Gait and energy consumption in adolescent idiopathic scoliosis: A literature review

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REHAB-1054; No. of Pages 10 Annals of Physical and Rehabilitation Medicine xxx (2016) xxx–xxx

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Review

Gait and energy consumption in adolescent idiopathic scoliosis: A literature review Aliyeh Daryabor a, Mokhtar Arazpour a,*, Guive Sharifi b, Monireh Ahmadi Bani a, Atefeh Aboutorabi a, Navid Golchin c a Department of Orthotics and Prosthetics, University of Social Welfare and Rehabilitation Sciences, Kodakyarst, Daneshjo Boulevard, Evin, Tehran 1985713834, Iran b Loghman Hakim hospital, Shahid Beheshti University of Medical Sciences, Department of Neurosurgery, Tehran, Iran c Department of Neurosurgery, Firuzgar Hospital, Tehran University of Medical Sciences, Tehran, Iran

A R T I C L E I N F O

A B S T R A C T

Article history: Received 14 August 2016 Accepted 25 October 2016

Background: Adolescent idiopathic scoliosis (AIS) is a progressive growth disease that affects spinal anatomy, mobility, and left-right trunk symmetry. The disease can modify human gait. Objective: We aimed to review articles describing the measurement of gait parameters and energy consumption in AIS during walking without any intervention. Study design: Literature review. Methods: The search strategy was based on the Population Intervention Comparison Outcome method and included all relevant articles published from 1996 to 2015. Articles were searched in MEDLINE via PubMed, Science Direct, Google Scholar, and ISI Web of Knowledge databases. Results: We selected 33 studies investigating the effect of scoliosis deformity on gait parameters and energy expenditure during walking. Most of the studies concluded no significant differences in walking speed, cadence and step width in scoliosis patients and normal participants. However, patients showed decreased hip and pelvic motion, excessive energy cost of walking, stepping pattern asymmetry and ground reaction force asymmetry. Conclusion: We lack consistent evidence of the effect of scoliosis on temporal spatial and kinematic parameters in AIS patients as compared with normal people. However, further research is needed to assess the effect of scoliosis on gait and energy consumption.

C 2016 Published by Elsevier Masson SAS.

Keywords: Scoliosis Walking Gait parameters Energy consumption

1. Introduction Adolescent idiopathic scoliosis (AIS) is a three-dimensional spine deformation (lateral curvature, rotation of the vertebrae and rib hump) that is prevalent in 1% to 3% of adolescents 10 to 16 years old [1]. The scoliosis is accompanied by postural alterations, standing instability, and gait variations and can also cause pain and reduced quality of life if untreated, especially with greater curves [2–7]. Gait is the most common human movement involving daily activities. The human spine, pelvis, hip, knee, and ankle have been modified during evolution to create functional and efficient bipedal locomotion for ease of walking. AIS affects spinal

* Corresponding author. Tel.: +98 21 22 18 00 10; fax: +98 21 22 18 00 49. E-mail address: [email protected] (M. Arazpour).

mobility and trunk balance, altering locomotion patterns during each step. Because the trunk helps maintain equilibrium [8], spinal deformation changes the center of body mass (COM) during gait, which leads to gait abnormalities. Several studies have shown differing gait patterns between participants with untreated AIS and their healthy peers. The literature suggests that AIS affects walking speed [9–11], cadence [12], step length [6,9,13], range of motion (ROM) in pelvic, hip, and knee [6,10]; loading and unloading [14], ground reaction force (GRF) symmetry [14,15], and energy expenditure [16,17]. Nearly all studies that analyzed gait in participants with AIS reported some gait abnormality; however, these results were contradictory [6,13,14]. Moreover, several research groups have investigated gait analysis in experimental protocols to study functional disabilities in untreated AIS or in comparison to healthy peers. To the best of our knowledge, a comprehensive review of the topic is lacking. Thus, this review article aimed to assess the gait

http://dx.doi.org/10.1016/j.rehab.2016.10.008 C 2016 Published by Elsevier Masson SAS. 1877-0657/

Please cite this article in press as: Daryabor A, et al. Gait and energy consumption in adolescent idiopathic scoliosis: A literature review. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.10.008

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patterns and energy expenditure during walking in AIS adolescents without any therapy intervention.

kinetic parameters, mechanical work and energy expenditure in adolescent scoliosis patients and normal controls.

2. Methods

3.1. Temporal spatial parameters

2.1. Study eligibility criteria

3.1.1. Speed of walking The mean walking speed has been reported to be 1.24 m/s in healthy subjects during ambulation [18] (Table 1). Other studies reported the mean walking speed to be 1.04, 1.15, and 1.22 m/s. We found 14 studies that compared gait speed in scoliosis patients and normal participants; 11 reported no significant difference between scoliotic and normal participants in walking speed [13,19–28]. However, 3 studies found walking velocity significantly reduced in scoliosis patients [9–11]. Mallau et al. [9] investigated the effect of AIS on temporal and spatial parameters during walking in 17 AIS patients and 16 healthy participants (control) during various locomotor tasks: walking on the ground, walking on a line, and walking on a beam. For patients with AIS, the walking speed (m/s) was lower by 15% on the ground, 16% on a line, and 16% on a beam than for controls [9]. Chow et al. [27] evaluated the effect of backpack loads of 0%, 7.5%, 10.0%, 12.5% and 15.0% of weight bearing on walking in 22 healthy participants and 28 patients with mild AIS. Speed of walking was significantly reduced (P = 0.002) with increasing backpack load for both scoliotic and control participants but with no significant differences in gait velocity for the 2 groups [27].

