What factors can affect lumbopelvic flexion-extension motion in the sagittal plane?: A literature review

Human Movement Science 58 (2018) 205–218

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Human Movement Science journal homepage: www.elsevier.com/locate/humov

Full Length Article

What factors can affect lumbopelvic flexion-extension motion in the sagittal plane?: A literature review

T

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Magdalena Zawadkaa, , Maria Skublewska-Paszkowskab, Piotr Gawdac, Edyta Lukasikb, Jakub Smolkab, Miroslaw Jablonskid a

Faculty of Health Sciences, Medical University of Lublin, Jaczewskiego 8 Street, 20-090 Lublin, Poland Institute of Computer Science, Electrical Engineering and Computer Science Faculty, Lublin University of Technology, 20-618 Lublin, Nadbystrzycka 38D, Poland c Department of Rehabilitation and Physiotherapy, Chair of Rehabilitation, Physiotherapy and Balneotherapy, Faculty of Health Sciences, Medical University of Lublin, Magnoliowa 2 Street, 20-143 Lublin, Poland d Department of Rehabilitation and Orthopedics, Medical University of Lublin, Jaczewskiego 8 Street, 20-090 Lublin, Poland b

AR TI CLE I NF O

AB S T R A CT

Keywords: Lumbar spine Pelvic Coordination Lumbopelvic rhythm Narrative review

Clinicians use forward bending and backward return in routine clinical examinations for evaluating spine mobility. The magnitude and timing of lumbar spine and pelvic contributions have been described in the literature as lumbopelvic rhythm. There is still limited knowledge about the factors which can determinate lumbar and hip mobility and coordination in the sagittal plane. The aim of this study is to demonstrate those factors contributing to the lumbopelvic rhythm and to explain the differences observed between subjects. The studies included in the review present possible explanations of observed lumbar-pelvic motion and/or coordination. They measure movement of the lumbar spine, the pelvis and/or the hip in the sagittal plane. The search was conducted in August 2017. Two databases (PubMed and Web of Science) were searched. The search identified 126 potentially relevant articles (53 in PubMed, 73 in Web of Science). Initial screening based on titles and abstracts retrieved 35 articles. The second stage of selection involved reading the full texts of articles. Twenty-four papers were selected in this stage. After careful bibliographic study, seven papers were added for this review, resulting in a total of 31. This literature review demonstrates those factors contributing to lumbopelvic motion. Age and gender, hamstring muscle tightness, feet position, muscle fatigue, movement speed and external loading as well phase of motion can affect various aspects of lumbopelvic rhythm.

1. Introduction Trunk motion in the sagittal plane results from the motions of the spine and pelvis (Esola, McClure, Fitzgerald, & Siegler, 1996; Granata & Sanford, 2000). Clinicians use forward bending and backward return in routine clinical examinations for evaluating spine mobility (Esola et al., 1996; Shojaei, Vazirian, Salt, Van Dillen, & Bazrgari, 2017). The magnitude and timing of lumbar spine and pelvic contributions to trunk motion have been described in the rehabilitation, ergonomic and sport literature as lumbopelvic rhythm (LPR) (Laird, Gilbert, Kent, & Keating, 2014; Vazirian, Dillen, & Bazrgari, 2016; Zhou, Ning, Hu, & Dai, 2016). LPR is an organised pattern characterised by coordination of the lumbar spine and hip connected to the pelvis, especially during flexion and extension in the sagittal plane (Kim et al., 2013; Pries, Dreischarf, Bashkuev, Putzier, & Schmidt, 2015; Vazirian et al., 2016). In previous studies,

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Corresponding author. E-mail address: [email protected] (M. Zawadka).

https://doi.org/10.1016/j.humov.2018.02.008 Received 26 November 2017; Received in revised form 13 February 2018; Accepted 15 February 2018 0167-9457/ © 2018 Elsevier B.V. All rights reserved.

206

18

26

49

309

67

13

15

Iwasaki et al. (2014)

Kienbacher et al. (2015)

Pries et al. (2015)

Jandre Reis and Macedo (2015)

Hu and Ning (2015a)

Hu and Ning (2015b)

12

Kasahara et al. (2008)

Hasebe et al. (2014)

11

Maduri et al. (2008)

23

20

Pal et al. (2007)

Song and Qu (2014a)

33

Larivière et al. (2000)

8

18

Granata and Sanford (2000)

Tafazzol et al. (2014)

24

McClure et al. (1997)

16

41

Esola et al. (1996)

Kang et al. (2013)

39

Li et al. (1996)

12

30

Nelson et al. (1995)

Sorensen et al. (2011)

Sample size

Author (year)

0/15

0/13

26/41

175/134

25/24

10/16

0/18

13/10

0/8

0/16

0/12

0/12

4/7

0/20

0/33

5/13

Lack of information

14/27

22/17

30/0

Sex (Females/ Males)

Healthy

Healthy and LBP participants Healthy

Healthy

Healthy

Healthy

Healthy

Healthy

Healthy

Healthy

Heathy

Healthy

Healthy

Healthy and LBP participants Healthy

Healthy

Healthy and LBP participants Healthy and LBP participants

Healthy

Healthy

Characteristics of participants

3D magnetic field based motion tracking system, semg 3D magnetic field based motion tracking system, semg

Bending sensor segments and acceleration sensors Goniometer

3D accelerometers

Two flexible electrogoniometers and sEMG

Optoelectronic motion capture system and force plates Spinal mouse, three-dimensional system

Inertial tracking device

3D motion-capture system

Lumbar motion monitor, sEMG

Flexible electrogoniometer (egm) system

Electromagnetic motion analysis system

3D motion analysis system

Electromagnetic sensors and eigenvector model analyses Motion analysis system

3D optoelectric motion analysis system

3D optoelectric motion analysis system

3D Space tracker system, an electromagnetic tracking device 3D electromechanical digitiser

Measurement tool

Table 1 Summary of study characteristics of articles included in review (chronological by the year of publication).

