Eur Spine J (2014) 23:2626–2634 DOI 10.1007/s00586-014-3508-3
ORIGINAL ARTICLE
Altered head orientation patterns in children with idiopathic scoliosis in conditions with sensory conflict P. N. Eijgelaar • F. H. Wapstra • E. Otten A. G. Veldhuizen
•
Received: 22 April 2014 / Revised: 3 August 2014 / Accepted: 3 August 2014 / Published online: 17 August 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose Idiopathic scoliosis (IS) is the most common spinal deformity in adolescents. Defective postural equilibrium may be a contributing factor. The information of the three sensory systems combined enables the formation of a central representation of head position and body posture. Comparison of head angles of girls with and without scoliosis may result in a difference in head orientation. Methods 25 girls with IS and 16 girls without scoliosis (NS) between the age of 10–16 years stand in a special constructed box on a roll-tilting platform (tilt -14° to ?14°). Results NS and IS subjects behave quite similarly if there is no sensory conflict, but if there is conflict, the differences between the two groups are greater, especially within the 13- to 14-year-old category. Conclusions The differences between groups for different age categories suggest that the process of development of sensory integration for estimation of verticality appears to be different for girls with scoliosis. Keywords Idiopathic scoliosis Head orientation Perception of verticality Tilted room P. N. Eijgelaar Human Movement Sciences, Groningen, The Netherlands F. H. Wapstra A. G. Veldhuizen (&) Department of Orthopaedics, University Medical Center of Groningen, University of Groningen, Po.box: 30.001, 9700 RB Groningen, The Netherlands e-mail: [email protected] E. Otten Center for Human Movement Sciences, University Medical Center of Groningen, University of Groningen, Groningen, The Netherlands
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Introduction Idiopathic scoliosis (IS) is the most common spinal deformity in adolescents [1]. Although the ancient Greeks first made good anatomic descriptions of the structural changes seen in scoliosis, we have not as yet elucidated its pathogenesis. The deformity always develops from a straight spine into a curved spine, usually accompanied by a rib cage deformity, during the growth period in general, and in particular in the rapid growth period [2, 3]. Awareness of the position of the body in space is a highly developed sense in humans. The vestibular information is combined with incoming somatosensory and visual information, which enables the formation of a central representation of head position and body posture [4–6]. This representation is important in the maintenance of balance and therefore in the control of posture as well. With this sensory information, healthy subjects are able to determine the true vertical and horizontal, even when the head or body is tilted [7]. The functional ranges of the three systems overlap, so that they are able to compensate in part for each other’s deficiencies [8, 9]. Defective postural equilibrium has been proposed as a contributing factor in the development of scoliosis [10]. Several findings give reason to believe that patients with IS are less capable of making accurate estimations of verticality of their bodies. IS patients present perceptual impairments and deficits in sensorimotor adaptation, learning and balance control [1, 11]. These impairments are indicative of disorders at higher integrative levels of the central nervous system [11]. Since various patients with IS present longer somatosensory cortical potentials compared to healthy individuals, their balance instabilities could be associated with alteration in sensory signal processing [12].
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The occurrence of vestibular-related deficits in IS patients is well established [11, 13]. It is unclear whether a vestibular pathology is the common cause for the scoliotic syndrome and gaze and posture deficits, or if the latter behavioural deficits are a consequence of the scoliotic deformations. A possible vestibular origin was tested in the frog Xenopus laevis by unilateral removal of the labyrinthine end organs at larval stages. After metamorphosis into young adult frogs, X-ray images and three-dimensional reconstructed microcomputer tomographic scans of the skeleton showed deformations similar to those of scoliotic patients [14]. Furthermore, Wiener-Vacher and Mazda [15] found in their study that 66.7 % of the IS patients have greater asymmetry in their otolith responses than matched control subjects with congenital scoliosis or without scoliosis. Also, several studies examining vibratory sensitivity—which is used as an estimate of proprioceptive function—found a significant asymmetry between right and left detection thresholds in subjects with IS and/or a lower [16] or higher [17, 18] vibratory sensitivity in subjects with IS compared to healthy subjects, which could also be of influence in the estimation of verticality made by people with IS. The hypothesis is that patients with IS form their head orientations in a different manner from individuals without scoliosis. Whether the deviating aspect lies within the integration of the sensory systems or within one of the systems itself will not be answered directly by the outcome of this study; it mostly serves to answer the question whether individuals with IS do indeed have a different neural regulation for head position.
