Clinical Biomechanics
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1 Clinical Biomechanics 27 (212) Contents lists available at SciVerse ScienceDirect Clinical Biomechanics journal homepage: Altered muscle recruitment during extension from trunk flexion in low back pain developers Erika Nelson-Wong a,, Brendan Alex b, David Csepe b, Denver Lancaster b, Jack P. Callaghan c a Regis University School of Physical Therapy, 3333 Regis Blvd, G4, Denver, CO 8221, USA b Regis University, School of Physical Therapy, Denver, CO, USA c University of Waterloo, Faculty of Applied Health Sciences, Waterloo, Ontario, Canada article info abstract Article history: Received 18 May 212 Accepted 1 July 212 Keywords: Muscle activation Electromyography Low back pain Risk identification Neuromuscular control Standing Trunk flexion extension Background: A functionally induced, transient low back pain model consisting of exposure to prolonged standing has been used to elucidate baseline neuromuscular differences between previously asymptomatic individuals classified as pain developers and non-pain developers based on their pain response during a standing exposure. Previous findings have included differences in frontal plane lumbopelvic control and altered movement strategies that are present prior to pain development. Control strategies during sagittal plane movement have not been previously investigated in this sample. The purpose of this research was to investigate neuromuscular control differences during the extension phase from trunk flexion between pain developers and non-pain developers. Methods: Continuous electromyography and kinematic data were collected during standing trunk flexion and extension on 43 participants (22 male) with an age range of years, prior to entering into the prolonged standing exposure. Participants were classified as pain developer/non-pain developer by their pain response ( 1 mm increase on a 1 mm visual analog scale) during standing. Relative timing and sequencing data between muscle pairs were calculated through cross-correlation analyses, and evaluated by group and gender. Findings: Pain developers demonstrated a top-down muscle recruitment strategy with lumbar extensors activated prior to gluteus maximus, while non-pain developers demonstrated a typical bottom-up muscle recruitment strategy with gluteus maximus activated prior to lumbar extensors. Interpretation: Individuals predisposed to low back pain development during standing exhibited altered neuromuscular strategies prior to pain development. These findings may help to characterize biomechanical movement profiles that could be important for early identification of people at risk for low back pain. 212 Elsevier Ltd. All rights reserved. 1. Introduction Eighty percent of all individuals will suffer from low back pain (LBP) at some point in their life-time (Wong and Lee, 24). In 85% of LBP cases, there is no clear injury mechanism that can be identified as the source for the disorder, and these cases are typically referred to as non-specific (Waddell, 24). Multiple case control studies have discovered neuromuscular differences between individuals with and without non-specific LBP(Brumagne et al., 28; Esola et al., 1996; van Dieen et al., 23). One functional movement that has been commonly investigated in case control studies is trunk flexion and extension performed while standing. Altered relaxation responses of the extensor musculature have been observed in people with LBP (Alschuler et al., 29) as well as differences in muscle recruitment strategy and trunk/hip kinematics during performance of the movement (Esola et al., 1996; Wong and Lee, 24). The typical activation order for extensor muscle recruitment during the extension phase of a standing flexion task occurs in a Corresponding author. address: enelsonw@regis.edu (E. Nelson-Wong). caudal to cephalic sequence in healthy control subjects (McGorry et al., 21). Mcclure et al. (1997) described the typical movement pattern during extension from trunk flexion as being dominated by hip movement during the first 75% of the motion in healthy individuals. A movement pattern where a greater percentage of the extension motion originates from the lumbar spine than from the hip is considered a spine dominant strategy. Previous investigations have found that subjects with LBP demonstrated a spine dominant strategy compared with healthy controls (Esola et al., 1996) and premature activation of lumbar paraspinals during the extension phase of the movement (Wong and Lee, 24). While it has been accepted that differences exist between people with and without LBP, less well established is whether neuromuscular differences are present prior to the LBP condition and are perhaps contributory factors to LBP development. A functional standing model has been successfully used to induce transient LBP in previously asymptomatic individuals (Gallagher et al., in press; Gregory and Callaghan, 28; Marshall et al., 211; Nelson-Wong and Callaghan, 21b). The model allows for characterization of differences between LBP developers () and non-developers (N), prior to pain development, as only a percentage (4 6%) of people exposed to this protocol are found to /$ see front matter 212 Elsevier Ltd. All rights reserved.