Association of hamstring tightness and range of motion in anterior pelvic tilt, lumbar motion and trunk flexion during forward bending Lifting and lowering of a 20-lb box both before and after lumbar extensor muscle fatigue, generated through a static weight holding task Performing five repetitions of weightlifting tasks both before and after a lumbar extensor muscle fatiguing protocol (continued on next page)

Existence of a specific LPR during forward bending in relation to tight hamstrings Relationship between physical characteristics and the lumbar pelvic rhythm during stoop lifting. Changes of the lifting strategy caused by physical characteristics and variations in load. The sex and age related differences in the neuromuscular activation profiles of the lumbar extensors and the related spine and hip kinematics during trunk flexion–extension task Effects of age and gender on lordosis, sacrum orientation and LPR

Modification of the lumbar-pelvic rhythm in chronic low-back pain patients during lifting Describe and compare the initiation patterns, the relative contribution and peak angular displacement of the lumbar spine and hip region during flexion and return The range of lumbar curvature rotation examined at four torso inclination angles during lifting tasks Relationship of movement direction (in the ‘forward bending’ and ‘rising from a forward flexed position’ phases) on the lumbar spine and the pelvis in regard to lumbopelvic coordination in the sitting position Sagittally symmetric lifting and lowering task (10 kg load) under three stance width conditions: narrow (feet together), moderate (feet shoulder width) and wide (feet 150% of shoulder width) Effects of hamstring-stretching exercises on the kinematics of the lumbar spine and hip during stoop lifting Measure three-dimensional angular rotations of the pelvis and lumbar spine, measure sagittal coordination during forward flexion and backward extension Examine age-related biomechanical differences during asymmetric lifting.

Lumbar and pelvic motion as subjects lifted and lowered a 9.5 kg box with knees extended Effects of stretching on hamstring muscle length, standing lumbar lordosis, standing pelvic inclination, and the relative amount of lumbar and hip motion during trunk forward bending Amount and velocity of lumbar spine and hip motion during forward bending; passive leg raising and active knee extension tests Amount and pattern of lumbar spine and hip motion when rising from forward flexed position; determine if hamstrings length is related to the pattern of motion Influence of load and lifting velocity on LPR.

Aim of investigation

M. Zawadka et al.

Human Movement Science 58 (2018) 205–218

18

8 38

38

60

Zhou et al. (2016b)

Tojima et al. (2016) Shojaei, Vazirian, et al. (2017)

Shojaei, Salt, Hooker, Van Dillen, and Bazrgari (2017) Vazirian et al. (2017)

35

60

Lack of information Lack of information 0/35

13

Zhou et al. (2016a)

Vazirian, Shojaei, Agarwal, et al. (2017) Tsang et al. (2017)

38/0

12 10

Hasebe et al. (2016) Zhou et al. (2016a, 2016b)

0/8 38/0

0/18

0/13

0/12 0/10

30/30

60

Shojaei et al. (2016)

Sex (Females/ Males)

Sample size

Author (year)

Table 1 (continued)

Healthy and LBP participants

Healthy

Healthy and LBP participants Healthy

Healthy Healthy and LBP participants

Healthy

Healthy

Healthy Healthy

Healthy

Characteristics of participants

3D inertial sensor system

Magnetic inertial motion trackers

Wireless inertial measurement unit system Magnetic inertial motion trackers

Wireless inertial measurement units and force platform. Spinal mouse Magnetic field based 3D motion tracking system 3D magnetic field based motion tracking system 3D magnetic field based motion tracking system 3D motion analysis system Wireless inertial measurement unit system

Measurement tool

Investigate age-related differences in lower-back biomechanics during sagittally-symmetric simulated manual material handlingtasks. Influence of dynamic 6-week stretching of hamstrings on LPR. Effects of foot placement, especially stance width and foot angle on lumbopelvic coordinations when performing sagittal trunk flexion motions Comparing the lumbopelvic rhythms of trunk flexion and extension motion by quantifying lumbopelvic CRP and CRP variability Lumbopelvic CRP and CRP variability during a paced trunk flexion routine over time periods of 3, 7, 11 and 15 s. Lumbar and hip ROM and L/P ratio during trunk extension Investigate differences in timing and magnitude aspects of lumbo-pelvic coordination between patients with acute LBP and asymptomatic controls during forward bend-ing and backward return. Investigate lumbo-pelvic kinematics in individuals with and without acute LBP Age-related differences in the timing aspect the LPR was investigated using the continuous relative phase method. Age-related differences in lumbar contribution to the trunk motion in the sagittal plane Effects of different bending speeds on the kinematics and coordination of lumbopelvic movements during forward bending in people with and without chronic mechanical LBP

