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Low back pain affects trunk as well as lower limb movements during walking and running Roy Müller, Thomas Ertelt, Reinhard Blickhan

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Accepted date: 30 January 2015 Cite this article as: Roy Müller, Thomas Ertelt, Reinhard Blickhan, Low back pain affects trunk as well as lower limb movements during walking and running, Journal of Biomechanics, http://dx.doi.org/10.1016/j.jbiomech.2015.01.042 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Title Low back pain affects trunk as well as lower limb movements during walking and running

Authors Roy Müller a,*, Thomas Ertelt b, Reinhard Blickhan a

a

Motionscience, Institute of Sport Sciences, Friedrich-Schiller University Jena, Seidelstraße

20, 07749 Jena, Germany b

Hochschule für Gesundheit und Sport, Technik und Kunst, Vulkanstraße 1, 10367 Berlin,

Germany

Corresponding Author *Phone: +49 3641 945724, Fax: +49 3641 945702 Email: [email protected]

1

Abstract Up to now, most gait analyses on low back pain concentrate on changes in trunk coordination during walking on a treadmill. Locomotion on uneven ground as well as lower limb changes receives little attention in association with low back pain. The present study focuses on how chronic non-specific low back pain causes modifications in lower limb and trunk movements, in level and uneven walking and running. We found that trunk as well as lower limb movement was influenced by chronic non-specific low back pain. A consistent finding across all gaits and ground level changes is that patients with chronic non-specific low back pain show less pelvis and unchanged thorax rotation as compared to healthy controls. Furthermore, in chronic non-specific low back pain patients the trunk rotation decreased only during level and uneven running whereas the sagittal trunk inclination at touchdown increased only during uneven walking as compared to healthy controls. Besides significant changes in the upper body, in chronic non-specific low back pain patients the knee joint angle at touchdown was more extended during level walking but also during uneven walking and running as compared to healthy controls. We assume that trunk movements interact with lower limb movements or vice versa. Therefore, we recommend that further investigations on low back pain should consider both trunk (primarily pelvis) and lower limb (primarily knee) movements.

Keywords: Low back pain, Gait, Posture, Uneven ground

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7

1. Introduction Low back pain (LBP) is often accompanied by changes in gait (Keefe & Hill, 1985; Lamoth, Meijer, et al., 2002; Spenkelink et al., 2002; van der Hulst et al., 2010). A consistent finding is that people with LBP tend to walk slower than healthy control subjects. It is suggested that slower walking reflects the presence of pain and/ or avoidance behaviour associated with pain. At lower walking speeds, in healthy subjects horizontal thorax and pelvis rotations are more or less in phase (synchronous pelvis and thorax rotation in the same direction), but at higher speeds, the phase difference increases and tends toward anti-phase (Bruijn et al., 2008; Lamoth, Beek, et al., 2002; Selles et al., 2001; Wu et al., 2014). Subjects with chronic LBP encounter problems in adjusting pelvis-thorax coordination and the thorax and pelvis move less out of phase at higher walking speeds (Lamoth et al., 2006; Lamoth, et al., 2002; Seay et al., 2011; van den Hoorn et al., 2012). Also, during running LBP patients showed more inphase coordination and reduced transverse plane coordination variability when compared to healthy subjects (Seay, et al., 2011). One interpretation of the reduced variability is that the trunk’s stiffness increased in LBP (van den Hoorn, et al., 2012). When avoiding unplanned movements between pelvis and thorax during walking, patients with chronic LBP alter trunk stiffness while increasing superficial lumbar muscle activity (van Dieen et al., 2003). More precisely, muscle activity of the M. erector spinae and M. rectus abdominis increase (Arendt-Nielsen et al., 1996; Lamoth, et al., 2006; Vogt et al., 2003) and the activity of the M. obliquus externus remains unchanged (van der Hulst, et al., 2010). These changes in muscle activity suggest increased stiffness. Stiffening of the trunk in healthy subjects (while contracting their abdominal muscles, or wearing an orthopaedic brace that limits trunk motions) led to similar changes in thoraxpelvis coordination as observed in LBP patients, but to different changes in pelvis-leg