Because of limited RCT study designs, the review included clinical trials and observational studies (cohort, cross section and case-control) that studied the effect of scoliosis on gait (walking) parameters and/or energy expenditure in adolescents. We excluded studies that involved the use of spinal braces/orthoses, surgery and fusion as an intervention method on gait (walking) parameters and/or energy expenditure in idiopathic scoliosis and other interventions (such as functional electrical stimulation and casting). We also excluded studies in which participants had other disabilities such as kyphosis-scoliosis and studies that focused on other types of scoliosis such as congenital, neuropathic or traumatic scoliosis as well as myopathy and malformation scoliosis. 2.2. Information sources The search strategy was based on the Population Intervention Comparison Outcome (PICO) method and included all relevant articles published in English from 1996 to 2015. Articles were searched in MEDLINE via PubMed, Science Direct, Scopus, and ISI Web of Knowledge databases with the keywords adolescent, scoliotic, scoliosis, gait, walking, kinetic, kinematic, temporal spatial parameters, spatiotemporal, temporaspatial, speed of walking, walking speed, cadence, step length, stride length, step width, ground reaction force, energy expenditure, energy cost, energy consumption, heart rate, respiratory ratio, physiological cost index, O2 consumption and VO2. 2.3. Search strategy Two researchers (AD and MA) conducted the search separately and final selection by checking the abstracts was conducted. A three-step search strategy was used. An initial limited search was undertaken, followed by an analysis of the keywords contained in the title and abstract across all included databases. A second search involved checking the abstracts against the inclusion criteria. Finally, the search was complemented with searches of references list of included studies and gray literature (dissertations and theses, conference papers). 2.4. Data extraction and synthesis The retrieved studies were initially screened by reading the title and abstract. Two reviewers (AD and MAB) independently extracted data from each study, including general information such as author names, data of publication, study design, participant characteristics, outcome measures and key results. A narrative approach was used to synthesize the study findings due to heterogeneity of study design and outcomes and clinical (participant) features. This approach enabled exploration of relationships within the data. P < 0.05 was considered statistically significant in data analysis. 3. Results The search resulted in 33 articles (Fig. 1) investigating the effect of scoliosis deformity on temporal spatial, kinematic and

3.1.2. Cadence Eleven studies reported no significant difference in cadence for scoliosis patients compared to normal controls [6,11,13, 19,20,23–28]. However, in a comparative study of 15 healthy participants and 30 idiopathic scoliosis patients, Chen et al. [29] found cadence significantly smaller in scoliosis patients (P = 0.0001) [29]. Chow et al. [27] also reported significantly reduced cadence (P = 0.033) with increasing backpack load in both scoliotic and control participants, with no significant difference between the 2 groups [27]. 3.1.3. Stride/step length Thirteen studies analyzed stride length in scoliosis versus normal participants. Six noted a significant decrease in stride length in patients [6,9–11,13,20]; the remaining 7 reported no significant difference between normal and scoliosis groups [19,23,24,26–29]. Mallau et al. [9] showed that for AIS patients, the stride length (m) was shorter by 9% on the ground and 12% on a line as compared with healthy participants [9]. Chow et al. [27] reported a significant reduction in stride length (P = 0.001) and step length (P = 0.003) with increasing backpack load in healthy and scoliotic patients, with no significant difference between the 2 groups [27]. Two studies reported reduced step length with increasing Cobb angle (CA) and with the sum of angles describing the spinal deformity in frontal and sagittal planes (P < 0.05) [30,31]. 3.1.4. Stride/step width Only 2 studies reported the effect of scoliosis deformity on stride width. Mallau et al. [9] found that this factor did not change significantly between AIS patients and controls when walking on the ground, on a line, or on a beam. However, the authors reported that step width was reduced for controls when walking on narrow supports (P < 0.001) and for patients with AIS [9]. In the Yee study [26], the 2 groups did not differ in step width.

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Records identified through database searching PubMed (n=1325) ISI web of knowledge (n=480) Scopus (n=992)

3

Additional records identified through other sources (conference, thesis) (n= 140)

Records after duplicates removed (n=345)

Records screened (n=3043)

Full-text articles assessed for eligibility (n= 82)

Full-text articles excluded (n= 50)

1 Added after examining the references

33 papers included 3 Prospective studies 15 Comparative studies 15 Research support Fig. 1. The selection of studies for the review. Preferred reporting items for systematic reviews and meta-analyses (PRISMA).

3.1.5. Gait asymmetry Five studies showed that side-to-side asymmetry for walking speed, cadence, and step length did not differ for scoliosis patients [11,23,24,28,29]. However, Yang et al. [19] reported different step lengths for bilateral leg for scolosis patients and similar step lengths for bilateral legs for healthy controls. 3.2. Kinematic parameters 3.2.1. Pelvic ROM Four studies showed lower pelvic ROM in sagittal, frontal, and transverse planes for scoliosis patients than normal controls [6,10,26,32] (Table 2). However, 2 studies showed that the pelvic kinematics did not significantly differ between normal participants and AIS patients during walking [13,23]. Syczewska et al. reported significantly increased pelvic obliquity with the CA [30,31]. However, Mahaudens et al. reported no significant differences between 3 scoliosis groups for all kinematic parameters [6]. Other studies showed kinematic variables of the pelvis with a consistent increase or decrease with increasing load carriage between AIS and normal groups [26,27]. Neither

group showed a significant effect of increasing load on kinematic parameters of the pelvis [27]. 3.2.2. Hip, knee, and ankle ROM Four studies showed lower hip ROM in sagittal [32,33], frontal [6], and transverse [6,29,32] planes for scoliosis patients than normal controls. However, other studies showed no difference in hip ROM in the sagittal [20] and coronal planes between the 2 groups [29]. Kramers-de Quervain et al. [20] reported that the sagittal plane knee and ankle motion followed a physiological pattern. Syczewska et al. showed that the ankle joints in scoliosis patients had dorsiflexed position in the swing phase and internal rotation position with respect to the shank [32]. All hip kinematic data showed a consistent increase or decrease with increasing load, with the exception of peak hip extension in stance, which showed an initial decrease and then an increase [27]. Among the kinematic variables of the knee and ankle, the peak knee flexion in loading response demonstrated a significant main effect of load (P < 0.001) — an increase with increasing load. No significant main effect was reported for any of the kinematic variables of the hip, knee, and ankle for both AIS patients and normal controls [27].