2 E. Nelson-Wong et al. / Clinical Biomechanics 27 (212) develop LBP (Gregory and Callaghan, 28; Marshall et al., 211; Nelson-Wong and Callaghan, 21b). Using this model, alterations in neuromuscular control, particularly in the frontal plane of movement, have been identified in previously asymptomatic people who are classified as pain developers when exposed to prolonged standing (Nelson- Wong and Callaghan, 21b; Nelson-Wong et al., 28). In the sagittal plane, it was found that exhibited an increased relaxation response of the gluteal muscles during standing trunk flexion compared to N, although no differences were found in the lumbar extensor musculature (Nelson-Wong and Callaghan, 21b). While case control differences have been described in the literature (Esola et al., 1996; Wong and Lee, 24), timing and sequencing of extensor muscle activation during extension from trunk flexion were not characterized prior to LBP development in the aforementioned prolonged standing studies. Additionally, although the previous studies found no gender differences in pain reporting rates, gender differences were identified in postural control, neuromuscular strategies, and response to interventions (Gallagher et al., in press; Nelson-Wong and Callaghan, 21a, 21b, 21c). Movement strategy differences related to gender have also been identified in literature investigating knee mechanics and injury, where gender does appear to be a factor in injury rates (Beaulieu et al., 28; Joseph et al., 211). The purpose of the current study was to examine differences in neuromuscular strategies, assessed using recruitment timing between muscle pairs, during the extension phase following trunk flexion between individuals classified as and N with the induced LBP model. It was hypothesized that the and N groups would demonstrate differences in neuromuscular strategies during extension from trunk flexion, and that would demonstrate a more spine dominant strategy, similar to the pattern that has been observed in patients with LBP (Wong and Lee, 24). Although not a primary aim of this study, gender differences during the movement were also of interest, with the expectation that males and females would demonstrate different muscle recruitment strategies for the extension phase of trunk flexion. 2. Methods Experimental data were collected at the University of Waterloo and IRB approval was received through the University of Waterloo Office for Research Ethics. Data analysis for the current study took place at Regis University, and was determined to be exempt by the Regis University IRB. Forty-three participants (age range years old, 22 male) from the University of Waterloo and surrounding community volunteered for this study (Table 1). Participants were excluded from participation if they had any lifetime history of LBP that was severe enough to seek medical care or that required greater than 3 days off from work or school; prior hip or spine surgery; were unable to stand for greater than 4 hours; inability to complete questionnaires; or had been employed within the previous 12 months in an occupation requiring prolonged standing. Informed consent was obtained prior to participation. Detailed methods Table 1 There were no significant differences in age, Body Mass Index (BMI), or activity level, between /N groups. have been published previously, and readers are encouraged to refer to these earlier publications for complete data collection parameters and signal processing details (Nelson-Wong and Callaghan, 21b; Nelson-Wong et al., 21). In brief, participants completed several questionnaires to assess attitudes towards pain, injury and disability to determine if these were factors in their response to the pain inducing protocol. There were no group differences in the questionnaire responses and these findings have been published elsewhere (Nelson- Wong and Callaghan, 21b). Participants also completed a physical activity questionnaire, Minnesota Leisure Time Physical Activity Questionnaire (Folsom et al., 1986) for the 3 days prior to entrance into the study to determine equivalence in physical activity status at baseline. Continuous surface electromyography (EMG) data (AMT-8, Bortec, Calgary, Canada) were collected from bilateral thoracic erector spinae (TES), lumbar erector spinae (LES) and gluteus maximus (GMax) muscles (sampling frequency of 248 Hz). Kinematic data were simultaneously collected (sampling frequency of 32 Hz) with an OptoTrak Certus system (Northern Digital Instruments, Waterloo, Canada) to create an 8-segment (trunk, pelvis, bilateral thighs, shanks, and feet) rigid link model using Visual3D software (C-Motion, Inc., Germantown, MD) for calculation of relative joint angles, trunk velocity, and to track segmental movement. EMG data had high frequency and 6 Hz electrical noise components removed (bandpass filter 1 5 Hz, bandstop