1

coordination, with the pelvis remaining more out of phase with the legs (Wu, et al., 2014). These results may suggest that LBP patients do not simply stiffen their spine during gait. Until now, lower limb movements receive little attention in association with LBP. In healthy subjects, during slow walking hamstring activity at the end of the swing phase (before touchdown) decreased as walking speed decreased and the knees were significantly more extended at touchdown (Hanlon & Anderson, 2006; Murray et al., 1984). As mentioned previously, people with LBP tend to walk slower and thus, we assume with more extended knees and reduced hamstring activity at the instant of touchdown. Nevertheless, a more extended knee joint at touchdown leads to increased vertical forces and minor shockabsorption (Murray, et al., 1984; Podraza & White, 2010). Furthermore, patients with chronic LBP showed increased (and no decreased) hamstring activation at the end of the swing phase and in the early stance phase (Vogt, et al., 2003). However, until now it is not known how LBP influences lower limb movements. The available literature shows that chronic LBP primarily affects trunk movement during level walking. In daily living, frequently changes of level are necessary (such as when crossing a road and stepping on the sidewalk, mounting doorsteps entering stores, or climbing stairs). These situations require adaptations in muscle recruitment and more effort than level walking. To better understand how chronic LBP affects movement, we here investigate whether chronic non-specific LBP causes modifications in lower limb and trunk movements and how it influences the different strategies of locomotion on level and uneven ground. We hypothesized that CNLBP patients show lower limb and trunk movements that differ from healthy control subjects, in level and uneven walking and running.

2. Methods 2.1 Subjects

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Eleven patients with chronic non-specific low back pain (CNLBP) diagnosed by a physician and eleven healthy control participants took part in this study (Table 1). Both groups were gender, age, height and weight matched. Informed written consent was obtained from each volunteer. The experiment was approved by the local ethics committee (University of Jena, 2917-09/10) and in accordance to the Declaration of Helsinki.

Table 1

2.2 Measurements At the beginning of the investigation, CNLBP patients indicated their current level of low back pain on a visual analogue scale that ranged from “no pain” (0) to “maximum pain” (10). Afterwards, all subjects were instructed first to walk and second to run along a 17 m walkway with two consecutive force plates in its centre (Figure 1; the walkway was adapted to a previous study described in (Müller & Blickhan, 2010)). Subjects were allowed to choose their walking and running speed ad libitum but had to make sure that they moved naturally with constant speed and centred their right foot on the first and left foot on the second force plate (1. and 2. contact; Figure 1). The ground reaction forces were sampled at 2000 Hz by using one variable-height force plate at the site of the first contact (9281B, Kistler, Winterthur, Switzerland) and one ground-level force plate at second contact (9287BA, Kistler). After walking and running on the unperturbed flat track, the setup was changed. The variable-height force plate at first contact was set up to an elevation of 10 cm and the subjects were instructed again first to walk and second to run along the uneven walkway (Figure 1). All subjects were visually aware of the walkway and had to accomplish at least five successful trials per experimental setup and gait. A trial was successful when the subjects centred both touchdowns on the corresponding force platforms without losing any reflective joint markers. The markers (19 mm) were placed on 3

the tip of the toe, lateral malleolus, epicondylus lateralis and trochanter major on both lower limbs as well as on acromion, L5 and C7 proc. spinosus. All trials were recorded with eight cameras (240 Hz) by a 3D infrared system (MCU 1000, Qualisys, Gothenburg, Sweden) and synchronized by using the trigger of the Kistler soft- and hardware.

Figure 1

2.3 Data processing Kinetic and kinematic data were analysed using custom written Matlab code (The Mathworks, Inc., Natick, MA, USA). For kinetic analysis the ground reaction force was normalized to subject body weight (bw). A vertical ground reaction force threshold of 0.02 bw was used to determine the instants of touchdown and take-off at first and second contact. The raw kinematic data were filtered with a third-order low-pass Butterworth filter at 50 Hz cut-off frequency (Müller & Blickhan, 2010). The main parameters used for the kinematic analysis in the transverse plane were the rotational amplitudes (calculated as max-min between 200 ms before touchdown and 100 ms after touchdown) of: thorax rotation (calculated as the rotation of the acromion markers, projected on the global transverse plane, around the vertical axis of C7 proc. spinosus), pelvis rotation (calculated as the rotation of the trochanter major markers, projected on the global transverse plane, around the vertical axis of L5), and trunk rotation (calculated by subtracting thorax rotation from pelvis rotation; described in (van den Hoorn, et al., 2012)). The main parameters in the sagittal plane were: trunk inclination at the instant of touchdown (the line joining the C7 proc. spinosus to the L5 with respect to the vertical) and inner angles at the knee and ankle joint at the instant of touchdown (Figure 1). Besides transverse plane and sagittal plan parameters we calculated speed of locomotion and step length (between first and second contact).