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Fig. 1 The experimental setting of condition 1. The subject is standing inside the tilting room on the platform. Condition 3 has the same circumstances minus the box and condition 4 equals condition 3 with eyes closed
Methods For this study, 25 girls with thoracic, thoracolumbar or lumbar IS (Cobb angle 33.5° ± 16°, age 13.5 ± 2) and 16 girls without scoliosis (NS) (age 13.2 ± 2) between the ages of 10–16 years stand in a special constructed box on a roll-tilting platform (tilt -14° to ?14°). Criteria for exclusion from the study are the presence of any vestibular disorders or motor impairments in an individual, and/or a height over 1.78 m. The box (112 9 112 9 180 cm) is constructed out of blackpainted wooden pergolas and white Chinese paper to obscure the outside world (Fig. 1). A Canon HF-100 HD digital video camera (with a frame rate frequency set at 25 Hz) is used to record the subjects on video while undergoing the experimental conditions (Figs. 1, 2). Protocol Markers are placed on the head cap (Fig. 3) and additional markers are placed on the box or on an upside down table
Fig. 2 The experimental setting of condition 2. The subject is sitting inside the tilting room, but is supported by a table that does not tilt along with the platform
(depending on the condition) to determine head and platform positions. The subjects were instructed to look straightforward and to relax and, if wearing a brace in daily life, to do so during the experiment. The following four conditions are investigated:
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Fig. 3 The positions of the markers on the subject’s cap
1.
2.
3.
4.
Inbox: subject is standing inside the box with her eyes open (the box and subject’s support surface are rolltilting along with the platform). Inbox sit: subject is sitting on the table inside the box with her eyes open (the box is roll-tilting along with the platform, but the subject’s support surface is not). Outbox open: subject is standing on the platform without the box with her eyes open (subject’s support surface is roll-tilting along with the platform). Outbox closed: subject is standing on the platform without the box with her eyes closed (subject’s support surface is roll-tilting along with the platform).
In 60 s the platform roll-tilts 14° to the right, stops, and tilts back to the 0° starting position, where it pauses shortly and then continues to tilt 14° to the left and then returns to the 0° position again. Half of the subjects start the cycle with roll-tilting to the right and half of them start roll-tilting to the left. Also, the order of conditions is varied per subject.
also used to calculate the mentioned cross-correlation coefficients, delays, and slopes and head angular velocities. For every subject in every condition, head angle graphs are used to determine what different behavioural patterns of head angles are present among subjects, and the subjects are categorised based on their head angle pattern. SPSS version 16.0 is used for concordance analysis between groups (NS and IS) and portrayed patterns and also within NS and IS groups between age categories (10–12, 13–14 and 15–16 years old) and portrayed patterns. Furthermore, multivariate analysis of variance (MANOVA) is conducted between groups for every condition for dependent variables’ cross-correlation coefficient, delay, slope and head angular velocity and repeated measures MANOVAs between and within groups over all conditions. The effects of hand preference and age category are determined for both groups, and for the IS group the effects of convexity (right, left and right/left), location (thoracic, lumbar and thoraco-lumbar) and Cobb angle (B40° and [40°) are also determined. If a significant effect of any of these betweensubjects factors is found, and the factor has at least three categories, a post hoc test with Bonferroni correction is conducted to determine between which of the categories the variables are significantly different.
Results Analysis of head angle conducts provides us with six categories of head angle patterns:
Variables 1. The video recordings provide us with footage of the marker positions of the head cap worn by the subjects. These video recordings are converted into mp4-files, which are entered into the analysis program Nbody Project A, written especially for this study. This software is used to track the marker positions of the head cap and these positions are used for calculating head angles. The platform angle is calculated using markers at the edges of the box (condition 1 and 2) or markers at the legs of an upside down table on the platform (condition 3 and 4). Cross-correlation and delay between the platform angle and head angle are calculated and used as measures to describe characteristic behaviour of subjects in all conditions in terms of accuracy and delay of coupling, respectively. Two other measures calculated are slope of the head angle signal and average head angular velocity.
2.