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Table 1 Studies investigating the effect of scoliosis on temporaspatial parameters of gait. Author/year

Study type

Participant(s)

Cobb angle (CA)

Outcome measures

Results

Schmid et al., 2016 [23]

Comparative

Normal: 15 AIS: 14

T: 43.7 TL: 38.7

Gait speed, cadence and stride length

Kaviani et al., 2015 [22]

Comparative cross-sectional study

Normal: 10 AIS: 10

T: CA 248–478

Gait speed

Park et al., 2015 [10]

Comparative study

Normal: 30 AIS: 20 (23: T and 16: TL)

33.6

Walking speed and stride length

Yang et al., 2013 [19]

Research support Age-matched

Normal: 39 AIS: 20 (16: T, 19: TL and 7: L)

15.48 T, 17.658 TL and 4.458L

Gait speed, cadence and stride length

Mahaudens et al., 2005 [13]

Paired sample matched for age and gender

Normal: 12 AIS: 24

TL and L: 108 < CA

Gait speed, cadence and stride length

Kramers-de Quervain et al., 2004 [20]

Research support

AIS: 7

Left L: 38.71 Right T: 53

Gait speed, cadence and stride length

Mallau et al., 2007 [9]

Comparative study

Normal: 16 AIS: 17

T, TL and L CA 08–308

Gait speed, step width and stride length

Yazdani and Farahpour, 2014 [24]

Research support

Normal: 18 AIS: 18

T: CA > 108

Gait speed, cadence and stride length

Haber and Sacco, 2015 [11]

Comparative research, case-control

Normal: 31 AIS: 31

CA > 108

Gait speed, cadence and stride length

Chan et al., 2006 [25]

Research support

T: 43.5

Gait speed and cadence

Lao, 2001 [28]

Comparative study-thesis

Normal: 9 AIS: 19 (AIS: 9T; AIS: 3TL; AIS: 4 L; AIS: 3 double T and L) Normal: 8 AIS: 9

Right T 24.28

Gait speed, cadence and stride length

Spatiotemporal gait parameters did not indicate significant differences between the two groups No significant difference in walking speed for CG versus SG Significant reduction in walking speed and stride length in SG compared to CG CG and SG showed similar walking speeds, stride lengths and cadences. Similar step length for right and left limbs for CG but different step length for SG No significant difference in speed and cadence except for step length, which was reduced by 10% in SG compared with CG Stride length was slightly reduced in participants. Asymmetry index for step length was within the physiological limit SG had a walking velocity lower by 15% on the ground, 16% on a line, and 16% on a beam. In addition, stride length was shorter by 9% on the ground and 12% on a line compared to CG. However, step width did not change significantly when walking on the ground Walking speed, cadence, and step length parameters were similar for both SG and CG. Sideto-side asymmetry for these parameters was not significantly different in SG With the exception of cadence, gait speed and stride length was reduced significantly in SG compared with CG. Lower limb asymmetry with regards to the walking speed in SG was significantly different, but not for cadence and step length No significant differences in walking speed and cadence between the 2 groups No significant difference in all the temporaspatial parameters between the 2 groups and between right and left limbs

Please cite this article in press as: Daryabor A, et al. Gait and energy consumption in adolescent idiopathic scoliosis: A literature review. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.10.008

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Table 1 (Continued ) Author/year

Study type

Participant(s)

Cobb angle (CA)

Outcome measures

Results

Yee et al., 2005 [26]

Comparative study-thesis

Normal: 19 AIS: 9

Right T left TL and L 43.5

Gait speed, cadence, step length, stride length and step width

Prince et al., 2010 [21]

Comparative study Conference

Normal: 9 AIS: 9

178

Gait speed

Mahaudens et al., 2009 [6]

Research support

Normal: 13 AIS: 41

Left TL and L AIS: 12, CA < 208 AIS: 13, CA < 208 AIS: 16, CA  408

Gait speed, cadence and Stride length

Chow et al., 2006 [27]

Research support

Normal: 22 AIS: 28

CA < 258

Gait speed, cadence, step length and stride length

Chen et al., 1998 [29]

Comparative study

Normal: 15 AIS: 30

CA 228–678

Cadence and stride length

Syczewska et al., 2010 [30]

Research support

AIS: 35

TL CA  208

Step length

Syczewska et al., 2012 [31]

Research support

AIS: 63

TL CA 208–618

Gait velocity, cadence and step length

None of the parameters significantly differed between the 2 groups in load carrying conditions. Speed did not significantly differ between the different loading conditions No difference in walking velocity between the groups Step length and the stance phase were significantly lower in SG than CG (7%). No significant difference in walking velocity and cadence Significant decreases in walking speed, stride length, step length and cadence with increasing backpack load. However, no significant main effect of group found in these parameters Cadence was significantly slower in SG versus CG. No significant difference in cadence and stride length between left and right legs in SG Step length was reduced with increasing Cobb angle and with the sum of angles describing the spine deformation in sagittal and frontal planes Gait velocity, cadence, and step length were affected by severity of the scoliosis and type of pelvic deformity

TL: thoracolumbar; L: lumbar; T: thoracic; SG: scoliosis group; CG: control (normal) group.