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2.4 Statistical analysis The results were expressed as mean ± standard deviation for healthy controls and CNLBP patients separated for gait type (walking, running), ground condition (level, uneven ground) and contact (first, second; SPSS 15.0; SPSS®, Chicago, IL, USA). To determine the influence of CNLBP, we used repeated measures ANCOVAs (univariate) with pain (controls, CNLBP) as factor and speed as covariate (separated for gait type, ground condition and contact). The significance level was set at p < .05.

3. Results A summary of the subject information confirmed that there was no statistical difference between the groups for sex, age, height, or weight. Furthermore, CNLBP patients reported a pain intensity of 1.9 ± 1.2 at the beginning of the experiment.

3.1 Speed of locomotion and step length During walking, CNLBP patients chose a 6.5% reduced preferred walking speed on level ground (p < 0.01) and a 6% reduced preferred walking speed on uneven ground (p < 0.01; Table 2). During running, speed did not differ significantly between healthy controls and CNLBP (Table 2). Compared to healthy controls, step length did not change in CNLBP patients, neither during walking nor during running (Table 2).

Table 2

3.2 Walking During walking on level ground, in CNLBP patients early peak ground reaction force (1.46bw ± 0.10bw)

decreased

significantly 5

as

compared

to

healthy

controls

(1.55bw ± 0.11bw). Additionally, kinematic differences were found in the pelvis rotation but also in the knee joint angle. As compared to healthy controls, the amplitude of pelvis rotation decreased significantly in CNLBP patients (Table 3, Figure 2). Furthermore, in CNLBP patients the knee joint angle at touchdown was significantly more extended than in healthy controls (Table 3, Figure 2). Kinematic differences between both groups with respect to thorax and trunk rotation, trunk inclination and ankle joint angle at touchdown were not found. During walking on uneven ground, in CNLBP patients early peak ground reaction force (1.25bw ± 0.14bw) at elevated first contact decreased significantly as compared to healthy controls (1.35bw ± 0.11bw). When stepping down, in CNLBP patients early peak ground reaction force at the lowered second contact (1.75bw ± 0.12bw) was significantly less as compared to the value observed in the healthy controls (1.85bw ± 0.16bw). Kinematic differences between the two groups were found in the pelvis rotation, in trunk inclination and in the knee joint angle. As observed during level walking, in CNLBP patients the amplitude of pelvis rotation decreased significantly as compared to healthy controls (Table 3). Furthermore, in CNLBP patients the knee joint at the lowered second contact was significantly more extended at touchdown as compared to the controls (Table 3). In contrast to level walking, the trunk inclination at touchdown increased significantly in CNLBP patients as compared to the healthy controls (Table 3). Kinematic differences with respect to thorax and trunk rotation and ankle joint angle at touchdown were not found.

Table 3

3.3 Running During running on level ground, the peak ground reaction force did not differ significantly between CNLBP patients (2.26bw ± 0.270bw) and healthy controls (2.34bw ± 0.27bw).

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Furthermore, in CNLBP patients we found no kinematic differences with respect to thorax rotation, trunk inclination and ankle and knee joint angle at touchdown as compared to healthy controls (Table 3, Figure 2). However, the amplitude of pelvis and trunk rotation decreased in CNLBP patients as compared to healthy controls (Table 3, Figure 2).

Figure 2

During running on uneven ground in CNLBP patients peak ground reaction force (1.73bw ± 0.31bw) at elevated first contact decreased significantly as compared to healthy controls (1.85bw ± 0.18bw). At the lowered second contact in CNLBP patients peak ground reaction force (2.43bw ± 0.25bw) decreased significantly as compared to healthy controls (2.58bw ± 0.23bw). Kinematic differences were found in the pelvis and trunk rotation but also in the knee joint angle. As observed during level running, the amplitude of pelvis and trunk rotation decreased significantly in CNLBP patients as compared to healthy controls (Table 3). Furthermore, in CNLBP patients the knee joint angle at the lowered second contact was significantly more extended (Table 3). Kinematic differences with respect to thorax rotation, trunk inclination and ankle joint angle at touchdown were not found.

4. Discussion CNLBP patients show lower limb and trunk movements that differ from healthy control subjects, in level and uneven walking and running (Table 3).

