Basic Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Orthop. Mar 18, 2017; 8(3): 256-263
Published online Mar 18, 2017. doi: 10.5312/wjo.v8.i3.256
Spinal alignment evolution with age: A prospective gait analysis study
Sébastien Pesenti, Benjamin Blondel, Emilie Peltier, Elke Viehweger, Vincent Pomero, Guillaume Authier, Stéphane Fuentes, Jean-Luc Jouve
Sébastien Pesenti, Emilie Peltier, Jean-Luc Jouve, Pediatric orthopedics, Timone Enfants, Aix-Marseille University, 13005 Marseille, France
Sébastien Pesenti, Institute of Movement Sciences (CNRS UMR 7287), 13288 Marseille, France
Benjamin Blondel, Gait Analysis Laboratory, Hopital Timone Enfants, Aix-Marseille University, 13005 Marseille, France
Benjamin Blondel, Spine Unit, Hôpital de la Timone, 13005 Marseille, France
Elke Viehweger, Vincent Pomero, Guillaume Authier, Spine unit, Timone, Aix-Marseille University, 13005 Marseille, France
Stéphane Fuentes, Neurosurgery, Timone Enfants, Aix-Marseille University, 13005 Marseille, France
Author contributions: All authors contributed equally to this work.
Institutional review board statement: The Spine unit review board reviewed this study and gave his approval.
Institutional animal care and use committee statement: No animal has been involved in this study.
Conflict-of-interest statement: No conflict of interest.
Data sharing statement: Authors agreed to share data with the editor.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Benjamin Blondel, MD, PhD, Spine Unit, Hôpital de la Timone, 264 rue Saint Pierre, 13005 Marseille, France. benjamin.blondel@ap-hm.fr
Telephone: +33-4-91384430 Fax: +33-4-91384247
Received: July 25, 2016
Peer-review started: July 29, 2016
First decision: September 2, 2016
Revised: November 10, 2016
Accepted: December 27, 2016
Article in press: December 28, 2016
Published online: March 18, 2017

Abstract
AIM

To describe, using gait analysis, the development of spinal motion in the growing child.

METHODS

Thirty-six healthy children aged from 3 to 16 years old were included in this study for a gait analysis (9 m-walk). Various kinematic parameters were recorded and analyzed such as thoracic angle (TA), lumbar angle (LA) and sagittal vertical axis (SVA). The kinetic parameters were the net reaction moments (N.m/kg) at the thoracolumbar and lumbosacral junctions.

RESULTS

TA and LA curves were not statistically correlated to the age (respectively, P = 0.32 and P = 0.41). SVA increased significantly with age (P < 0.001). Moments in sagittal plane at the lumbosacral junction were statistically correlated to the age (P = 0.003), underlining the fact that sagittal mechanical constraints at the lumbosacral junction increase with age. Moments in transversal plane at the thoracolumbar and lumbosacral junctions were statistically correlated to the age (P = 0.0002 and P = 0.0006), revealing that transversal mechanical constraints decrease with age.

CONCLUSION

The kinetic analysis showed that during growth, a decrease of torsional constraint occurs while an increase of sagittal constraint is observed. These changes in spine biomechanics are related to the crucial role of the trunk for bipedalism acquisition, allowing stabilization despite lower limbs immaturity. With the acquisition of mature gait, the spine will mainly undergo constraints in the sagittal plane.

Key Words: Sagittal balance, Spine biomechanics, Gait analysis, Thorcic kyphosis, Spine growth

Core tip: Many postural changes occur during childhood, including the adaptation of the spine to maintain an erect posture. The aim was to describe, using gait analysis, the development of spinal motion during growth. Various kinematic parameters were recorded in 36 healthy children. Thoracic kyphosis and lumbar lordosis were not found to increase during childhood whereas sagittal vertical axis increased with age. The kinetic analysis showed a decrease of torsional constraint while sagittal constraint increased. These changes in spine biomechanics are related to the crucial role of the trunk for bipedalism acquisition, allowing stabilization despite lower limbs immaturity.