3.2.3. Gait asymmetry In evaluating asymmetrical gait in AIS, Mahaudens et al. [6] and Kramers-de Quervain et al. [20] reported that scoliosis patients showed no side-to-side asymmetry (convex vs. concave) for segmental kinematic data (pelvic, hip, knee and ankle). Chen et al. reported that some scoliosis patients had side-to-side variations in hip rotation [29]. Yang et al. found AIS patients with side-to-side gait asymmetry (a combination of all segments) in the frontal and transverse planes as compared with controls [19]. 3.3. Kinetics parameters 3.3.1. Kinetics parameters during gait Two studies reported no difference in the moment of force and power peaks between control and scoliotic groups [21,28] (Table 3). However, the ankle plantar flexor and hip flexor work was significantly decreased in AIS patients versus normal controls [21]. Yazji et al. found significantly lower right hip mediolateral forces in AIS patients with left lumbar or thoracolumbar scoliosis as compared with healthy participants [34]. During walking, health participants and AIS patients did not differ in vertical and anterior-posterior GRF peaks in 3 studies [11,12,28]. However, Giakas et al. reported significantly increased GRF in scoliosis than healthy participants, especially in the mediolateral component, which suggests the presence of balance control malfunction [12].

3.3.2. Gait asymmetry The results of 4 studies showed no asymmetry in GRF data for scoliosis patients [11,12,20,28]. The GRF data from the Yang et al. study indicated that patients with AIS had asymmetrical GRF gait in the mediolateral direction versus healthy controls [19]. Schizas et al. and Chockalingam et al. noted an asymmetry of at least one kinetic parameter (contact time, value of the 2 peaks of the vertical forces and loading and unloading rates) in scoliosis patients. However, no relation was found for the noted gait asymmetry and curve direction, curve magnitude, or vertebral rotation [14,15]. Chu et al. showed that the gait asymmetry of both magnitude and time variables of GRF was associated with the pelvic tilt and severity of the spinal deformities [35]. 3.3.3. Kinetics parameters during stepping patterns Bruyneel et al. compared GRF data in terms of occurrence; impulse; the GRF values Fx (mediolateral), Fy (anteroposterior) and Fz (vertical); and asymmetry index (AI) in 10 AIS patients with a right thoracic curvature and 15 control participants during forward and lateral initiation step. Whatever the direction, AI increased for scoliosis patients as compared with healthy controls. All kinetic parameters were significantly increased in the lateral step for scoliosis than healthy participants, with no significant difference in forward step for the parameters [36]. In another study [37], for small lateral steps (LSs), convexity side initiation significantly increased the GRF impulse during the postural phase

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Table 2 Studies investigating the effect of scoliosis on kinematic parameters of gait. Authors/year

Study type

Participants

Cobb angle (CA)

Outcome measures

Results

Mahaudens et al., 2009 [6]

Research support

Normal: 13 AIS: 41

Left TL and L AIS: 12, Cb < 20 AIS: 13, Cb < 20 AIS: 16, Cb  40

Pelvic, hip knee and ankle ROM

Park et al., 2012 [33]

Research support

Normal: 5 AIS: 6

CA  258

Hip joint angles

Mahaudens et al., 2005 [13]

Paired sample matched for age and gender Research support Paired sample matched for age

Normal: 12 AIS: 12

TL and L CA > 108

3D pelvic kinematics

Normal: 20 AIS: 20

CA: 15.48 T, 17.658 TL and 4.458 L

Kramers-de Quervain et al., 2004 [20]

Research support

AIS: 7

Left L: 38.71 Right T: 53

Side-to-side gait symmetry by derivative of the angular displacements of 6 segments (foot, shank, thigh, pelvis, trunk, and head) Sagittal plane hip, knee and ankle ROM

SG showed significantly reduced pelvis, hip motion in the frontal plane, hip transverse motion and knee sagittal motion compared to CG. No significant differences between the 3 SG groups and between convex-concave sides for all kinematic variables SG showed significantly smaller hip joint angle during right foot mid-stance phase as compared to CG. No significant difference in other phases during the support phase between the 2 groups 3D pelvic kinematics did not differ between SG and normal CG during walking SG showed gait asymmetry in the transverse and frontal planes compared to CG

Park et al., 2015 [10]

Comparative study

Normal: 30 AIS: 39 (23: T and 16TL)

33.68

3D pelvic kinematics

Chow et al., 2006 [27]

Research support

Normal: 22 AIS: 28

CA < 258

Pelvic and hip ROM in all the planes and sagittal knee and ankle ROM in the sagittal plane at backpack loads of 0%, 7.5%, 10%, 12.5% and 15% body weight

Schmid et al., 2016 [23]

Comparative study-cohort Research support

Normal: 15 AIS: 14 AIS: 25

T: 43.7 TL: 38.7 CA > 208

3D pelvic kinematics

Yee et al., 2005 [26]

Comparative study-thesis

Normal: 9 AIS: 19

Right T left TL and L 43.5

Chen et al., 1998 [29]

Comparative study

Normal: 15 AIS: 30

CA 228–678

Transverse and frontal pelvic ROM in the following load carrying conditions: (1) carrying no load; (2) carrying 5 kg (10–12% body weight) on the right and (3) on the left shoulder Transverse and coronal pelvic ROM

Syczewska et al., 2010 [30]

Research support

AIS: 35

TL CA  208

Yang et al., 2013 [19]

Syczewska et al., 2006 [32]

Pelvic, hip, knee and ankle ROM

Pelvic obliquity, pelvic tilt, range of pelvic rotation, knee ROM, dorsiflexion of the foot in the swing phase