4.1 Trunk movements A consistent finding across all gaits and ground level changes is that CNLBP patients show less pelvis and unchanged thorax rotation. In more detail, in CNLBP patients the amplitude (Table 3) and the curve shape (Figure 2) of the thorax rotation angle is similar to that of 7

healthy controls, whereas the amplitude of the pelvis rotation (Table 3) was significantly decreased and the curve shape of the pelvis rotation was changed (Figure 2). This is in contrast to previous studies that found no significant differences in pelvis rotation amplitudes between LBP and control participants (Lamoth, et al., 2002; Seay, et al., 2011; van den Hoorn, et al., 2012) and could be attributed to the method used (walkway instead of treadmill, different marker sets to calculate rotational angles, and different samples; for more details see 4.3 Limitations of the study). Nevertheless, the pelvis seems to play an important role in discriminating CNLBP patients from healthy controls. In the case of level walking, to discriminate LBP patients from healthy subjects the trunk motion in the transverse plane plays a more important role than the motion in the sagittal plane (Lamoth, et al., 2002). This is in accordance with our results (Table 2). Compared to healthy controls, in CNLBP patients the transverse pelvis rotation decreased significantly and the sagittal trunk inclination at touchdown remained unchanged during level walking. The same applies to running on level ground with the difference that in CNLBP patients the transverse pelvis and trunk rotation decreased significantly as compared to healthy controls (Table 3). Nevertheless, during walking on uneven ground transverse pelvis rotation decreased and sagittal trunk inclination at touchdown increased in CNLBP patients (Table 3). This is supported by results in stair climbing (Lee et al., 2011). There, the authors show that the sagittal plane motions play a more important role in satisfying the biomechanical requirement of stair climbing as compared to level walking. We assume that a trunk-flexed posture restricts movements of pelvis (and trunk) rotation. However, compared to walking on uneven ground, during running on uneven ground, trunk inclination does not change significantly. In healthy subjects trunk-flexed postures may require compensatory changes in the lower limb kinematics to maintain balance during walking (Saha et al., 2008). During trunk-flexed walking, healthy subjects adopt a crouched gait pattern characterized by sustained knee 8

flexion (Saha, et al., 2008). This contradicts the kinematic changes observed in CNLBP patients during walking on uneven ground. Here, CNLBP patients showed a trunk-flexed posture and an extended knee joint angle at touchdown (Table 3). It seems that CNLBP patients differ from healthy controls in compensating trunk-flexed postures by changes in the lower limb kinematics. Since trunk and lower limbs are linked via the hip, it is necessary to consider the muscle activation of the hip extensors (especially M. gluteus maximus and the hamstrings) that have a key role in stabilizing and transferring forces to the hip joint (Snijders et al., 1993a, 1993b). In healthy subjects, hamstring activity (e.g. M. biceps femoris) at the end of the swing phase decreased and M. gluteus maximus activity began earlier in the swing phase as walking speed decreased (Murray, et al., 1984). Another study focussing on chronic low-back pain showed that at the end of the swing phase and in the early stance phase patients with chronic LBP activate the M. biceps femoris as well as M. gluteus maximus noticeably earlier and higher than healthy people (Vogt, et al., 2003). Thus, slow walking healthy subjects and patients with chronic LBP show similar adaptations in M. gluteus maximus activation but different adaptations in M. biceps femoris activation. It seems that altered trunk and lower limb coordination and the deviating M. biceps femoris activation are linked. CNLBP patients may have problems in adjusting M. biceps femoris activity with walking speed, thus supporting the assumption that the deviant activation of the M. biceps femoris may be related to altered trunk and lower limb coordination. But this is subject of future research.

4.2 Lower limb movements Increased hamstring (e.g. M. biceps femoris) activity at the end of the swing phase and in the early stance phase during walking indicated a more flexed knee joint angle at touchdown. This contradicts the kinematic changes observed in CNLBP patients. Compared to healthy subjects, the only observable difference in the lower limb kinematics of CNLBP patients was 9