Static: the head angle does not follow the platform angle, but remains close to zero. (Fig. 4) (Partially) trailing: the head angle follows the platform angle during both the leftward and rightward tilts, albeit to different extents. (Fig. 5)
Data analysis The marker positions signals are filtered with a 2 Hz low pass zero lag filter, using Matlab version 2007b. Matlab is
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Fig. 4 Static head angle signal (condition 2 for NS 2, age 15 years old)
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Fig. 5 Trailing head angle signal (condition 1 for IS 23; Cobb angle 20°, age 15 years)
Fig. 7 Delayed trailing head angle signal (condition 1 for IS 12; Cobb angle 43°, age 10 years old)
Fig. 6 Partially trailing head angle signal (condition 2 for NS 6, age 14 years old)
Fig. 8 Leading head angle signal (condition 3 for IS 16; Cobb angle 40°, age 11 years old)
3.
4.
5.
6.
Delayed trailing: the head angle remains close to zero, until the platform reaches a certain angle, at which point the head angle starts to follow the platform angle. This is the case in both leftward and rightward tilts. (Fig. 6) Leading: the head angle follows the platform angle; however, around or shortly before reaching the maximum platform angle, the head angle starts decreasing before the platform angle does. This is the case in both leftward and rightward tilts. (Fig. 7) Mirroring: as the platform angle increases towards one side and decreases again, the head angle increases towards the opposite side and decreases again. This is the case in both leftward and rightward tilts. (Fig. 8) Residual: no specific head angle pattern. (Fig. 9)
Fig. 9 Mirroring head angle signal (condition 3 for IS 19; Cobb angle 25°, age 14 years old)
Condition 1: inbox Descriptive statistics See Tables 1 and 2.
All subjects—of both the NS and IS groups—show a (partially) trailing pattern. None of the dependent variables
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Table 1 Frequencies of head angle patterns in NS and IS groups and among different age groups NS All
IS 10–12 years
13–14 years
15–16 years
All
10–12 years
13–14 years
15–16 years
Condition 1 N
16
6
7
3
25
11
6
8
(Partially) trailinga
100.0
100.0
100.0
100.0
88.0
100.0
50.0
100.0
Otherb
0.0
0.0
0.0
0.0
12.0
0.0
50.0
0.0
Condition 2 N
15
6
6
3
25
11
6
8
Staticc (Partially) trailinga
40.0 33.3
0.0 50.0
33.3 33.3
66.7 33.3
28.0 24.0
9.1 27.3
83.3 0.0
12.5 37.5
Delayed trailingd
13.3
33.3
16.7
0.0
32.0
36.4
16.7
37.5
Otherb
13.3
16.7
16.7
0.0
16.0
27.3
0.0
12.5
Condition 3 N
16
6
7
3
25
11
6
8
Staticc
18.8
0.0
14.3
66.7
20.0
9.1
16.7
37.5
Leadinge
50.0
50.0
57.1
33.3
48.0
72.7
50.0
12.5
Mirrorringf
31.2
50.0
28.6
0.0
20.0
9.1
33.3
25.0
Otherb
0.0
0.0
0.0
0.0
12.0
9.1
0.0
25.0
Condition 4 N
16
6
7
3
25
11
6
8
Leadinge
81.2
83.3
71.4
100.0
80.0
81.8
83.3
75.0
Otherb
18.8
16.7
28.6
0.0
20.0
18.2
16.7
25.0
Frequencies are displayed in percentages NS no scoliosis, IS idiopathic scoliosis a
The head angle follows the platform angle during both the leftward and rightward tilt, albeit to different extents
b
The subjects show no specific pattern
c
The head angle does not follow the platform angle, but remains close to zero
d
The head angle remains close to zero, until the platform reaches a certain angle, at which point, the head angle starts to follow the platform angle
e
The head angle follows the platform angle, until around or shortly before reaching the maximum platform angle, at which point the head angle starts decreasing before the platform angle does
f
As the platform angle increases towards the one side and decreases again, the head angle increases towards the other side and decreases again