INTRODUCTION

With the acquisition of bipedalism, many anatomical and postural changes occurred in humans[1-3]. Among these changes, an adaptation of the spine has been necessary to maintain an erect position, in combination with an adaptation of the pelvis and the lower limbs[4-6]. Although gait acquisition is apparently complete by the age of 3, adaptation to erect posture continues until the end of growth. According to Peterson et al[7], mature gait patterns are visible in children only from the age of 12.

With the development of modern tools for gait analysis, it is possible to obtain a precise evaluation of the kinematic and kinetic for different segments of the human body. While many of these tools have been developed for lower limbs analysis, various authors have demonstrated their accuracy for trunk dynamic analysis[8-10]. Many studies have described the evolution of spinal curvatures with radiological or other methods[11,12]. Using these tools, it has been shown that thoracic kyphosis and lumbar lordosis increase with age.

To our knowledge, there is no evidence in literature about this development using gait analysis tools. Moreover, gait analysis provides dynamic data such as constraints applied to spinal joints, these parameters having never been discussed in literature before. The hypothesis of this work was that spinal motion changes all along growth. The aim of this study was to describe, using gait analysis, the development of spinal motion in the growing child.

MATERIALS AND METHODS
Study design

To obtain a homogenous pediatric cohort, only healthy volunteers were included in this prospective study after informed consent. Inclusion criteria were children aged from 3 to 16 years old, without known disease and volunteers to participate to the study. Exclusion criteria were every history of orthopedic or neurologic disorders, major orthopedic trauma or allergy to the components used for gait analysis.

Anthropometric data

For each participant, the following anthropometric data were collected for gait analysis: Age, weight, height, lower limb length and knee and ankle diameters.

Gait analysis

All measurements were obtained using an optoelectronic system (Vicon, Oxford, United Kingdom) with six high-resolution cameras with infrared light and a sampling frequency of 100 Hz which recorded the position of passive retroreflective markers and two force platforms (AMTI, United States). This protocol included all the markers necessary to obtain parameters of a standing posture and to calculate the force of external efforts in the different intersegmental centers, as described by Blondel et al[13], according to the International Society of Biomechanics[14,15].

Subjects were equipped with a set of 28 retroflective markers as described in Table 1 and Figure 1. These markers allowed an analysis of different body segments such as head and neck, the scapular girdle, the thorax and thoracic spine, the abdomen and lumbar spine, the pelvis and the lower limbs.

Table 1 Optoelectronic markers placement following anatomical landmarks according to Blondel et al[13] gait analysis protocol.
Parameters
HeadVertex: 1
Nasion: 1
Tragus: 2
Trunk - thoraxAcromion: 2
Manubrium: 1
Xiphoid: 1
C7: 1
T6: 1
T9: 1
Trunk - abdomenT12: 1
L3: 1
S1: 1
PelvisASIS: 2
Lower limbs - thighsFemoral shaft: 2
Lateral femoral condyle: 2
Lower limbs - legsTibial shaft: 2
Lateral malleolus: 2
Lower limb - feetCalcaneus: 2
2nd metatarsal head: 2
Figure 1
Figure 1 Gait analysis model used for trunk motion assessment. Retroflective markers were placed according to anatomical landmarks, such as described by Blondel et al[13] (Table 1). Six markers were used for spine motion.

Before the beginning of gait analysis, a short trial was performed to check the good positioning of the markers according to the analysis of knee valgus/varus[16].

For gait analysis, subjects were asked to walk at a self-selected speed, barefoot, on a flat and straight 9 m-walkway. A minimum of seven trials was recorded to collect kinematic and kinetic data.

The data collected by the 6 high-resolution cameras were converted into a 3D model using NEXUS software (Vicon Motion Systems, Oxford, United Kingdom) for the lower limbs and data were integrated to MATLAB software for trunk analysis.

The characteristic moments of the beginning and the end of the double stance phase were used to compare subjects.

For kinetic analysis, calculations were made from anthropometric reference tables[17].