filter Hz) were full wave rectified and low pass filtered (zero phase lag, Butterworth filter with effective cutoff frequency of 2.5 Hz) and were normalized to maximal voluntary contractions to be expressed as %MVC (Nelson-Wong and Callaghan, 21b). Participants were asked to perform a series of self-paced movements, including standing trunk flexion, prior to entering into the 2-hour standing protocol. During the 2-hrs of standing, participants were asked to rate their LBP on a 1 mm Visual Analog Scale (VAS) with end point anchors of mm being no pain and 1 mm being worst pain ever experienced, every 15 min. All participants reported mm on the VAS upon entrance into the study. A threshold of 1 mm increase in LBP was used to categorize participants as or N (Nelson-Wong and Callaghan, 21b). The contributions to total trunk flexion range of motion from the hip (thigh relative to pelvis segment) and lumbar spine (trunk relative to pelvis segment) at terminal flexion were calculated by subtracting the neutral standing angle from the maximum angle at terminal flexion. The ratio of lumbar motion to hip motion was then calculated for terminal flexion. The extension phase of each trunk flexion trial was isolated using the kinematic data (trunk angle calculated as thorax relative to pelvis) to determine the instant of terminal flexion, and the frame numbers extracted to determine the appropriate window for the EMG data. Angular velocity of the trunk segment was also calculated for the extension phase of each trunk flexion trial. Cross-correlation was then used to determine relative phase relationships between activation of muscle pairs and muscle activation relative to pelvis position during extension from trunk flexion. Using cross-correlation (Eq. (1)), spatial and temporal similarity can be determined between two time-varying signals, x(t) and y(t). In brief, one signal, x(t), is held stationary while the second signal, y(t), is time-shifted incrementally forwards and backwards over the total length of the record N, with a spatial correlation, R xy, calculated at each time shift, τ, to create a cross-correlation function, R xy (τ).thevalueforτ at the point of maximum spatial correlation can be considered to be the phase lag between the two signals (Nelson-Wong et al., 29). Group N Independent t-test P-value Age (years) N (.61) (.91) BMI (kg/m 2 ) N (.64) (.8) Activity Level (MPAQ Score) N (7733) (8938) MPAQ=Minnesota Leisure Time Physical Activity Questionnaire. R xy ðτþ ¼ X N 1 N X N 1 N ðx i x ðx i x Þ 2XN Þ y iþτ y ðy i y Þ 2 ð1þ
3 996 E. Nelson-Wong et al. / Clinical Biomechanics 27 (212) For this study, the following cross-correlations were performed to provide relative sequencing/timing information between two signals, using custom software written in Matlab version 211b (MathWorks, Natick, MA) for both right and left sides: TES-LES (right and left), TES-GMax (right and left), LES-GMax (right and left), LES-Pelvis position (right and left), and GMax-Pelvis position (right and left). Phase lags, τ, at maximum R xy for each of these 1 pairs were extracted and recorded. As a data reduction measure, paired t-tests were used to determine symmetry between left and right phase lags, with p.5 (no significant differences between sides) indicating symmetrical muscle activation. When left/right symmetry was determined, an average value was taken for left/right phase lags, leaving 5 variables for the analysis. Independent t-tests were conducted on age, Body Mass Index (BMI), and physical activity data to ensure the /N groups were equivalent in those factors. To determine differences in neuromuscular strategy, lumbar/hip ratios at terminal flexion, trunk velocities and phase lags were entered into two-way ANOVAs with between factors of /N group and gender with a significance criterion of α.5. SPSS Version 19. (IBM, Armonk, NY) was used for all statistical analysis. 3. Results Seventeen of the 43 participants (4%) were classified as with an average increase in LBP VAS of 22.7 (±2.91) mm versus 1.37 (±.45) mm for N (Fig. 1). Seven of the 17 and 15 of the 26 N were male. and N participants were found to be equivalent on age, BMI and physical activity level at baseline (Table 1). Because left/right comparisons yielded no significant differences in muscle activation timing, symmetry was assumed. There were no significant main effects of /N group or gender, and no interactions found for trunk velocities during the extension phase of return to stand from flexion. There were also no significant main effects or interactions found for phase lags between muscle activation and pelvis movement. There was no significant /N group by gender interaction for the muscle activation comparisons. A significant main effect of /N group (F 1,39 =5.22, p=.3) was found for the phase lag between LES and GMax muscle pairs. activated LES.39 (±.86) s prior to GMax while N activated GMax.196 (±.71) s prior to LES (Fig. 2). The other muscle pairs (TES-GMax, and TES-LES) showed a similar directionality, however these comparisons failed to reach statistical significance. Table 2 displays summary data for phase lags between muscle pairs by /N group. There was also a significant main effect of gender (F 1,39 =4.42, p =.4) for phase lag between the TES and GMax muscle pairs (Fig. 3), with males activating TES.85 (±.11) s prior to GMax and females activating GMax.123 (±.1) s prior to TES. While there were no differences between genders in total range of motion at terminal flexion, there was a main effect of gender for lumbar/hip ratio (F 1,38 =7.6,p=.9), hip (F 1,38 =4.9,p=.33) and lumbar (F 1,38 = 4.7, p=.36) range of motion, independent of /N group. Table 3 displays summary data for phase lags between muscle pairs and range of motion contributions by gender. 4. Discussion Findings from this study show a cephalic to caudal muscle activation strategy during extension from trunk flexion in individuals who developed pain during standing compared with individuals who did not, supporting the primary hypothesis that pain developers would utilize a spine dominant strategy during trunk extension. Gender differences were also found in lumbar/hip ratios and muscle activation sequencing during this sagittal plane movement, with females exhibiting a hip initiation strategy compared with males, although these differences were independent of /N group. The N group in this study demonstrated a typical activation order of caudal to cephalic sequence, similar to what has been described previously in healthy control subjects (McGorry et al., 21). In this study, individuals classified as demonstrated an atypical top-down recruitment strategy with lumbar extensors being activated prior to gluteal musculature compared to their N counterparts. This is of special interest as these subjects were not a clinical LBP sample, but did respond to an induced pain model with development of LBP. Furthermore, the altered muscle recruitment strategy was present prior to exposure to the pain inducing protocol, and subjects were painfree at the time they performed the standing trunk flexion trial. Movements were performed at a self-selected speed, however there were no significant differences between groups or genders in speed of movement, indicating the muscle activation differences were independent of movement pacing. Implications from these findings are that neuromuscular differences exist apriori between individuals who do and do not exhibit a LBP response to standing. These results support similar findings, published elsewhere, from these data that found altered muscle activation profiles during standing as well as an increased relaxation response of the gluteal muscles during terminal flexion in (Gallagher et al., in press; Nelson-Wong and Callaghan, 21b). The findings of delayed gluteal muscle activation during extension from trunk flexion, as well as increased relaxation of gluteal musculature during terminal flexion, in are consistent with previous studies that have proposed gluteal muscle inhibition exists in people with LBP (Bullock-Saxton et al., 1993) * p <.5 Visual Analog Scale (mm) NDP N Fig. 1. The standing protocol was successful at inducing low back pain in 4% of subjects, with pain developers () averaging 22.7 (±2.91) mm and non-pain developers (N) averaging 1.37 (±.45) mm on the VAS during 2-hours of standing exposure. Phase Lag (sec) TES-LES LES-GMax TES-GMax N Fig. 2. Pain developers () demonstrated reversed muscle recruitment strategies during extension (cephalic-caudal sequence). Non-pain developers (N) exhibited the typical caudal-cephalic sequence. Positive phase lag indicates the cephalic muscle of the pair activated first. (TES=thoracic erector spinae; LES=lumbar erector spinae; GMax=gluteus maximus).
4 E. Nelson-Wong et al. / Clinical Biomechanics 27 (212) Table 2 Phase lag between extensor muscle pairs during extension from trunk flexion. A positive value indicates the more cephalic muscle of the pair was activated first. Muscle Pair Phase lag (s) N Phase lag (s) P-value TES-LES.1 (.9).1 (.9).21 LES-GMax.4 (.9).2 (.7).3 a TES-GMax.11 (.13).1 (.1).8 a Significantly different P.5. N=non-pain developers; =pain developers; TES=thoracic erector spinae; LES=lumbar erector spinae; GMax=gluteus maximus. Published case control studies have investigated differences in recruitment strategy during standing trunk flexion and extension between LBP cases and healthy controls. Findings from this study on asymptomatic individuals are similar to reported reversals of activation order during extension (Wong and Lee, 24), and decreased gluteus maximus activation (Leinonen et al., 2) inpeoplewithlbp. Leinonen et al. (2) also found that patients with LBP responded to an exercise