are significantly different between the NS and IS groups. In the IS group, age appears to be a significant factor in conduct; the 13- to 14-year category has a significantly lower right cross-correlation (p = 0.002 and p = 0.005, respectively) and smaller right slope (p = 0.026 and p = 0.039, respectively) than the 10- to 12-year and 15- to 16-year age categories. Their average head angular velocity, on the other hand, is greater, which, all together, implies that their head angle signals are noisier than the other two categories. Head angle graphs confirm this: although all subjects follow a pattern roughly similar to that of Fig. 5, 10 shows the variation on this, which three out of the six 13- to 14-year-olds of the IS group show. Note that—in all three cases—the sudden switch of the head angle towards the other side as the platform angle approaches its maximum only happens when the roll-tilt of
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the platform is to the right. Besides being 14 years old, these three subjects have in common that they are all righthanded. Their convexities, locations of the scoliosis and Cobb angles are of various categories. Condition 2: inbox sit In condition 2, subjects can be categorised into four groups of head angle patterns: static (Fig. 4), partially trailing (Fig. 6), delayed trailing (Fig. 7) and residual patterns. Subjects in the NS group tend towards the static pattern (40.0 %), while the main pattern in the IS group is the delayed trailing pattern (32.0 %). Correspondence analysis shows that little correspondence exists between age category and head angle pattern within the NS group (v2 = 1.667, p = 0.948), while, on the other hand, great
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Table 2 Descriptive statistics of cross-correlations between head angles and platform angles for NS and IS groups and for different age categories within the NS and IS groups NS
IS a
N
Overall
16
0.955 ± 0.08
Left
b
N
Overalla
Leftb
Rightc
0.970 ± 0.06
25
0.941 ± 0.06
0.952 ± 0.04
0.943 ± 0.10
Right
c
Condition 1 All categories
0.957 ± 0.08
Age category 10–12 years
6
0.972 ± 0.02
0.976 ± 0.02
0.982 ± 0.02
11
0.947 ± 0.05
0.948 ± 0.05
0.967 ± 0.06
13–14 years
7
0.930 ± 0.12
0.933 ± 0.11
0.950 ± 0.09
6
0.905 ± 0.09
0.945 ± 0.04
0.861 ± 0.17
15–16 years
3
0.981 ± 0.01
0.976 ± 0.01
0.991 ± 0.01
8
0.960 ± 0.03
0.964 ± 0.04
0.972 ± 0.02
15
0.825 ± 0.10
0.821 ± 0.15
0.823 ± 0.15
25
0.795 ± 0.17
0.801 ± 0.16
0.821 ± 0.24
Condition 2 All categories Age category 10–12 years
6
0.837 ± 0.08
0.819 ± 0.13
0.837 ± 0.20
11
0.834 ± 0.11
0.830 ± 0.13
0.896 ± 0.09
13–14 years
6
0.818 ± 0.12
0.862 ± 0.08
0.817 ± 0.12
6
0.656 ± 0.26
0.662 ± 0.22
0.610 ± 0.38
15–16 years
3
0.815 ± 0.14
0.742 ± 0.28
0.806 ± 0.17
8
0.828 ± 0.12
0.833 ± 0.12
0.843 ± 0.18
16
0.645 ± 0.21
0.625 ± 0.34
0.511 ± 0.36
25
0.636 ± 0.20
0.551 ± 0.32
0.531 ± 0.30
6
0.601 ± 0.23
0.611 ± 0.40
0.413 ± 0.40
11
0.665 ± 0.21
0.621 ± 0.29
0.591 ± 0.29
Condition 3 All categories Age category 10–12 years 13–14 years
7
0.690 ± 0.20
0.678 ± 0.34
0.623 ± 0.34
6
0.621 ± 0.18
0.507 ± 0.24
0.471 ± 0.21
15–16 years Condition 4
3
0.630 ± 0.26
0.538 ± 0.39
0.481 ± 0.38
8
0.630 ± 0.20
0.493 ± 0.35
0.508 ± 0.32
All categories
16
0.739 ± 0.23
0.802 ± 0.23
0.703 ± 0.28
25
0.777 ± 0.20
0.772 ± 0.25
0.753 ± 0.25
Age category 10–12 years
6
0.752 ± 0.23
0.810 ± 0.19
0.687 ± 0.32
11
0.805 ± 0.21
0.758 ± 0.33
0.764 ± 0.29
13–14 years
7
0.711 ± 0.26
0.796 ± 0.27
0.684 ± 0.29
6
0.722 ± 0.22
0.731 ± 0.24
0.712 ± 0.23
15–16 years
3
0.777 ± 0.25
0.801 ± 0.28
0.779 ± 0.27
8
0.840 ± 0.17
0.867 ± 0.13
0.823 ± 0.21
NS no scoliosis, IS idiopathic scoliosis a
Cross-correlations between head angles and platform angles over whole cycles
b
Cross-correlations between head angles and platform angles over the left half cycles
c
Cross-correlations between head angles and platform angles over the right half cycles
correspondence exists between age group and head angle pattern within the IS group (v2 = 13.225; p = 0.040). In the IS group, five out of seven static pattern subjects are in the 13- to 14-year category. Post hoc tests confirm that, within the IS group, the 13- to 14-year subjects show significantly smaller cross-correlations than the 15- to 16-year category (p = 0.033) and their cross-correlations are smaller, although not significantly smaller, than those of the 10- to 12-year category (p = 0.055). All of the static group subjects are right-handed, but are of various convexity, location and Cobb angle categories (Fig. 5).