Gait parameters

Kinematic parameters during gait are described hereafter and summarized in Table 2 and Figure 2: (1) Sagittal Vertical Axis Adimensioned (SVA Ad): distance between the marker “S1” and the vertical line passing by the marker “C7”. This value was weighted by the height of the subject to be comparable between subjects, regardless to age and height (SVA Ad=SVA/Height). This parameter reflects trunk position during gait: A great value of SVA indicates that the trunk is leaning forward; (2) angle pelvis-acromion (APA): Angle defined in the transverse plane between the line joining the 2 “Acromion” markers and the line joining the 2 “anterosuperior iliac spine” markers. The APA-rom (range of motion) was calculated as the difference between the maximum and the minimum values of the APA during a gait cycle[18]; (3) thoracic angle (TA): Angle between the “C7”-“T7” line and the “T9”-“T12” line; and (4) lumbar Angle (LA): Angle between the “T12”-“L3” line and the “L3”-“S1” line.

Table 2 Kinematic parameters measured during gait analysis.
FrontalSagittalTransversal
Overall balanceSVA Ad
ShouldersAPA
Thoracic spineTA
Lumbar spineLA
PelvisPelvic version
Lower limbsKnee Varus/valgusHip flex/ext
Knee flex/ext
Figure 2
Figure 2 Sagittal vertical axis and angle pelvis-acromion. A: SVA was defined as the distance between the marker “S1” and the vertical line passing by the marker “C7”. This parameter reflects trunk position during gait: A great value of SVA indicates that the trunk is leaning forward; B: APA was defined as the angle between the line joining the 2 “Acromion” markers and the line joining the 2 “anterosuperior iliac spine” markers. SVA: Sagittal vertical axis; APA: Angle pelvis-acromion.

Kinetic parameters are detailed in Table 3. In frontal plane, moments applied to the spine are relative to lateral bending movements, in sagittal plane they are flexion-extension movements and in transversal plane, they were consecutive to torsional movements. These data were dimensioned (i.e., divided by the weight) to be comparable between individuals, independently from their body mass.

Table 3 Kinetic parameters measured during gait analysis.
Frontal momentsSagittal momentsTransversal moments
Thoracolumbar junctionLateral bendingFlexion-extensionTorsion
Lumbosacral junctionLateral bendingFlexion-extensionTorsion
Statistical analysis

Gait data were analyzed to compare subjects in a continuous analysis according to age. A Pearson Product Moment Correlation Coefficient (r) was used to determine differences between subjects according to age. Level of significance was set at 5% for every statistical analysis.

RESULTS
Demographic data

From October 2012 to October 2013, 36 subjects were included in this study. Mean age of the population was 8.8 years old (3.3 to 15.6 years old). Demographic and anthropometric data are shown in Table 4.

Table 4 Details of demographic and anthropometric data.
Subject No.SexAge (yr)Height (cm)Weight (kg)Lower limb length (cm)
Knee diameter (cm)
Ankle diameter (cm)
RightLeftRightLeftRightLeft
1F3.38801142042055554545
2F3.410601751051080806060
3M3.99351450050070704444
4F3.910501952052080806060
5M4.110801855055070705050
6F4.610901665065050504545
7F5.811351957057070705050
8M6.111501957557580806060
9F7.013452767067090906565
10F7.212002157057070705050
11F7.411602158558580806060
12M7.71370347307301101107070
13F7.713003168068095957070
14F7.812802665065090907070
15M8.013402768068090907070
16M8.113302868568595956565
17M8.513603371071090905555
18M8.81400407207201101107070
19F8.91380377207201001006565
20M9.113202468068080806060
21M9.214202675076055555050
22F9.31524388208201001006565
23M9.51395367507501101056565
24F10.013602971071070705555
25F10.613703974074095956060
26F10.814253275075090906565
27F11.01530418108101051057070
28M11.11520518508501001007070
29F11.11463477407401051057070
30F11.31610468408401051057080
31M11.913903470070085856060
32F12.51470357407401001007070
33F12.71570549009001151107570
34F13.91690479259251001007070
35M15.516504883083085856565
36M15.61770879309301001007070
Gait analysis: Kinematics

Sagittal plane: TA and LA curves were not statistically different (respectively, r = 0.06 and r = 0.023, P = 0.32 and P = 0.41, Figure 3).