Aim of investigation

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various patterns of altered lumbopelvic rhythm have been reported in patients with low back pain (LBP) (Laird et al., 2014). However, the spine should not be considered in isolation from the lower limbs when trying to understand LBP causes. Movement in the hips, knees and ankles can give support for trunk movement and additional stability for moving the body’s center of gravity (Barwick, Smith, & Chuter, 2012; Cobb, Bazett-Jones, Joshi, Earl-Boehm, & James, 2014; Resende, Deluzio, Kirkwood, Hassan, & Fonseca, 2015; Svoboda, Janura, Kutilek, & Janurova, 2016). Clinical experience shows that patients with LBP often demonstrate a mal-alignment of the pelvis due to asymmetry in lower limb posture, restricted motion at the hip joint, weak gluteal muscles and transversus abdominis, but tight hamstring, psoas muscles and quadratus lumborum (McGregor & Hukins, 2009). The pelvis is a structure located between the hip joint and the lumbosacral spine. With the use of multiple muscles, the pelvis integrates the movements of the hip joint and other joints of the lower extremities and the lumbosacral region (Cho, 2015) (see Table 1). A large variety of measurement methods describing lumbopelvic motion needs a brief explanation of terms used in order to avoid confusion throughout the remaining part of this paper. The timing of lumbopelvic rhythm can be calculated by different methods: the critical points method where the time difference is calculated between different event times such as onset time or maximal velocity of lumbar and pelvic motion (Pal, Milosavljevic, Sole, & Johnson, 2007; Thomas & Gibson, 2007; Vazirian et al., 2016); the crosscorrelation method where lumbar and pelvic motion are cross-correlated by determining the time lag at which the absolute value of the correlation coefficient is maximal e.g. positive time lag implied that the lumbar spine moved earlier than the hip in the movement cycle (Wong & Lee, 2004); the continuous relative phase (CRP) – in this method a new signal is generated representing the difference in phase angles of the two original signals (Lamb & Stöckl, 2014). The relative phase measures the relationship between two joint or body segment angles to characterize inter-joint coordination patterns (Galgon & Shewokis, 2016). The mean absolute relative phase (MARP) and the deviation phase (DP) are single measures derived from continuous relative phase curves that can quantify coordination patterns and describe the stability of the patterns during functional movements. (Galgon & Shewokis, 2016). MARP values closer to zero represent a more ‘‘in-phase’’ lumbo-pelvic coordination (more synchronous movement of segments) where as values closer to π radians represent a more ‘‘out-of-phase’’ lumbo-pelvic coordination (less synchronous movement of segments). The smaller DP represents a lumbo-pelvic coordination with less trial-to-trial variability (more stable motion pattern) (Shojaei et al., 2017). The lumbar range of motion (ROM) is defined as the difference between the maximal and minimal angles reached during motion (Laird et al., 2014). The lumbar spine angle is defined as the motion determined by the angle between marker pairs (McClure, Esola, Schreier, & Siegler, 1997) or as the difference between thoracic and pelvic motion (Granata & Sanford, 2000; Shojaei, Vazirian, Croft, Nussbaum, & Bazrgari, 2016). The pelvic or hip ROM is defined as the motion determined by the angle formed between thigh and pelvis or between pelvis and a vertical line (Vazirian et al., 2016). The pelvic tilt is measured by a line drawn from the anterior to the posterior superior iliac spines with an angle formed relative to the horizontal plane; it may be also called the anterior tilt (when pelvis rotates forward) or the posterior tilt (when pelvis rotates backward) (Laird et al., 2014). The lumbopelvic ratio (L/P ratio) is subsequently calculated by dividing the total lumbar rotation (L) by the pelvis rotation (P) in the sagittal plane (Tafazzol, Arjmand, Shirazi-Adl, & Parnianpour, 2014). In the literature it is also called the ‘‘lumbar/hip ratio” (Esola et al., 1996) or ‘‘spine/hip ratio” (Thomas & Gibson, 2007). An indicator that compares lumbar and hip contributions to ROM is defined as the relative contribution of lumbar and pelvic motion to the trunk motion pattern. It is estimated by calculating the percentage contribution of lumbar ROM to peak trunk ROM (Laird, Kent, & Keating, 2016). Velocity or acceleration of movement is described by angular velocity (deg/s) and angular acceleration (change in the angular velocity over time) (Christian Larivière, Gagnon, & Loisel, 2002; Pal et al., 2007). Altered movement patterns of the spine and hip may be a potential factor contributing to the development of low back pain. Changes in the spine and hip’s range of motion and timing can alter the bending stresses of the lumbar segments (Shum, Crosbie, & Lee, 2007a). On the other hand, altered movement patterns of the spine and hip may be the consequence of low back pain. It may be a compensatory response to reduce pain or to protect injured tissues. The measurement methods and approaches used to characterise the timing and magnitude aspects of LPR differ across studies (Vazirian et al., 2016). Differences in measurement instruments or methods, biological differences, or errors in measurements may by causes of this variability (Laird et al., 2014). It remains unclear what factors determine the lumbar and hip range of motion and the LPR during the sagittal plane movement. Thus, the aim of this study is to demonstrate factors contributing to the lumbopelvic rhythm and to explain the differences observed between subjects. 2. Material and methods The studies included in this review had to present possible explanations of the observed lumbopelvic motion and/or coordination. They had to measure the movement of the lumbar spine and the pelvis and/or the hip in the sagittal plane. 2.1. Study selections: Inclusion and exclusion criteria This review included full-text original articles written only in English. The search was conducted in August 2017. Because there are many ways of describing lumbopelvic motion and many devices and methods are used to measure it, the inclusion criteria concerned: the use of non-invasive measurement systems like optic motion analysis systems, magnetic motion tracers, video analysis and others. No time filters were used to limit the search. Studies were examined to determine whether they met the following inclusion criteria: studies with healthy adult participants or both healthy participants and patients. In the study the papers presenting results concerning only patients were excluded. Patients examined in studies had to be defined as LBP patients with or without other symptoms (e.g. leg pain) but without division into subgroups and not after surgery. Motion should occur in the sagittal plane sitting position or the standing position (bending, lifting objects, squatting) but not during walking, running or rowing. Studies were excluded if they did not present factors determining the 208

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Fig. 1. Flowchart demonstrating the selection of articles through the review process.

observed lumbar, pelvic or hip motion in the sagittal plane but presented differences in motor patterns between subjects or utilized only EMG analysis. 2.2. Data sources Two databases (PubMed and Web of Science) were searched. In our experience PubMed and Web of Science are two of the largest and most used databases. They include only papers which were at least double-reviewed. The search criteria used are the same as those used in a similar review (Vazirian et al., 2016). Articles having the following keywords: ‘lumbopelvic rhythm’, ‘lumbar-pelvic rhythm’, ‘spino-pelvic rhythm’, ‘lumbopelvic coordination’, ‘lumbar-pelvic coordination’, and ‘spino-pelvic coordination’ were included in this review. Initial search results were further screened for the following inclusion criteria: original research using in vivo measurements – skin surface measurement techniques, reporting pelvic and spine motion in the sagittal plane and explaining the observed results. 3. Results The search identified 126 potentially relevant articles (53 in PubMed, 73 in Web of Science). Thirty-five duplicates (same articles found in both databases) have been removed. The selection of articles was in two stages. The first stage involved a brief analysis of the titles and abstracts of 91 papers, resulting in the selection of 35 papers. The second stage involved reading the full texts of articles. Eleven papers were excluded because they did not fulfill the assumed criteria. In four papers patients were divided into subgroups; in one the only participants were adolescents; in two the full texts were unavailable; two concerned only an EMG study without kinematic analysis; one study investigated only LBP patients. Finally 24 papers were chosen. Additionally, after careful bibliographic study, we added seven papers for this review, resulting in a total of 31. The whole review process is presented in Fig. 1. The n value indicates the number of papers. The studies included were grouped into the following categories:

• age and gender; • hamstrings muscles; • external load; • muscle fatigue; • feet position; 209