Sagittal plane hip, knee and ankle ROM and pelvic symmetry in transverse plane followed a physiological motion pattern Significant reduction in pelvic ROM in the transverse and frontal planes in SG versus CG. Pelvic ROM in the sagittal plane did not differ between the 2 groups All the kinematic parameters of the pelvis and hip showed a consistent decrease or increase with load, with the exception of the peak hip extension in stance. For the knee and ankle ROM, only the peak knee flexion in loading responsive phase demonstrated a significant effect of load, which increased with increasing load No significant main effect of group found on any of the kinematic parameters of the pelvis, hip, knee and ankle Pelvic ROM in the 3 planes did not significant differ between the 2 groups ROM of the sagittal pelvis increased, the pelvis was rotated in the transverse plane with respect to the line of progression, and the pelvis was obliqued in the frontal plane The hip orientation in the transverse and frontal planes was incorrect in half of the subjects, and the knees were slightly flexed at initial contact Ankle joints had dorsiflexed position in the swing phase and internal rotation position with respect to the shank Coronal pelvic ROM was decreased with load for all participants. Transverse pelvic ROM was significantly less in the SG than the CG when not carrying any loads. During load carrying, transverse pelvic ROM decreased for all subjects, significant only for the CG Transverse pelvic ROM was smaller in SG than CG, with the coronal pelvic ROM about the same between the 2 groups Pelvic rotation, pelvic tilt, knee ROM, and foot dorsiflexion in swing did not depend on Cobb and rotation angles, but pelvic obliquity increased with Cobb angle

Please cite this article in press as: Daryabor A, et al. Gait and energy consumption in adolescent idiopathic scoliosis: A literature review. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.10.008

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Table 2 (Continued ) Authors/year

Study type

Participants

Cobb angle (CA)

Outcome measures

Results

Syczewska et al., 2012 [31]

Research support

AIS: 63

TL CA 208–618

Pelvic retraction, pelvic tilt, pelvic rotation, pelvic obliquity, hip and knee ROM in the sagittal plane, knee flexion at initial contact, ankle dorsiflexion in swing, foot progression angle

Gait pathology in all kinematics parameters depended on the severity of scoliosis

TL: thoracolumbar; L: lumbar; T: thoracic; SG: scoliotic group; CG: control (normal) group; ROM: range of motion

Table 3 Studies that investigated the effects of scoliosis on kinetic parameters of gait. Authors/year

Study type

Participants

Cobb angle (CA)

Outcome measures

Results

Yazji et al., 2015 [34]

Comparative study

Normal: 12 AIS: 28

Left L and TL 12 AIS: CA 208–408 16 AIS: CA > 408

Hip joint mediolateral forces

Chockalingam et al., 2004 [15]

Research support

AIS: 13

69.928

Schizas et al., 1998 [14]

Research support

AIS: 21

T: 428 L: 308

Vertical first peak force (Fz1), second peak force (Fz2), loading rate (LR), unloading rate (UR), impulse and symmetry indices (SIs) LR, UR, Fz1, Fz2, mid-stance trough occurrence and stance time

Yang et al., 2013 [19]

Research support Age-matched

Normal: 20 AIS: 20

Prince et al., 2010 [21]

Comparative study-conference

Normal: 10 AIS: 9

CA: 15.48 T CA: 17.658 TL CA: 4.458 L 178

Vertical (Fz), anteriorposterior (Fy) and mediolateral (Fx) GRF Moment, power and ankle plantar flexor and hip flexor work

Giakas et al., 1996 [12]

Comparative study

Normal: 20 AIS: 20

25 < CA < 62

Force-time parameters and frequency content of the Fx, Fy and Fz component

Kramers-de Quervain et al., 2004 [20] Bruyneel et al., 2009 [36]

Research support

AIS: 7

Vertical GRF

Comparative study

Normal: 15 AIS: 10

Left L: 38.71 Right T: 53 Right T and TL CA  188

Bruyneel et al., 2008 [38]

Comparative study

Normal: 15 AIS: 10

Right T and TL CA  188

Bruyneel et al., 2010 [37]

Comparative study

Normal: 15 AIS: 10

Right T and TL CA  188

Gelalis et al., 2012 [39]

Comparative study

Normal: 8 AIS: 8

Structural curves = 18.3 Nonstructural curves = 17.58

The mediolateral forces at the right hip were significantly lower for scoliosis patients with CA 208–408 than healthy subjects. No significant difference between the 2 groups in this parameter Forces and loading rate did not differ between left and right sides in scoliosis patients No specific relationship between the curve magnitude and SIs for impulse Asymmetry of at least one kinetic parameter, but no relation between gait asymmetry and curve magnitude SG showed asymmetrical gait in the mediolateral direction of the GRF compared to the CG No difference in moment of force and power peaks between the 2 groups. Ankle plantar flexor and hip flexor work were significantly lower for in the SG than CG No significant difference in GRF time domain variables between the 2 groups. Frequency domain was significantly higher for the SG than CG, especially in the mediolateral component Vertical GRF did not display an asymmetry for the SG Whatever the direction, the asymmetry of the GRF increased for the SG than CG. For both groups, lateral initiation showed the largest asymmetry reported for forward initiation Gait initiation duration, impulses, occurrences and forces values were greater for the SG than CG For both stepping sides, the asymmetry of GRF was increased for the SG than CG No significant difference between SG and CG for GRF variables. Moreover, the bag position had no effect on loading rate

Chow et al., 2006 [27]

Research support

Normal: 22 AIS: 28

CA < 258

GRF recorded for right-limb stepping and for left limb stepping associated to forward and lateral directions

GRF evaluated for the right and left limbs during gait initiation GRF recorded for the right and left legs during large and small lateral steps Participants walked under 3 walking conditions: (1) without a schoolbag, (2) carrying a schoolbag bilaterally and (3) carrying a schoolbag unilaterally GRF data were: Fz1, T1, LR, T2 Moment and power parameters were analyzed under backpack loads of 0%, 7.5%, 10%, 12.5% and 15% weight bearing