based intervention by demonstrating earlier activation of gluteus maximus during extension from trunk flexion, further suggesting that this is a normalized recruitment strategy. It appears that individuals with no prior history of LBP, who responded to prolonged standing with reports of LBP, demonstrated similarities in their biomechanical profiles to patients with LBP. This finding suggests that these altered strategies may be present before the development of the LBP disorder, and could be considered as a factor that might proveusefulinearlyidentification of people at risk for future LBP. Abnormal sequencing of trunk musculature may create alterations in biomechanical loading through the lumbar spine that may not otherwise have occurred with a caudal to cephalic activation sequence (Colloca and Hinrichs, 25). Early activation of lumbar paraspinals (or delayed activation of gluteal muscles), during extension from trunk flexion or a reversal of the normal pattern of sequencing may exacerbate maladaptive loading patterns in the lumbar spine and could potentially contribute to back pain. It is interesting that there were gender differences detected in TES-GMax timing during extension from trunk flexion. This could be due to anthropometric gender differences such as males carrying a greater percentage of their total body mass in their trunk leading to earlier activation of thoracic musculature. Hoffman et al. (212) recently described gender differences in relative hip and lumbar spine contribution to standing trunk flexion range of motion, with males having a greater percentage of the total motion originating from the lumbar spine and females having a greater contribution from the hip. Findings from the current study are similar, and this could explain the gender Phase Lag (sec) TES-LES LES-GMax TES-GMax Male Female * p <.5 Fig. 3. Males activated thoracic erector spinae (TES) prior to gluteus maximus (GMax) during extension. Females demonstrated the opposite recruitment order. Positive phase lag indicates the cephalic muscle of the pair activated first. (TES=thoracic erector spinae; LES=lumbar erector spinae; GMax=gluteus maximus). Table 3 Phase lags between extensor muscle pairs during extension from trunk flexion, and range of motion at terminal flexion by gender. Muscle pair differences in muscle activation timing that were observed. Females had a larger percentage of their total standing flexion arising from the hip, and also activated the hip musculature first during the extension back into standing. There were no gender differences in velocity of movement or in total range of motion, therefore the females in this study would have spent relatively more time moving at the hip while males would have spent relatively more time moving at the trunk, which is consistent with the muscle activation timing findings. There are some limitations to this study. The participants in this study were relatively young (18 33 years old) and therefore may not be representative of the clinical LBP population. Participants were allowed to move at a self-selected pace, which may have been a confounding factor, although there were no significant differences found in velocity of movement. The trunk was treated as a single rigid segment, which did not allow for a realistic representation of the lumbopelvic kinematics. The relationship between pain development during a bout of prolonged standing and future development of clinical LBP has not yet been determined and this is an area of ongoing research. 5. Conclusion In conclusion, previously asymptomatic individuals who developed LBP during exposure to a 2-hour standing protocol displayed altered neuromuscular strategies compared to individuals who did not develop LBP. Specifically, lumbar paraspinals were activated earlier than gluteus maximus in pain developers during extension from trunk flexion, which a reversal of the expected and typical activation sequence present in trunk extension from full standing flexion. Identification of predisposing factors for LBP development has the potential to aid health care professionals in early intervention and possibly prevention of LBP. Acknowledgments The authors would like to thank Regis University Sponsored Academic Projects Research Council for supporting this research. The original data collection was funded by the Natural Sciences and Engineering Research Council (NSERC) of Canada. Dr. Erika Nelson-Wong was supported by the Foundation for Physical Therapy through a Promotion of Doctoral Studies II Scholarship. Dr. Jack P. Callaghan is supported by a Canadian Research Chair in Spine Biomechanics and Injury Prevention. References Males (n=22) Females (n=21) P-value Phase lag (s) Phase lag (s) TES-LES.12 (.1).6 (.8).52 LES-GMax.13 (.8).8 (.8).916 TES-GMax.9 (.12).12 (.1).42 a Range of motion Flexion Flexion P-value Hip 6.4 (4.) 74.9 (4.2).33 a Lumbar 73. (1.8) 64.7 (2.9).36 a Ratio 1.33 (.47).95 (.4).9 a a Significantly different at P.5. TES=thoracic erector spinae; LES=lumbar erector spinae; GMax=gluteus maximus. A positive value indicates the more cephalic muscle in the pair was activated first for phase lag data. Alschuler, K.N.M.S., Neblett, R.L.P.C.B.-C., Wiggert, E.P.T., Haig, A.J.M.D., Geisser, M.E.P., 29. Flexion-relaxation and clinical features associated with chronic low back pain: a comparison of different methods of quantifying flexion-relaxation. Clin. J. Pain 25, Beaulieu, M.L., Lamontagne, M., Xu, L., 28. Gender differences in time-frequency EMG analysis of unanticipated cutting maneuvers. Med. Sci. Sports Exerc. 4,