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• movement speed; • phase of movement (flexion/extension). 3.1. Age and gender Eight studies examined LPR in males and females of different ages. Individuals over 50 years of age, irrespective of gender or pace had smaller lumbar contribution than younger subjects. The lumbar contribution to trunk motion is smaller in females than males (Vazirian, Shojaei, Agarwal, & Bazrgari, 2017). Pries et al. also indicate that, with aging, the lumbar ROM decreased, whereas the pelvic range of flexion compensated for this effect and increased. The L/P ratio decreased with age from 0.80 to 0.65; however, this decrease was only significant in men (Pries et al., 2015). Further, a more in-phase and more stable lumbopelvic rhythm denoted respectively by smaller MARP and DP was observed in older versus younger individuals (Vazirian, Shojaei, & Bazrgari, 2017). Kienbacher et al. report that hip ROM from standing to the maximum flexion position is significantly lower in males than in females. Older males displayed significantly smaller gross trunk ROM from standing to maximum flexion than any other group. In contrast to Vazirian et al. findings, the relative contributions of the hips and the lumbar spine to gross trunk movement were similar in all groups of participants (Kienbacher et al., 2015). Shojaei et al. observed that contribution of lumbar spine to the total trunk motion during second and third quarters of both flexion and extension from flexed position was significantly larger in younger subjects (40–50 years old) than in older ones (50–60 or 60–70 years old). However, no age differences in MARP or DP were found in this investigation (Shojaei et al., 2017). The same author reports that pelvic ROM was significantly larger in older groups compared to younger ones and lumbar ROM was significantly smaller in older participants (Shojaei, Salt, Hooker, Van Dillen, & Bazrgari, 2017; Shojaei et al., 2016). Now Song’s and Qu’s study indicate, that older participants showed significantly decreased peak trunk flexion in both the lifting and deposit phases. The peak trunk angular velocities and accelerations in the sagittal plane in both the lifting and deposit phases were significantly smaller in older participants compared with younger ones (Song & Qu, 2014a). 3.2. Hamstring muscles Seven studies present the influence of hamstring muscles tightness on LPR. The straight leg rise test (SLR) angle and pelvic motion correlated strongly during the ending phase of forward bending. LPR comprises two patterns—lumbar dominant and pelvis dominant. In flexible subjects, the pelvis movement was dominant. These findings suggest that subjects without tight hamstrings have a high pelvic rotation angle (Hasebe et al., 2014). The LBP group investigated by Jandre and Macedo had a significantly smaller (p = 0.02 and p = 0.01 respectively) pelvic tilt (57.0°) and a total trunk flexion (82.2°) but a not significantly greater (p = 0.07) lumbar range of motion (79.8°) than controls (66.7°, 104.6° and 64.5°) (Jandre Reis & Macedo, 2015). Participants with LBP showed restriction in the pelvis and trunk flexion ROM, but had higher amplitudes in the lumbar spine during forward bending. However, lack of differences in the active knee extension test suggested that there is no difference between LBP and asymptomatic volunteers in hamstring tightness. Therefore, the authors indicate that hamstring tightness may have no influence on pelvic motion during forward bending in patients (Jandre Reis & Macedo, 2015). A positive correlation was observed between the sacral inclination angle and the hip flexion ROM during the SLR test. Iwasaki et al. found that a disorder of the LPR can be caused by both load and hamstring tightness (Iwasaki, Yokoyama, Kawabata, & Suzuki, 2014). A positive effect of stretching exercises on pelvic motion was observed during forward bending. Hasebe et al. investigated that, after 6 weeks of dynamic stretching, significant improvements were seen in the finger floor distance with maximum forward bending and in the SLR angle. Total pelvic rotation was also significantly increased in contrast to total lumbar flexion. A observed that L/P ratio was significantly decreased in the late phase of forward bending (Hasebe et al., 2016). Li et al. reported that SLR and hip motion during forward bending were significantly increased after hamstrings stretching. However, no changes occurred in lumbar motion during forward bending (Li, McClure, & Pratt, 1996). Kang et al., after hamstring-stretching exercises found not only a significant increase in hip flexion but also decreases in both lumbar flexion and the L/P ratio during the preparation phase of stoop lifting (Kang, Jung, An, Yoo, & Oh, 2013). However, McClure et al. reports that hamstrings length is not correlated to any kinematic variables of backward return from a flexed position but at the same time remarks that LBP patients had tighter hamstrings than healthy controls. Esola et al. found that total hip motion and total forward bending range were positively correlated to hamstrings flexibility in subjects with a history of LBP but not in healthy ones (Esola et al., 1996). 3.3. External load Four studies investigate the relation between external load lifting and LPR. Lifting a 12 kg load during flexion-extension of the trunk confirmed alteration in trunk section coordination in both a low back pain and a control group (C. Larivière, Gagnon, & Loisel, 2000). A pattern of hyper-kyphosis during extension was observed in lumbar curvature during lifting loads. Subjects were found to move from a more neutral to a more kyphotic extension of lumbar curvature during lifting tasks, particularly while they lifting heavier objects (Maduri, Pearson, & Wilson, 2008). That result confirms Iwasaki et al.’s that the lumbar pelvic rhythm can be altered by load (Iwasaki et al., 2014). 210