Except for the hip extension moment and the knee flexion moment, increasing load significantly increased in all internal joint moments at the hips, knees and ankles, with no significant difference between CG and SG. SG showed lower peak sagittal power generation and peak sagittal power absorption in the knee than the CG

Please cite this article in press as: Daryabor A, et al. Gait and energy consumption in adolescent idiopathic scoliosis: A literature review. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.10.008

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8 Table 3 (Continued ) Authors/year

Study type

Participants

Cobb angle (CA)

Outcome measures

Results

Haber and Sacco, 2015 [11]

Comparative research, case-control

Normal: 31 AIS: 31

CA > 108

Vertical peak GRF values and asymmetry during loading and propulsion phases

Chu et al., 2015 [35]

Research support

AIS: 9

CA > 108

Gait asymmetry in regard to GRF

Lao, 2001 [28]

Comparative study-thesis

Normal: 8 AIS: 9

Right T 24.28

Values and times of the vertical and anteriorposterior GRF

Peak vertical GRF values did not differ between the CG and SG in both phases (P < 0.05). Lower limb symmetry for GRF was similar between right and left limbs Gait asymmetry of both values and time variables of GRF associated with severity of the pelvic tilt and spinal deformity No significant difference in all kinetic parameters between the 2 groups. Lower limb symmetry for all parameters was similar between right and left limbs

TL: thoracolumbar; L: lumbar; T: thoracic; SG: scoliotic group; CG: control (normal) group; GRF: ground reaction force; PCI: physiological cost index.

Table 4 Studies investigating the effect of scoliosis on mechanical work and energy expenditure. Authors/year

Study type

Participants

Cobb angle (CA)

Outcome measures

Results

Wallace et al., 2016 [40]

Comparative cross-sectional

Normal: 15 AIS: 15

36.2

Kaviani et al., 2015 [22] Sperandio et al., 2014 [41]

Comparative cross-sectional Comparative cross-sectional

Normal: 10 AIS: 10 Normal: 20 AIS: 29

T, CA 248–478

Oxygen consumption or VO2 PCI and THBI

dos Santos Alves and Avanzi, 2009 [17]

Clinical prospective, random study

Normal: 40 AIS: 86

Mahaudens et al., 2009 [16]

Research support

Normal: 13 AIS: 41

No significant difference during walking in volume of oxygen consumed between SG and CG No significant difference between PCI and THB index between SG and CG During incremental shuttle walk test, no difference in RR, HR between SG and CG. However, VO2 was reduced significantly in SG compared with CG (25 vs. 28) During 6-min walk test, SG showed significantly higher HR and RR, lower SpO2 (oxygen saturation) and walked less distance compared to CG In all SG, the mechanical work was significantly reduced as compared with the CG. In all SG, the average energy cost was larger by 30% (i.e., from 1.8 to 2.4 J kg 1 m 1, and the VO2 increased from 9.9 to 13.8 mL kg 1 min 1)

T and TL AIS: 3 CA < 208 AIS: 18 CA 208–408 AIS: 8 CA > 408 T 59.268

TL and L AIS: 12, CA < 20 AIS: 13, CA < 20 AIS: 16, CA  40

RR, HR, VO2

RR, SpO2, HR and distance of walking (endurance) Mechanical work (Wext, Wint and Wtot) and energy cost and VO2

THBI: total heart beat index; PCI: physiological cost index; RR: respiratory ratio; HR: heart rate; SG: scoliosis patients; CG: control group.

for scoliosis patients. For large LSs, concavity side initiation significantly increased the GRF impulse during the landing phase only. For both stepping sides, the AI was larger for scoliosis patients than controls (AI,  0.2 to  85 vs. < 0.1 to > 24.4) [37]. In another study [38], regardless of the step-initiating side, gait initiation duration (in terms of all 3 components) was significantly longer in AIS patients than healthy controls. For AIS patients, the impulse, force, and occurrence values were also greater. Under the stance foot, Fy and Fz were always increased. Under the swing foot, the scoliosis group demonstrated the same characteristics associated with reduced Fx impulse variables. Healthy participants showed only few differences in values between the 2 sides, with significantly larger values reported for AIS patients when gait was initiated with the left side compared to the right side [38]. 3.3.4. Effect of load carrying on kinetics parameters Gelalis et al. [39] compared the effect of carrying a school bag on kinetics in 8 patients with AIS and 8 healthy controls during 3 walking conditions:  without a schoolbag;  carrying a school bag bilaterally (over both shoulders — symmetrical load);  carrying a school bag unilaterally (over each shoulder — asymmetrical load).

The outcomes were first peak GRF peak (Fz1), time needed to reach Fz1 (T1), loading rate (LR) of Fz1, and total contact time (T2). Healthy and scoliotic children did not differ in any of the kinetic parameters. In addition, the bag position had no effect on LR [39]. Chow et al. [27] showed that, with the exception of the knee peak flexion moment in stance phase and hip peak extension moment in load response phase, an increase in backpack load significantly increased all internal joint moments at the hips, knees, and ankles. However, healthy and AIS groups did not differ in calculated moments. The AIS group demonstrated significantly lower peak sagittal (flexion–extension) power generation than the healthy group (0.587  0.250 vs. 0.749  0.253 W/kg; P < 0.05) and significantly lower peak power absorption at the knee (1.004  0.280 vs. 1.179  0.281 W/kg; P < 0.05). Backpack load had a significant effect in hip peak sagittal power absorption and generation as well as ankle peak sagittal power generation during toe-off, which increased with increasing load [27]. 3.4. Mechanical work and energy expenditure Mahaudens et al. [16] evaluated the differences in mechanical work during gait between normal controls (n = 13) and 3 scoliosis groups: group 1 (n = 12; CA  208), group 2 (n = 13; CA 208–408), and group 3 (n = 16; CA  408) (Table 4). The internal (Wint), external (Wext), and total (Wtot) mechanical work were significantly lower for all scoliosis groups than healthy participants.