5 998 E. Nelson-Wong et al. / Clinical Biomechanics 27 (212) Brumagne, S., Janssens, L., Janssens, E., Goddyn, L., 28. Altered postural control in anticipation of postural instability in persons with recurrent low back pain. Gait Posture 28, Bullock-Saxton, J., Janda, V., Bullock, M., Reflex activation of gluteal muscles in walking. An approach to restoration of muscle function for patients with low-back pain. Spine 18, Colloca, C., Hinrichs, R., 25. The biomechanical and clinical significance of the lumbar erector spinae flexion-relaxation phenomenon: a review of the literature. J. Manipulative Physiol. Ther. 28, Esola, M.A., Mcclure, P.W., Fitzgerald, G.K., Siegler, S., Analysis of lumbar spine and hip motion during forward bending in subjects with and without a history of low back pain. Spine 21, Folsom, A.R., Jacobs, D.R., Caspersen, C.J., Gomez-Marin, O., Knudsen, J., Test-retest reliability of the Minnesota Leisure Time Physical Activity Questionnaire. J. Chronic Dis. 39, Gallagher, K., Nelson-Wong, E., Callaghan, J.P., 211. Do individuals who develop transient low back pain exhibit different postural changes than non-pain developers during prolonged standing? Gait Posture 34 (4), Gregory, D.E., Callaghan, J.P., 28. Prolonged standing as a precursor for the development of low back discomfort: an investigation of possible mechanisms. Gait Posture 28, Hoffman, S.L., Johnson, M.B., Zou, D., Van Dillen, L.R., 212. Differences in end-range lumbar flexion during slumped sitting and forward bending between low back pain subgroups and genders. Man. Ther. 17, Joseph, M., Rahl, M., Sheehan, J., Macdougall, B., Horn, E., Denegar, C., et al., 211. Timing of lower extremity frontal plane motion differs between female and male athletes during a landing task. Am. J. Sports Med. 39, Leinonen, V., Kankaanpaa, M., Airaksinen, O., Hanninen, O., 2. Back and Hip Extensor Activities During Flexion/Extension: Effects of Low Back Pain and Rehabilitation. Arch. Phys. Med. Rehabil. 81, Marshall, P.W.M., Patel, H., Callaghan, J.P., 211. Gluteus medius strength, endurance, and co-activation in the development of low back pain during prolonged standing. Hum. Mov. Sci. 3, Mcclure, P.W., Esola, M., Schreier, R., Siegler, S., Kinematic analysis of lumbar and hip motion while rising from a forward, flexed position in patients with and without a history of low back pain. Spine 22, Mcgorry, R.W., Hsiang, S.M., Fathallah, F.A., Clancy, E.A., 21. Timing of Activation of the Erector Spinae and Hamstrings During a Trunk Flexion and Extension Task. Spine 26, Nelson-Wong, E., Callaghan, J.P., 21a. The impact of a sloped surface on low back pain during prolonged standing work: A biomechanical analysis. Appl. Ergon. 41, Nelson-Wong, E., Callaghan, J.P., 21b. Is muscle co-activation a predisposing factor for low back pain development during standing? A multifactorial approach for early identification of at-risk individuals. J. Electromyogr. Kinesiol. 2, Nelson-Wong, E., Callaghan, J.P., 21c. Changes in Muscle Activation Patterns and Subjective Low Back Pain Ratings During Prolonged Standing in Response to an Exercise Intervention. J. Electromyogr. Kinesiol. 2, Nelson-Wong, E., Gregory, D.E., Winter, D.A., Callaghan, J.P., 28. Gluteus medius muscle activation patterns as a predictor of low back pain during standing. Clin. Biomech. 23, Nelson-Wong, E., Howarth, S.J., Callaghan, J.P., 21. Acute Biomechanical Responses to a Prolonged Standing Exposure in a Simulated Occupational Setting. Ergonomics 53, Nelson-Wong, E., Howarth, S.J., Winter, D.A., Callaghan, J.P., 29. Application of Auto and Cross-correlation Analysis in Human Movement and Rehabilitation Research. J. Orthop. Sports Phys. Ther. 39, Van Dieen, J.H., Selen, L.P.J., Cholewicki, J., 23. Trunk muscle activation in low-back pain patients, an analysis of the literature. J. Electromyogr. Kinesiol. 13, Waddell, G., 24. The back pain revolution. Churchill Livingstone, Edinburgh; New York. Wong, T.K.T., Lee, R.Y.W., 24. Effects of low back pain on the relationship between the movements of the lumbar spine and hip. Hum. Mov. Sci. 23,
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