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On the other hand, Granata and Sanford show that trunk extension was achieved through simultaneous but nonlinear contributions from both the pelvis and lumbar spine throughout the whole ROM. The task weight increased the lumbar contribution to total trunk motion, which supports previous observations (K. P. Granata & Sanford, 2000). 3.4. Muscle fatigue Two studies present muscle fatigue as a factor altering LPR. The results of these studies show that, after lumbar muscles became fatigued, the subjects displayed a larger L/P ratio during weight lifting and such changes also resulted in larger spinal loading (Hu & Ning, 2015a). After the fatiguing protocol, subjects demonstrated significantly more in-phase lumbar-pelvic coordination (Hu & Ning, 2015b). 3.5. Feet position Two studies showed the influence of feet position on LPR in this review. Zhou et al. observed a significantly larger maximum pelvic angle with the increase of feet placement width. The maximum lumbar angle, however, was not significantly affected by such width. The study shows that a more in-phase coordination pattern was adopted by participants to compensate for their decreased stability in the narrow stance condition. Wide stance seems to be a more stable position and gives better support for spino-pelvic coordination (Zhou et al., 2016). A greater (17%) lumbar sagittal flexion was noted in the narrow stance condition as compared to the wide stance condition (Sorensen, Haddad, Campbell, & Mirka, 2011). 3.6. Movement speed Four studies demonstrated the influence of movement speed on LPR. A more antiphase and unstable lumbopelvic coordination pattern was observed during the long duration of motion. Compared with the 3-s condition, the lumbopelvic CRP was significantly greater in the 15-s condition, indicating a more anti-phase coordination pattern. Phase variability was also greater in the 15-s trials than in the 3-s trials. Therefore, an unstable coordination pattern can be caused by more active neuromuscular control (Zhou, Ning, & Fathallah, 2016b). Vazirian et al. stated that lumbar contribution to trunk motion was smaller under a fast pace than under a slow one (Vazirian et al., 2017). The trajectory of three cycles of repeated bending performed by the asymptomatic and LBP groups were examined by Tsang et al. There was no significant difference in the mean flexion range of the lumbar spine and hip across the 5 speed levels or between the 2 groups. However, LBP patients bent with a significantly lower peak velocity at their lumbar spine at the very slow and slow speed levels, compared to the asymptomatic group (Tsang et al., 2017). Lumbar contribution to the trunk motion was significantly smaller during the second and third quarters of both motion phases (flexion and return from flexion) of task performed at a fast pace compared to the task at the preferred pace. The MARP during forward bending and DP during both phases were significantly smaller in the task at a fast pace than in the preferred pace (Shojaei, Vazirian, et al., 2017). 3.7. Phase of movement (Flexion/extension) Six studies compare flexion and/or extension phases during the sagittal plane motion of the trunk. The lumbopelvic CRP in trunk flexion in standing was significantly greater than during trunk extension motion, which indicates a more out-of-phase (asynchronous) coordination pattern. A more out-of-phase lumbopelvic motion could help reduce spinal loading during trunk flexion. Motion CRP changed from a larger variability in the first half of the motion to a smaller variability in the second half of the trunk flexion (Zhou, Ning, & Fathallah, 2016a). Tojima et al. reported that lumbar ROM was greater than hip ROM during the backward phase of the extension. Moreover, the lumbar ROM was more reduced than the hip ROM during the forward phase of the extension. The L/P ratio increased significantly in the backward phase of the extension (Tojima, Ogata, Nakahara, & Haga, 2016). In another study, lumbar and pelvic motion was monitored while lifting and lowering a 9.5 kg box with knees extended. The LPR varied depending on whether the trunk was flexing or extending. During trunk flexion there was a greater tendency for lumbar and pelvic rotations to occur simultaneously. However, during extension they tended to occur more sequentially (Nelson, Walmsley, & Stevenson, 1995) The study of Pal et al. shows that, in flexion, the initial movement was dominated by the lumbar spine followed by a brief period in which there was an equal contribution from the lumbar spine and hip. In the final part of forward flexion, hip domination was observed. The hip dominated also the first part of the return movement with an equal contribution from the hip and lumbar spine throughout the remaining part of the movement (Pal et al., 2007). Similar findings of Tafazzol et al. demonstrate that the trunk movements were primarily accomplished by the lumbar rotation during the early phases of flexion while it occurred mainly at the pelvis during the final phases. The lumbar spine contributed more to the trunk rotation during the final stages and the pelvis contributed more during the early stages of backward extension (Tafazzol et al., 2014). Results from the same direction task noted by Kasahara et al. indicate the existence of LPR in the sitting position similar to that observed in the standing position. The L/P ratio was consistent during the movement from an erect to a slumped sitting position (lumbar spine and pelvis then moved in opposing directions) (Kasahara, Miyamoto, Takahashi, Yamanaka, & Takeda, 2008). 211