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Scoliosis groups 1 and 3 (CA  408) showed a significant difference in total work only [16]. However, in another study, the Wext was 1.6-fold greater for AIS patients than normal controls (0.4 vs. 0.25 J kg 1 m 1). The transformation between the potential and kinetic energy was reduced in the AIS group, giving a recovery equal to 55%, which corresponded to 0.7 times the value in normal controls (70%) [13]. Energy expenditure has been measured during walking in scoliosis patients by evaluating the O2 consumption or VO2 (mL/kg/ min), energy cost (J kg 1 m 1), the physiological cost index (PCI) (beat/m), heart rate (HR) (beat/min), peripheral oxygen saturation (SpO2), respiratory ratio (RR), and endurance (the distance the person can walk) [16,17,22,40,41]. Mahaudens et al. demonstrated that in all groups, the mean energy cost was increased by 30% (i.e., from 1.8 to 2.4 J kg 1 m 1, P < 0.001) and the VO2 increased from 9.9 to 13.8 mL kg 1 min 1 (P = 0.001). The 3 scoliosis groups did not differ in these energetic parameters [16]. However, in another study, VO2 was reduced in scoliosis patients [41]. Wallace et al. reported no significant differences between control and AIS groups in VO2 during gait [40]. Two studies found no difference in the 2 parameters evaluating HR, RR, and PCI during walking in scoliosis patients [22,41]. dos Santos Alves et al. showed significantly higher mean HR and RR as well as lower oxygen saturation and shorter distances on the 6-min walk test for AIS patients than healthy controls [17].

prolonged activation timing of the lumbar and pelvic muscles [6], compensation mechanism of the upper body balance because of geometric asymmetry of spine in lateral direction deformation and the misalignment of spine muscles [29]. Scoliosis patients with reduced sagittal hip motion during mid-stance phase lift the hip joint more than do healthy participants during gait [33]. In addition, in patients with oblique pelvis position resulting from a difference in the length of the lower limbs or transverse pelvic rotation, the compensatory mechanisms is activated to level the pelvis in the frontal plane during gait. These mechanisms involve primarily asymmetrical flexion of the knee joints during stance, as well as premature heel rise during stance of the functionally longer limb [32]. Moreover, lowering the ROM of pelvic might change the coordination between the thorax and pelvic in patients with idiopathic scoliosis [6]. Therefore, clinicians must consider that differences in the kinematics of the spine, pelvic, and lower extremities during gait might contribute to the progression of CA in AIS. The absence of side-to-side asymmetry for segmental kinematic data may be explained as a global phenomenon characterized by bilateral disturbances and malalignment of spine muscles. Scoliosis deformity produces asymmetrical trunk rotation, thereby resulting in an asymmetrical load on the spine, which could lead to altered body center of body mass (COM) position during walking [6,19,20,29].

4. Discussion

4.3. Kinetic parameters

We selected for review 33 studies investigating the effect of scoliosis deformity on gait parameters and energy expenditure during walking. Most of the studies concluded no significant differences in walking speed, cadence and step width in scoliosis patients and healthy controls. However, patients showed decreased hip and pelvic motion, excessive energy cost of walking, stepping pattern asymmetry and ground reaction force asymmetry. Further studies are needed to draw firm conclusions.

The spinal deformity relates to decreasing mediolateral forces of the hip. This reduced force can be explained by the decreased muscle efficiency that results from the longer contraction time of the lumbar and pelvic muscles. The reduced mediolateral force at the hip corresponds to a postural adjustment balancing the increased pelvic moment generated by the mediolateral shift of the thoracic mass during walking [34]. The GRF data indicate that scoliosis patients showed an asymmetrical gait as compared with healthy controls in the vertical [14,15] and mediolateral GRF components [12,19] and also stepping patterns (lateral and forward stepping) [36–38]. The asymmetrical gait in scoliotic children may be due to changes in global postural control strategies caused by spine deformation [19] and to changes in the sensory [9] and/or somatosensory systems [44–46].

4.1. Temporal spatial parameters The effect of altered speed of walking, stride length, and cadence on the AIS patients was contradictory among the studies. Several authors reported no changes in walking speed [13,19–27], cadence [6,11,13,19,20,23–27] and stride length [19,23,24, 26,27,29] for scoliosis patients as compared with normal controls, whereas other studies found reduced speed [9–11], stride length [6,9–11,13,20] and cadence [29]. These contradictory results might be due to differences in severity of spinal deformity [24,31], curve location in the spine [24], and postural stability control of body center for AIS patients [29] among the studies. Some possible explanations for reduced walking speed in scoliosis patients include trunk movement asymmetry [20], decreased balance control [42,43] or adaptive strategy used by AIS patients in response to balance difficulty [9], increased energy cost of locomotion [16] and resulting decreased efficiency of the gait cycle [11]. Moreover, temporal spatial variables decrease with an increase in CA [30,31]. 4.2. Kinematic parameters Several authors have highlighted that AIS patients show decreased frontal and transverse pelvis motion [6,10,32], decreased transversal and frontal hip motion [6,29], decreased sagittal hip motion [32,33], and decreased sagittal knee motion [6] as compared with normal people. Possible explanations for these findings include stiffness of the spine deformation, bilateral

4.4. Mechanical work and energy expenditure During gait, humans move their COM up and down at each step. Hip and pelvic motions in the frontal plane are the main determinants that minimize the vertical displacement of the COM [47], allowing for optimal mechanical work during walking [47], and therefore reduced energy consumption [48]. Walking with a muscular mechanical work that is lower or higher than the normal limit increases the energy cost of the walking [49]. The energy expenditure of walking may increase because of prolonged activation timing of the lumbo-pelvic and pelvic-femoral muscles [13]. In contrast, Mahaudens et al. reported low muscular mechanical work positively related to reduced vertical displacement of the COM and reduced hip and pelvic motions [16]. Moreover, adolescents with idiopathic scoliosis have reduced muscle strength [50], which could explain the poorer performance of these patients, thereby causing shorter distances, increased HR, RR, and VO2 [17]. Likewise, the results of some studies showed no difference in energy expenditure between scoliosis and normal groups [22,40]. These contradictory results might be due to the difference in severity of spinal deformity [22] and measurement methods of energy expenditure [40].