Fig. 10 Head angle signal in condition 1 for subject IS11 (Cobb angle 60°, age 14 years old). The pattern of this signal resembles the patterns of three head angle signals of the 13- to 14-year group of the IS (idiopathic scoliosis) group in condition 1
Condition 3: outbox open Analysis of the head and platform signals allows us to divide the subjects into four categories based on their
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behaviours: static (Fig. 4), leading (Fig. 8), mirroring (Fig. 9) and residual patterns. In both groups, the 15- to 16-year-olds tend towards the static pattern (for NS and IS, 66.7 and 37.5 %, respectively). For the IS group, the majority (72.7 %) of the 10- to 12-year group shows the leading pattern, as does a great share of the 13- to 14-year group (50.0 %). In the NS group, 10- to 12-year-olds show either the leading pattern (50.0 %) or the mirroring pattern (50.0 %), as does the major share of the 13- to 14-year-olds (57.1 and 14.3 %, respectively). Although the correspondence between age group and head angle pattern is considerable, analysis shows that it is not significant (v2 = 6.740, p = 0.346 for NS and v2 = 8.632, p = 0.195 for IS). Differences in patterns between the NS and IS groups are relatively small and multivariate and univariate tests do not show any significant differences between the two groups for any of the dependent variables. Condition 4: outbox closed Condition 4 shows a lot of similarities to condition 3. In condition 4, however, the variance between the subjects is smaller. Most subjects (13 out 16 NS subjects and 20 out of 25 IS subjects) show the leading pattern. Delays of head angle signals confirm that the leading pattern is the main pattern in this condition; both the NS and the IS group show great positive delays, indicating that the head angle precedes the platform angle. However, in the IS group, the 13- to 14-year group shows negative overall, left and right delays, and in the NS group this also is the case for the 15to 16-year group. Multivariate and univariate tests do not show any significant differences for any of the dependent variables between the two groups. Comparison of conditions Some correspondence exists between patterns shown in one condition and those in another condition. For example, 9 out of 13 subjects, showing the static pattern in condition 2, show the leading pattern in condition 3. Also, NS subjects belonging to the residual group in condition 4 show the mirroring pattern in condition 3. For the IS group, residual pattern subjects in condition 4 show either the static, mirroring or residual pattern in condition 3. For both groups, it can be stated that if subjects show the leading pattern in condition 3, they also show the leading pattern in condition 4. All but one static pattern subjects in condition 3 also show the leading pattern in condition 4. Correspondence analysis shows that great correspondence exists between patterns in condition 3 and condition 4 (v2 = 15.265, p = 0.002). Correspondences between patterns of other conditions are much smaller.