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4. Discussion 4.1. Age and gender Trunk flexion is closely associated with low back load, and has been regarded as a risk factor for occupational LBP (Ma & Shan, 2017; Marras et al., 1995; Song & Qu, 2014a). Age related differences observed during trunk motion may be interpreted in two ways. On the one hand, they can be precursors of LBP in older people. According to Shojaei et al. the older participants completed the tasks with larger pelvic rotation and smaller lumbar flexion. With age, connected tissue elasticity decreases and may in consequence limit the range of motion (Barros et al., 2002). The decreased spine flexion in older adults could be associated with age-related decreases in trunk flexibility. These movement patterns suggest that older individuals may be at a higher risk for developing LBP when completing similar manual material handling tasks. That is consistent with epidemiological evidence for higher risks of occupational LBP among this group (Shojaei et al., 2016). On the other hand, older participants have a large margin in their flexibility/ROM capacity when conducting the lifting tasks. Therefore, a reduction in trunk flexibility and ROM with age may not be the major cause of the age-related decrease in trunk flexion. Instead, changes of trunk kinematics could mainly reflect the adoption of a safer lifting strategy to reduce low back load by older adults (Song & Qu, 2014a). The results showed that older adults tend to use safer lifting strategies compared with young adults (Song & Qu, 2014b). Smaller pelvic ROM and larger lumbar ROM were observed in younger versus older female participants during sagittal plane motion (Shojaei et al., 2017). A more in-phase and more stable LPR noted in older versus younger individuals may be a neuromuscular strategy to protect the lower back tissues from excessive strain in order to reduce the risk of injury (Vazirian et al., 2017). 4.2. Hamstring muscles Hamstrings are biarticular muscles, which mainly flex the knee and extend the hip. They also stabilise the pelvis in the sagittal plane by controlling the anterior pelvic tilt during trunk flexion. Hence, hamstrings may have influence on the lumbosacral region (Esola et al., 1996; Gajdosik, Hatcher, & Whitsell, 1992; Jandre Reis & Macedo, 2015; Jang, Koh, & Han, 2013; López-Miñarro, Muyor, Belmonte, & Alacid, 2012). Thus, it was hypothesised that hamstring tightness could decrease pelvic motion and, as a compensatory reaction on ROM deficit, increase spine motion. On the other hand, more flexible hamstring muscles may help to save “normal” lumbar pelvic coordination. During the toe-touch test, the mean flexion ROM of the pelvis was less for men with short hamstrings (52°; SD, 9°) than for men without short hamstrings (72°; SD, 4°), but the lumbar flexion ROM was not significantly different (Gajdosik et al., 1992). The purpose of stretching is most usually to increase the ROM and reduce stiffness of the muscle-tendon unit. López-Miñarro et al.’s study demonstrates significant increases in the hip flexion ROM in the active SLR test immediately after the stretching protocol. This change was associated with a significant improvement in anterior pelvic tilt and lumbar flexion as well as reduced thoracic kyphosis during the sit and reach test (López-Miñarro et al., 2012). The passive knee extension exercise in the sitting position and SLR exercises are both effective in improving forward bending in LBP subjects. However, passive knee extension, which allows for stability of the lumbar spine, was more effective when the motion required LPR. Thus, these findings support the hypothesis about the controlling function of hamstring muscles on LPR during forward bending (Jang et al., 2013). Flexion-relaxation response is present in the lumbar erector spinae, in the hamstrings and lower thoracic erector spinae during trunk sagittal motion (McGorry, Hsiang, Fathallah, & Clancy, 2001). In standing, the timing of activation differed significantly by site in extension. However, it was not observed in flexion (McGorry et al., 2001). The hamstring muscles and back extensors relax during forward flexion but with different timing. This may confirm that LPR is controlled by the back and the hamstring muscles at different timing (Sihvonen, 1997). Iwasaki et al. indicate that an increase in spinal instability and stress on the posterior ligaments can be caused by delayed lumbar extension during stoop lifting. This mechanism shows that stoop lifting of a load may be a risk for the lower back of subjects with hamstring tightness (Iwasaki et al., 2014). Tight hamstrings are often observed in patients suffering from LBP. Back pain is associated with changes in the mechanical characteristics of the posterior hip tissues or changes in the level of activity of the posterior hip muscles such as the hamstrings (Wong & Lee, 2004). However, the causes of increased tension or shortness of these muscles remain unclear. A possible explanation can be compensation in response to poor stability of the lumbar pelvic complex in LBP subjects. 4.3. External load The lifting technique using forward bending with straightened knees is one of the most investigated and popular ways of picking up an object from the floor (van Dieën, Hoozemans, & Toussaint, 1999). However, it is not a recommended technique because of shear and compression forces acting on lumbar spine structures (Bazrgari, Shirazi-Adl, & Arjmand, 2007). Stoop lifting is often compared with squat lifting, which seems to be safer (Bazrgari et al., 2007; Hwang, Kim, & Kim, 2009; van Dieën et al., 1999). During the extension phase of the stoop, lifting subjects were found to assume a more kyphotic posture, approaching the edge of the functional ROM. This strategy allows the lumbar curvature to go in a highly kyphotic posture, and subjects may take advantage of stretch-shortening behavior in extensor musculature and tendons to reduce the energy required to raise the trunk. Such a kyphotic posture during extension may put an excessive load on the elastic structures of the spine, thus increasing the risk of injury (Maduri et al., 2008). 212

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The eccentric co-contraction of the gastrocnemius and hamstrings was found to be important for maintaining the leg straight during the stoop lifting. Hwang et al. reported that hip moment had significant correlation with the lumbar joint moment in stoop lifting. (Hwang et al., 2009). It was hypothesised that an increase of pelvic and spine mobility can decrease lumbar spine loading. It had previously been investigated that no significant differences in the pelvic forward tilt were observed between trials in which the subject acted with or without instruction to increase the pelvic forward tilt in the stoop posture. The stoop posture required a high angle of pelvic tilt. Probably because of that, a further increase in pelvic forward tilt might be difficult to perform (Hayashi, Katsuhira, Matsudaira, & Maruyama, 2016). Changes observed during lifting tasks in ROM and timing can be a mechanism making lifting more economical. However, repeating it regularly, for example in occupational work, can cause back injuries. 4.4. Muscle fatigue Results of a study by Hu and Ning showed that, after fatigue, protocol subjects adopted larger lumbar motion during weight lifting and demonstrated significantly more in-phase LPR (Hu & Ning, 2015a, 2015b). These results are quite similar to those observed during standard lifting but may confirm that muscle fatigue increases the observed changes. Fatigue in the extensor muscles of the trunk affects neuromuscular recruitment and control of the spine. Previously it has been suggested that the trunk had poorer dynamic stability when the muscles were fatigued. Thus, fatigue may contribute to low back disorders due to spinal instability (Granata & Gottipati, 2008). Moreover, it has been hypothesised that changes in muscle recruitment patterns, such as muscle co-contraction, act as compensation for spinal instability resulting from passive element laxity or reduced neuromuscular control. A transient elongation of a muscle due to passive static stretching produces fatigue-like responses including reduced motor unit activation and average conduction velocity, reduced reflex responses, reduced active force generating capacity at any given state of activation, and a rightward shift of force-length relationship curve (Shin, D’Souza, & Liu, 2009). The creep in the spine ligaments is thought to increase the intervertebral joints laxity, allowing increased relative motion (Abboud, Lardon, Boivin, Dugas, & Descarreaux, 2017; Abboud, Nougarou, & Descarreaux, 2016) Therefore, muscle fatigue can be related to muscle creep during prolonged flexion posture associated with lifting and carrying in occupational work. However, it remains unclear how muscle fatigue affects reflex latency of erector spinae muscles (Abboud et al., 2017) Shin et al. reported that the flexion-relaxation onset angle in isokinetic flexion and the EMG amplitude of isometric extension were significantly greater after static flexion. Fatigue of low back extensor muscles may occur in static flexion due to prolonged passive stretching of the muscles. When the contribution of creep deformed passive tissues is reduced, low back extensor muscles are required to generate more active forces in weight holding or lifting after static flexion. Prolonged trunk flexion leads to passive tissue deformation which may increase trunk muscle contribution to spinal stabilization mechanisms during fatigue (Abboud et al., 2016; Shin et al., 2009). Fatigue and creep may also be related in another way. It is possible that these muscles, in a state of fatigue, are not able to provide sufficient stabilization to the spine, transferring load-sharing to passive structures earlier in trunk flexion (Descarreaux, Lafond, Jeffrey-Gauthier, Centomo, & Cantin, 2008). What is more, the power frequency of lumbar erector spinae during isometric extension was significantly lower after static flexion. The degraded force generating capacity of the fatigued muscles can be a significant risk factor for low back pain (Shin et al., 2009). This suggests that spinal tissue creep induces neuromuscular adaptations similar to those observed under muscle fatigue or muscular pain conditions. This opinion is confirmed by Abboud et al. They found that median frequency values showed a significant main creep effect, with lower median frequency. The results also showed that prolonged flexion of the trunk led to adaptations in muscle activity distribution. The increase in full flexion angle observed following a spinal tissue creep might result from the combined viscoelastic elongation of hamstring and erector spinae muscles (Abboud et al., 2016). However, results of a Sparto and Parnianpour study do not suggest that an increase in the muscular loading of the spine occurs as a result of changing trunk muscular recruitment patterns. Changes of the erector spinae and latissimus dorsi muscle forces was dependent on the load level and repetition rate. The reduction in erector spinae forces offset must increase force in the other muscles because the net changes in compression and lateral shear forces on the spine were not significant (Sparto & Parnianpour, 1998). 4.5. Feet position Ankle and foot deviations can be considered a potential cause for LBP due to the disruption of the kinetic chain from the foot to the back. Changes in feet posture may lead to the presence of postural alterations of the lumbopelvic complex, increasing the risk of developing LBP. By examining the kinetic chain from the ankle and foot up to the back, mechanical causes of LBP can be better understood (O’Leary, Cahill, Robinson, Barnes, & Hong, 2013). It has been reported previously that decreased ankle dorsiflexion may be a factor in chronic mechanical LBP (Brantingham, Lee Gilbert, Shaik, & Globe, 2006). The influence of foot pronation (measured as calcaneal eversion) on pelvic alignment during standing is not well known. The bilateral and unilateral pronation caused increases in pelvic anteversion (sagittal plane), and the unilateral pronation led to lateral pelvic tilt (Pinto et al., 2008). Foot and pelvic kinematics have an influence on each other. Cho et al. investigated correlations among pelvic positions and differences in lower extremity joint angles during walking. Pelvic position was found to be positively correlated to differences between left and right hip flexion; hip abduction; knee flexion and abduction; and ankle inversion (Cho, 2015). Khamis and Yizhar found that standing on wedges at various angles induced hyperpronation, a statistically significant increase in internal shank rotation. Internal hip rotation and anterior pelvic tilt were also identified (Khamis & Yizhar, 2007). A relationship was 213