found in the knee joint angle. In CNLBP patients the knee joint angle was more extended at touchdown during walking across level and uneven ground (Table 3, Figure 2). While running, in CNLBP patients the knee joint angle was more extended solely on uneven ground as compared to the controls (Table 3). The ankle joint angle did not differ significantly between CNLBP patients and healthy controls, neither during walking nor during running. We found that people with CNLBP prefer to walk slower than healthy controls (Table 2). This result is in accordance with previous studies on LBP and walking (Keefe & Hill, 1985; Lamoth, et al., 2002; Spenkelink, et al., 2002; van der Hulst, et al., 2010). In healthy subjects, lower limb kinematics is significantly influenced by walking speed (Hanlon & Anderson, 2006; Lelas et al., 2003; Murray, et al., 1984). As walking speed increased, in healthy subjects the knee was in progressively more flexion at touchdown and during early stance. It has been suggested that this could be due to the need for greater shock-absorption at faster walking speeds (Murray, et al., 1984). Inversely, during slow walking the knees were more extended at the instant of touchdown. As compared to healthy controls, in CNLBP patients the knee joint angle at touchdown was significantly more extended and our covariate analysis shows that this was not due to walking speed (Table 3, Figure 2). A more extended knee at touchdown and an unchanged step length results in a significantly increased vertical force in healthy subjects (Podraza & White, 2010). Despite more extended knees we found that in CNLBP patients the early peak ground reaction force decreased significantly as compared to healthy controls. It seems, when CNLBP patients walk with extended knees in general (may be caused by pain-induced earlier onset and/ or higher muscle activation) they may slow down their speed of locomotion to compensate increased forces introduced by an extended knee joint at touchdown.

4.3 Limitations of the study

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Some limitations of the present study require consideration. First, the number of participants in this study was relatively small. However, significant differences were found between CNLBP patients and matched healthy controls, which highlights that the study had sufficient power to detect differences. Based on gait analysis, further investigations (maybe embedded in a clinical environment) could provide a basis to discriminate CNLBP patients from healthy subjects. Second, the setup of the experiment (first: level walking, second: level running, third: uneven walking, fourth: uneven running) was fixed and not randomized. Hence, order effects cannot be avoided. Third, to simulate uneven ground we had to use an instrumented walkway including a 10 cm elevated step. In contrast to walking and running on a treadmill, participants were able to choose different speeds of locomotion. Thus, when considering the influence of pain the covariance with respect to speed was considered. However, future investigations should separate the influence of speed and pain by using a suitable protocol. Fourth, on the basis of a limited marker set we used the trochanter major markers (placed on both legs) to calculate pelvis angles around the vertical axis of L5. Thus, pelvis rotation was affected by leg movements. This could be the reason why our pelvis angles seem to be way larger than in literature. To exclude this influence it would have been better to place the markers on spina iliaca. The same applies to the thorax rotations that were calculated by the acromion markers around the vertical axis of C7 proc. spinosus.

Acknowledgements We like to thank Olga Schröder (Department of Biological and Clinical Physiology, FSU Jena) for contacting the investigated patients, to our project partners for stimulating discussions and Denise Lauenroth-Ertelt and Isabel Kolkka for proof reading the manuscript. This project has been supported by the Federal Ministry of Education and Research (BMBF; 01EC1003B).

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Conflict of interest statement The authors declare that no financial and personal relationships with other people or organizations have inappropriately influenced the content of the work reported in this paper.

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Figure Legends

Figure legends

Figure 1 Side view of the instrumented walkway with two consecutive force plates in its centre. The first force plate (1.contact) was set at two different elevations: 0 cm (level ground) and 10 cm (uneven ground). In the sagittal plane, we calculated the trunk inclination with respect to the vertical (γ) and the inner angles at the knee (β) and ankle joints (α). The figure exemplifies walking across uneven ground.

Figure 2 Transverse trunk rotation (above) and sagittal knee joint angles during 100 ms precontact and stance phase while walking (left) and running (right) on level ground. The beginning of the ground contact is marked by the vertical line. Above: the bold (black) lines (solid: trunk, dashed: thorax, dotted: pelvis) represent the mean rotation angles of healthy controls and the grey shaded area the corresponding standard deviation; thin (red) lines represent the mean rotation angles of CNLBP. Below: bold (black) lines represent the mean sagittal knee joint angle of healthy controls and the grey shaded area the corresponding standard deviation; thin (red) lines represent the mean sagittal knee joint angle of CNLBP.

Figure1

Figure 1

Figure2

Figure 2

level walking

level running

trunk rotation [deg]

Figure2_trunklevelwalking

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trunk rotation [deg]

Figure2_trunklevelrunning

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Figure2_kneelevelrunning

knee angle [deg]

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Figure2_kneelevelwalking

knee angle [deg]

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Low back pain affects trunk as well as lower limb movements during walking and running.

Up to now, most gait analyses on low back pain concentrate on changes in trunk coordination during walking on a treadmill. Locomotion on uneven ground...
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