
The authors declare no conflicts of interest. Acknowledgements
Pelvis frontal vs. thigh frontal (°) Thigh sagittal vs. shank sagittal (°) Thigh sagittal vs. shank transverse (°) Shank transverse vs. rearfoot frontal (°)
Uninjured
ITBS pain
ITBS no pain
Mean
SD
Mean
SD
Mean
SD
P-value
− 2.09
7.33
3.96
6.92
0.30
6.98
0.29
The authors wish to thank Dr. Howard Hillstrom and the Leon Root, MD Motion Analysis Laboratory at the Hospital for Special Surgery for support during the collection of data for this study.
− 0.34
0.97
1.04
2.11
0.36
0.72
0.11
References
− 0.48
1.85
0.14
4.13
0.86
3.24
0.62
− 0.61
1.89
−2.12
4.63
− 0.74
4.53
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potentially be explained by the fact that our injured group may actually have been made up of two subsets of runners: those who experienced pain and those who did not during their run to exertion. There may be a differential impact of injury and injury symptoms on coordination variability. The majority of studies reporting decreased coordination variability in ITBS compared to uninjured runners have examined an injured population that is not in pain (MacLean et al., 2010; Miller et al., 2008). Runners with currently symptomatic patellofemoral pain have displayed decreased coordination variability in comparison to uninjured runners in some studies (Hamill et al., 1999; Heiderscheit et al., 2002), while at least one study showed that runners with symptomatic patellofemoral pain had greater coordination variability in comparison to uninjured runners (Cunningham et al., 2014). We found there were no differences in the change in coordination variability by pain level. In the current study, it is evident that within the ITBS pain and ITBS no pain groups there was substantial inter-participant variation in response to the run to exertion (Fig. 2). Future studies should further examine the interaction between pain and coordination variability during a run to high exertion or fatigue. Nevertheless, when looking across a sample of runners who currently have ITBS, there does not appear to be a difference in coordination variability, nor does exertion affect them differently from healthy runners. In addition to the small sample size in the ITBS pain and ITBS no pain groups, the current study has a few limitations. First, data were collected as participants ran on a treadmill and coordination variability may differ between treadmill and overground running. The impact of this limitation on the findings of this study is likely minimal as all participants were exposed to the same running conditions and so any difference from overground running would be systematic. Additionally the use of treadmills in the study of running gait, especially for methods requiring at least 10 strides of input data, is increasingly common. Finally, while participants ran until they reached a standard level of subjective fatigue and the length of this run was not different between groups, it is possible that an objective measure of fatigue (e.g., change in muscle power) would reveal that not all participants were fatigued to the same extent.
5. Conclusions The results of this study suggest that segment coordination variability does not change from the beginning to the end of a run to exertion in either uninjured runners or runners who currently have ITBS. This finding indicates that, while joint kinematics or kinetics may change, runners do not constrain the patterns of segment motion they use in response to exertion. Additionally, it appears that the absence or occurrence of pain during a run does not result in a differential change in coordination variability. 77
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