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found between the anterior pelvic tilt and internal thigh rotation, in all investigated standing positions (Khamis, Dar, Peretz, & Yizhar, 2015). Zhou et al. investigated the sudden release of a 6.8-kg external load from symmetric or asymmetric directions while maintaining four different foot placements. The results showed that subjects experienced less trunk flexion and less shear force with a staggered stance with the right foot forward (the most preferred placement) compared with a wide stance (Zhou, Dai, & Ning, 2013). To conclude, not only is pelvic tilt affected by bilateral induced hyperpronation while in a standing position but also other joints and trunk dynamics. Foot position (width and angle) can alter spino-pelvic motion during sagittal trunk conditions, for example, during lifting tasks. As the cited studies show, a wide stance seems to be a more recommended position. 4.6. Movement speed Speed effects on movement characteristics have been studied previously (Thomas, Corcos, & Hasan, 2003). The LBP group was significantly slower compared with healthy controls. The reduced speed of lumbar movement may be linked to fear of movement (Laird et al., 2014; Thomas, France, Lavender, & Johnson, 2008). Slower paced flexion-extension trunk movements are associated with more motor variation as well as local and orbital stability, implying a lesser potential risk of injury for the trunk. Chronic LBP patients exhibited more stable trunk movements over long-term periods, indicating the probable temporary pain relief of functional adaption strategies (Asgari et al., 2015). That conclusion is confirmed by Shojaei et al. They consider the reduced lumbar range of flexion and a slower task pace observed in patients with acute LBP, as a result of a neuromuscular adaptation to lower back tissue deformation and avoiding pain (Shojaei et al., 2017). However, Tsang et al. show that, in contrast to the movements of the pain-free group, LPR in the LBP group was independent of the bending speed level. This may suggest that individuals with LBP do not select movement strategies that take account of the different demands of functional tasks. Their stereotyped LPR could be an adaptive strategy to avoid aggravation of back pain (Tsang et al., 2017). 4.7. Phase of movement (flexion/extension) Phase of movement in the same direction as flexion and extension, or forward flexion and return may affect coordination of the lumbopelvic complex. The contribution of spine and pelvis may also depend on the stage of flexion/extension. As shown by Tafazzol et al., while the lumbar spine contributed more to the trunk rotation during early and final stages of forward flexion and backward extension, respectively, the pelvis contributed more during the final and early stages of forward flexion and backward extension, respectively (Tafazzol et al., 2014). In the first half of the trunk flexion, as demonstrated by Tafazzol et al., lumbar flexion and pelvic rotation were more asynchronous. In the second half of the trunk flexion, the two segments were more synchronous. Trunk extension showed an opposite pattern. Altered movement patterns of the spine and hip may be a potential factor that contributes to the development of low back pain (Tafazzol et al., 2014). A number of studies have shown that LBP patients demonstrated more in-phase lumbar-pelvic coordination and reduced lumbar stability, which could reduce the dynamic complexity of the body and may be viewed as a protecting mechanism (Hu & Ning, 2015a). Differences in trunk muscles co-contraction was observed during isometric lumbar flexion and extension. During flexion exertions co-contraction was significantly greater than during extension exertions. Associated with cocontraction, spinal load during flexion exertions was also significantly greater than during trunk extension (Kevin P. Granata, Lee, & Franklin, 2005). Differences in kinematics, timing and muscles activation during flexion and extension of trunk may play important roles in understanding the abnormalities observed in LBP patients and need to be carefully investigated having regard also to the different parts of these phases. 4.8. Practical implications Factors described in this study can be direct determinants of lumbopelvic kinematics during motion in the sagittal plane. However, there is also a possible explanation of all the observed changes in LPR as an indirect cause of them. This explanation includes motor control with neuro-muscular coordination and passive tissue mechanics. Motor control dysfunction can be a key to understanding lumbar and pelvic biomechanics. Dysfunctional neuromuscular control strategies such as muscle activation levels or the coordination of muscle contractions is defined as “clinical instability”. In other words it is “the loss of the ability of the spine to maintain its pattern of displacement under physiologic loads resulting in no initial or additional neurological deficit, no major deformity, and no incapacitating pain” (Bruno, 2014; Panjabi, 2003). Panjabi described three inter-coordinated subsystems that are collectively responsible for adapting to the stability requirements of the spine: a passive subsystem (passive tissue), an active subsystem (muscles) and a neural control subsystem (Panjabi, 1992). Motor control and proprioception deficits are two of the most frequent symptoms observed in LBP patients. Knowledge about factors which can cause LPR may help clinicians understand the mechanisms of LBP. Altered movement patterns of the spine and hip may be potential factors that contribute to the development of LBP. Changes in spine and hip mobility would alter the bending stresses of the spinal motion segment, facets and posterior spinal ligaments. On the other hand, altered movement patterns of the spine and hip may be the consequence of low back pain. It may be a compensatory response to reduce pain or to protect injured tissues (Lee & Wong, 2002; Shum, Crosbie, & Lee, 2005). Some findings suggest that hip and lumbar spine kinematics during forward flexion tasks are not the same as those observed during other functional tasks. The results of an Alqhtani et al. study show that there are similarities between flexion and lifting in spine mobility. The ROM was different at the hip for lifting, where a greater range of hip flexion was used to achieve the lift. This shift in hip contribution did not seem to 214