Figure 3
Figure 3 Continuous analysis of kinematic parameters according to the age. A: TA; B: LA; C: SVA. TA: Thoracic angle; LA: Lumbar angle; SVA: Sagittal vertical axis.

SVA Ad was significantly correlated to the age (r = 0.488, P < 0.001), revealing a progressive anterior increase of the projection of the C7 marker with regards to the S1 marker (Figure 4).

Figure 4
Figure 4 Continuous analysis of angle pelvis-acromion-rom according to the age. APA: Angle pelvis-acromion.

Transversal plane: There was a non-significant negative correlation between APA-rom and age (r = -0.063, P = 0.71).

Gait analysis: Kinetics

Sagittal plane: Results showed that flexion-extension moments at the lumbosacral junction were statistically correlated to age (r = 0.356, P = 0.003). In other words, mechanical sagittal constraints at the lumbosacral junction increase during growth. At the thoracolumbar junction, sagittal constraints were not significantly correlated to age (r = 0.189, P = 0.13, Figure 5).

Figure 5
Figure 5 Sagittal kinetic parameters of the trunk according to the age. A: TL; B: LS. Frontal plane constraints are relative to flexion-extension movements. TL: Thoracolumbar; LS: Lumbosacral.

Transversal plane: Results demonstrated that torsion moments at thoracolumbar and lumbosacral junctions were statistically correlated to age (r = -0.613 and r = -0.563, P = 0.0002 and P = 0.0006). In other words, transversal mechanical constraints at thoracolumbar and lumbosacral junctions decrease with age (Figure 6).

Figure 6
Figure 6 Transversal kinetic parameters of the trunk according to the age (continuous analysis). Transversal plane constraints are relative to torsional movements of the trunk. TL: Thoracolumbar; LS: Lumbosacral.
DISCUSSION

This study is the first to analyze spinal motion in children via gait analysis tool. Changes occur in spine motion in children with the acquisition of a mature gait even if dynamic parameters of the spine during growth seem to be established before the age of 3.

So far, only few studies have studied dynamic development of the spine according to age via gait analysis[19]. The studies from Wagner et al[20] and Farfan[21] showed that the presence of a lumbar spinal curvature concave toward the back is a necessary biomechanical condition for a stable erect posture, enabling an economic muscular functioning despite the posterior position of the spine. Lumbar lordosis thus appears as being a fundamental prerequisite to bipedalism, explaining its early appearance during childhood. Parameters determining bipedalism are acquired very early during growth[21,22]. However, some skeletal parameters which are not involved in the acquisition of bipedalism are variable and change until the end of growth. Some of these parameters are even found to be genetically predetermined during fetal life. This is, for example, the case of the morphology of the femoral trochlea[23] or the lumbar lordosis[24], which are genetically predetermined in humans. Their early kinematic setting is an element explaining the ability to bipedalism.

The spine appears to be of fundamental importance in the adaptation of the skeleton to bipedalism and we can define a real “spinal motor of bipedalism”; the spine being the first skeletal element to adjust its posture and functioning to bipedalism as the main element of locomotion[25]. The lower limbs adapt secondarily, around the age of 7, with a progressive pelvic anteversion, a progressive extension of the hips and the knees, lately mature.

Some radiographic and morphologic studies have evaluated the development of spinal curvatures during growth[11,12]. These studies revealed that from the age of 3 years until skeletal maturity, there is a linear enhancement of the thoracic kyphosis and lumbar lordosis. According to us, these changes do not reflect the adaptation of the skeleton to bipedalism, but an adaptation to the major constraints applied to the trunk during growth. In other words, formation of overlying sagittal curvatures to the lumbar lordosis with the appearance of thoracic kyphosis and cervical lordosis is related to biomechanical adaptation to an increase of load on the spine.

Most of the parameters used in this study for kinematic analysis, such as SVA, were chosen according to previous works[18]. These parameters seemed to be good descriptors because they are the dynamic equivalent of radiographic parameters. Thoracic angle and lumbar angle were meant to be the equivalent of thoracic kyphosis and lumbar lordosis, which are 2 radiographic parameters used in clinical practice.