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5. Conclusions We lack consensus on the effect of the scoliosis on temporal spatial parameters when comparing AIS patients and healthy controls, but the literature showed some kinetic and kinematic changes in AIS patients, including lower hip force, asymmetrical lateral stepping, decreased hip and pelvic ROM, especially in frontal and transverse planes, and GRF asymmetry. However, further research is needed to assess the effect of scoliosis on gait and energy consumption. Future studies should investigate the effect of scoliosis on COM displacement, energy cost and spinal deformity in scoliotic patients. As well, electromyography, not investigated for this article, could be examined during walking in people with AIS. Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. Disclosure of interest The authors declare that they have no competing interest. References [1] Weinstein SL, Dolan LA, Cheng JC, Danielsson A, Morcuende JA. Adolescent idiopathic scoliosis. Lancet 2008;371:1527–37. [2] Negrini S, Grivas TB, Kotwicki T, Maruyama T, Rigo M, Weiss HR. Why do we treat adolescent idiopathic scoliosis? What we want to obtain and to avoid for our patients. SOSORT 2005 Consensus paper. Scoliosis 2006;1:4. [3] Pehrsson K, Danielsson A, Nachemson A. Pulmonary function in adolescent idiopathic scoliosis: a 25 year follow up after surgery or start of brace treatment. Thorax 2001;56:388–93. [4] Danielsson AJ, Nachemson AL. Radiologic findings and curve progression 22 years after treatment for adolescent idiopathic scoliosis: comparison of brace and surgical treatment with matching control group of straight individuals. Spine 2001;26:516–25. [5] Danielsson AJ, Nachemson AL. Back pain and function 22 years after brace treatment for adolescent idiopathic scoliosis: a case-control study—part I. Spine 2003;28:2078–85. [6] Mahaudens P, Banse X, Mousny M, Detrembleur C. Gait in adolescent idiopathic scoliosis: kinematics and electromyographic analysis. Eur Spine J 2009;18:512–21. [7] Mayo NE, Goldberg MS, Poitras B, Scott S, Hanley J. The Ste-Justine adolescent idiopathic scoliosis cohort study: part III: back pain. Spine 1994;19:1573–81. [8] Thorstensson A, Nilsson J, Carlson H, Zomlefer MR. Trunk movements in human locomotion. Acta Physiol Scand 1984;121:9–22. [9] Mallau S, Bollini G, Jouve J-L, Assaiante C. Locomotor skills and balance strategies in adolescents idiopathic scoliosis. Spine 2007;32:E14–22. [10] Park H-J, Sim T, Suh S-W, Yang JH, Koo H, Mun JH. Analysis of coordination between thoracic and pelvic kinematic movements during gait in adolescents with idiopathic scoliosis. Eur Spine J 2016;25:385–94. [11] Haber CK, Sacco M. Scoliosis: lower limb asymmetries during the gait cycle. Arch Physiother 2015;5:1. [12] Giakas G, Baltzopoulos V, Dangerfield PH, Dorgan JC, Dalmira S. Comparison of gait patterns between healthy and scoliotic patients using time and frequency domain analysis of ground reaction forces. Spine 1996;21:2235–42. [13] Mahaudens P, Thonnard J-L, Detrembleur C. Influence of structural pelvic disorders during standing and walking in adolescents with idiopathic scoliosis. Spine J 2005;5:427–33. [14] Schizas C, Kramers-de Quervain I, Stu¨ssi E, Grob D. Gait asymmetries in patients with idiopathic scoliosis using vertical forces measurement only. Eur Spine J 1998;7:95–8. [15] Chockalingam N, Dangerfield PH, Rahmatalla A, Ahmed E-N, Cochrane T. Assessment of ground reaction force during scoliotic gait. Eur Spine J 2004;13:750–4. [16] Mahaudens P, Detrembleur C, Mousny M, Banse X. Gait in adolescent idiopathic scoliosis: energy cost analysis. Eur Spine J 2009;18:1160–8. [17] dos Santos Alves VL, Avanzi O. Objective assessment of the cardiorespiratory function of adolescents with idiopathic scoliosis through the six-minute walk test. Spine 2009;34:E926–9. [18] Perry J, Davids JR. Gait analysis: normal and pathological function. J Pediatr Orthop 1992;12:815. [19] Yang JH, Suh S-W, Sung PS, Park W-H. Asymmetrical gait in adolescents with idiopathic scoliosis. Eur Spine J 2013;22:2407–13. [20] Kramers-de Quervain IA, Mu¨ller R, Stacoff A, Grob D, Stu¨ssi E. Gait analysis in patients with idiopathic scoliosis. Eur Spine J 2004;13:449–56.

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Please cite this article in press as: Daryabor A, et al. Gait and energy consumption in adolescent idiopathic scoliosis: A literature review. Ann Phys Rehabil Med (2016), http://dx.doi.org/10.1016/j.rehab.2016.10.008