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affect the lumbar spine, suggesting that individuals who use more hip flexion during lifting do not necessarily decrease their lumbar flexion ROM (Alqhtani, Jones, Theobald, & Williams, 2015). Electromyographic amplitude of lumbar over thoracic erector spinae and antagonist muscles activation ratio was observed to be greater in patients than in control subjects. That mechanism may be used for stabilising the spine. Besides the positive effect of a change in trunk muscle recruitment patterns and increased cocontraction could cause pain in the muscles and increase the forces acting on the spine (van Dieën, Cholewicki, & Radebold, 2003). Nelson-Wong shows that participants with LBP demonstrated a variable strategy, while control subjects used a consistent proximal to distal muscle activation strategy during both frontal and sagittal plane movements (Nelson-Wong et al., 2013). That suggests that differences observed in kinematics can be involved in changes in neuromuscular control. During flexion, the erector spinae muscles in individuals with higher toe-touch scores were relaxed in larger trunk and hip angles and reactivated earlier during extension according to these angles (Hashemirad, Talebian, Hatef, & Kahlaee, 2009). It was previously investigated that differences in lumbar pelvic motion occurred between healthy individuals and LBP patients (Shum et al., 2007a), subjects with a history of low back pain (Esola et al., 1996) and between different subgroups of LBP patients (Dillen, Gombatto, Collins, Engsberg, & Sahrmann, 2007; Kim, Yoo, & Choi, 2013; Kim et al., 2013) as well. Kim et al. suggested that the differences between the two LBP subgroups may be a result of imbalance and asymmetry in erector spinae and hamstring muscle properties. The authors suggest that asymmetry of passive tissue can lead to asymmetry of muscular activation (Kim et al., 2013). Therefore, passive structures rather than the paraspinal muscles can provide spinal stability. However, changes in the flexibility of the spine exert a major influence on the neuromuscular stabilising system (Kim et al., 2013). On the other hand, it is equally possible that immobility of the hip and lower limb could lead to excessive spinal motion that could lead to LBP (McGregor & Hukins, 2009). It has been reported that a more in-phase lumbopelvic coordination pattern can be a spontaneous adaptation as a motor control strategy to attain a guarded movement (Shojaei et al., 2017; Zhou et al., 2016b). Deficiency of muscular stabilization in the trunk associated with LBP may help explain more stiff trunks and hip articulations to minimize the internal perturbation associated with the repeated bending tasks. The reduced lumbar contribution to trunk motion and more in-phase and less variable lumbopelvic coordination in LBP patients compared to the asymptomatic controls are a likely mechanism to reduce pain and protect injured back tissues (Shojaei et al., 2017). Participants who were currently asymptomatic but had a history of low back pain moved in a manner similar to that of participants with no history of low back pain. However, they demonstrated greater lumbar motion and velocity during the initial phase of extension (McClure et al., 1997). It has been observed that trunk flexion-extension coordination altered during the pain-free periods of recurrent LBP patients in a way different from that observed in patients experiencing acute pain. Relaxation of back muscles started later during flexion and finished earlier during extension. The reduction in the duration of flexionrelaxation response was not associated to differences in motion ranges, but testifies to different neuromuscular activation strategies (Sánchez-Zuriaga, López-Pascual, Garrido-Jaén, & García-Mas, 2015). Alqhtani et al. investigate the range of motion and velocity of the spine and hip in four functional tasks. They suggest that sagittal tasks use different lumbar-hip kinematics and place different demands on the spine and hip. The authors conclude that clinicians should not extrapolate findings from the clinical testing of flexion to other functional tasks (Alqhtani et al., 2015). Thus, investigations of functional tasks are needed to elaborate the best tests for patent evaluation (Shum, Crosbie, & Lee, 2007b). This review study provides useful information on the kinematic patterns of the spine and the pelvis. All the described factors should be taken into account by clinicians during physical examination. 4.9. Limitations The study has a few limitations. First of all, we focused mainly on searching investigations which included healthy participants. A number of researchers have reported differences in lumbopelvic rhythm between healthy subjects and patients. These findings often did not explain if these differences are the causes or results of the dysfunction. However, studies examining patients obviously have a practical application. Secondly, we did not consider the potential influence of study quality, as well as the methodological and measurement differences on the reported results. 5. Conclusion This paper includes in its review 31 studies. The literature review demonstrates factors contributing to lumbopelvic motion. Age and gender, hamstring muscle tightness, feet position, muscle fatigue, movement speed and external loading as well as phase of motion can affect various aspects of lumbar pelvic kinematics, such as range of motion, timing or lumbopelvic rhythm. References Abboud, J., Lardon, A., Boivin, F., Dugas, C., & Descarreaux, M. (2017). Effects of muscle fatigue, creep, and musculoskeletal pain on neuromuscular responses to unexpected perturbation of the trunk: A systematic review. Frontiers in Human Neuroscience, 10. http://dx.doi.org/10.3389/fnhum.2016.00667. Abboud, J., Nougarou, F., & Descarreaux, M. (2016). 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