Results from this study suggest that the sagittal efforts applied on the spine increase significantly with age leading to increased flexion-extension constraints at the lumbosacral junction. This phenomenon can be explained by the accentuation of spinal curvatures with age as a response to the increased load on the spine, deporting the lumbar spine forward and thereby increasing the lever arm and the moment applied to the underlying lumbosacral junction.

With regards to the kinetic parameters in the transverse plane, our results showed a significant reduction in torsional constraints at the thoracolumbar and lumbosacral junctions during growth. Although lumbar lordosis is acquired from fetal life, the central maturation processes coordinating the acquisition of a mature gait for the lower limbs appear only around the age of 7. Before this turning point, the lower limbs do not have a mature kinematics allowing balance and stability for satisfactory and stable erect posture. These results are in line with the posturographic study from Peterson et al[7] who have shown that sensory systems ensuring a satisfactory balance for maintaining erect station were efficient only from the age of 12. Thus, the spine undergoes greater constraints to compensate this permanent balance research. Large constraints applied to the spine and their reduction with age are a sign of the compensation by the trunk of a lack of stability due to lower limbs and sensory system immaturity. Prior to the acquisition of a definitive and mature bipedalism, the trunk is fundamental for the possibility of early bipedalism.

Furthermore, the significant increase of SVA during growth could be related to the same conclusion. The low value of SVA in young children reflects the need to keep the shoulders over the pelvis to stabilize the erect posture. With maturation and the acquisition of a final biped balance, the subject is projected more forward, then changing the direction of the constraints on the spine from the transverse plane to the sagittal plane.

These findings allow a better comprehension of the importance of constraints in the lumbar spine and can be a source of explanation for specific degenerative disorders of this anatomical region.

The small number of subject in each age group may be at the origin of a lack of statistical power and may explain the lack of significant difference. However, in similar series, changes in lower limb parameters are clearly established, these parameters being definitively acquired after the age of 7[26-31]. The protocol used for trunk assessment has been validated before in the study by Blondel et al[13]. This protocol is designed for clinical use and a low number of markers is a clear advantage in that case. The authors have demonstrated that 6 markers were sufficient to assess trunk kinematics and kinetics precisely. Moreover, there was a wide amount of variability. Including a greater number of subjects may increase statistical power and allow to highlight differences in sagittal kinematic parameters.

The biomechanical model developed by Blondel et al[13] in adults has enabled us to achieve the first dynamic study of spine development with age. The comparison of age groups and continuous analysis did not highlight major kinematic evolution of spinal curvatures during skeletal maturation. The acquisition of the lumbar lordosis and thoracic kyphosis is a morphological characteristic that probably appears very early in children, before the age of 3.

The kinetic analysis revealed a progressive decrease in torsional constraints applied on the spine while the constraints in flexion-extension increase with age. These changes allow stabilization of erect posture despite the immaturity of the lower limbs. With the acquisition of mature gait, the spine will mainly undergo constraints in the sagittal plane. These changes point out the major role of the trunk during the acquisition of bipedalism.

COMMENTS
Background

Although gait acquisition is apparently complete by the age of 3, adaptation to erect posture continues until the end of growth. Many studies have described the evolution of spinal curvatures with radiological methods. Using gait analysis tools, it is possible to obtain a precise analysis of the evolution of spinal alignment with age.

Research frontiers

Even if the sample size is quite limited, this study provides interesting information about evolution of spinal dynamics with growth. This study may help to understand changes in gait in spinal disorders.

Innovations and breakthroughs

Results from this study confirm the technical feasibility of the protocol in young children. Using this methodology, it was possible to evaluate net moments applied to spinal junctions. To the authors’ knowledge, this the first study to provide dynamic data of the spine of healthy children.

Applications

By providing normative data, this study may help to understand the changes that occur in children with spinal disorders. It could also help to evaluate the behavior of the spine in children after spinal surgery.

Peer-review

Although the sample size is relatively small, this is an interesting study.

Footnotes

Manuscript source: Invited manuscript

Specialty type: Orthopedics

Country of origin: France

Peer-review report classification

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P- Reviewer: Peng BG, Teli MGA S- Editor: Kong JX L- Editor: A E- Editor: Li D

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