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Discussion In situations without sensory conflict, the differences in head angle patterns and dependent variables between NS and IS girls are relatively small. This indicates that, in these situations, the head orientations and presumably the formation of the head orientations are similar for NS and IS girls. When sensory inputs are in conflict with each other, differences between NS and IS groups are greater. In condition 1, the trailing pattern implies that the incorrect static visual information is dominant over the contradictory correct dynamic vestibular and somatosensory systems information, and in condition 2, trailing means that the incorrect dynamic visual information is dominant over the correct static vestibular and somatosensory systems information in determining the head angle. Somehow, the CNS judges the visual information as more reliable than the other two systems in these cases, even though it is actually the other way around. According to the literature, healthy adults primarily rely on somatosensory inputs for posture control in a wellpractised situation, like standing on a stable surface, and under normal sensory conditions, and only in novel situations, such as situations of sensory conflict, visual input becomes more important [19]. However, it is also stated that in those new situations, information provided by the vestibular system is used as a reference and intersensory conflict is resolved by suppressing input that is incongruent with this vestibular information [19]. This is not in agreement with these trailing patterns. Visual motion—in this case rotation of the visual field—often leads to vection, which is the induced perception of self-motion, known to influence postural movement [20]. For most cases, the trailing of the platform angle by the head angle is only to a certain degree, which suggests that the suppression of the vestibular and somatosensory inputs is (partially) lifted at this point and determination of the head angle is based on a weighted combination of the three inputs. The vestibular cortex interacts with the visual cortex by means of reciprocal inhibitory visual–vestibular interaction for adequate self-motion perception [8]. This inhibitory interaction mechanism allows for a shift of the dominant sensorial weight during motion perception from one sensory modality to the other, depending on the prevailing mode of stimulation: acceleration (vestibular input) or constant velocity (visual input) or both [8]. When the platform angle reaches its maximum, the angle velocity of the rotation of the subject is no longer constant; it starts to decrease. When there is acceleration—which, in this case, is deceleration— contribution of vestibular input becomes increasingly important. In the IS group, we can see three 14-year-olds portraying deviating behaviour. One way to explain the sudden
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shift in the right half cycle is that the lift of suppression of the vestibular and somatosensory systems results in an E effect, which is the tendency by one to overcompensate for the body tilt, at moderate lateral body tilts up to 30°. This tilt leads the subjects to erroneously estimate the true vertical [5, 21]. This effect is the result of a dominance of visual–vestibular interaction over the situation [21], while a dominance of proprioceptive and kinesthetic sensations over the situation will cause the opposite effect, an undercompensation for the body tilt, also known as the A (Aubert) effect [5]. The sudden overcompensation found in the three IS subjects can be the result of a delayed ability to appropriately reweigh the inputs of the sensory systems as the suppression of the vestibular and somatosensory inputs is lifted. Further research is required to explain why the variation is only found in the right cycle. A possible explanation may be derived from the finding that girls with a severe scoliosis have a larger left pelvis depth and a wider right pelvis [22]. It is possible that this asymmetry leads to differences in proprioceptive inputs and thereby different results between the left and right cycles. Why the deviating patterns are only found in 14-year-olds is likely due to their stage of development of the sensory systems. Although lower-level processes, such as automatic postural adjustments, develop in early childhood, the higher-level weighing of proprioceptive, vestibular and visual inputs for head orientation is not fully developed to the adult level before the age of 15 or 16 years [23–25]. The visual system provides the most dominant input for controlling posture in young children [26]. When looking at the results of condition 2, this course of development is seen in the NS group, while the IS group deviates from this ‘normal’ development. The differences between the NS and IS groups for different age categories suggest that the process of development of the sensory integration for head orientation appears to be different for girls with scoliosis than for girls without scoliosis.
Conclusions When the sensory inputs are not in conflict with each other, no significant differences are found between the NS and IS groups in cross-correlations, delays or head angular velocities. However, differences are greater when there is conflict, especially for different age categories. When the sensory inputs are in conflict with each other, vision appears to become increasingly important, especially when the body is tilted. The visual system is dominant for most girls; however, all girls have head angle thresholds at which the vestibular and/or somatosensory contribution to head orientation increases. Especially girls with idiopathic scoliosis strongly rely on visual information in the case of
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sensory conflict, except for the 13- to 14-year category in this group, which shows a smaller role for the visual system and a strong reliance on the other perceptual systems. The differences in reliance on the sensory systems between the groups with and without scoliosis suggests that the central nervous systems of girls with scoliosis have a different way of determining how reliable a sensory system is and which system is most reliable. This supports our hypothesis. The differences between the groups for different age categories suggest that the process of development of the sensory integration for head orientation also appears to be different for girls with scoliosis than for girls without scoliosis. Conflict of interest
None.
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ORIGINAL ARTICLE
Altered head orientation patterns in children with idiopathic scoliosis in conditions with sensory conflict P. N. Eijgelaar • F. H. Wapstra • E. Otten A. G. Veldhuizen
•
Received: 22 April 2014 / Revised: 3 August 2014 / Accepted: 3 August 2014 / Published online: 17 August 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose Idiopathic scoliosis (IS) is the most common spinal deformity in adolescents. Defective postural equilibrium may be a contributing factor. The information of the three sensory systems combined enables the formation of a central representation of head position and body posture. Comparison of head angles of girls with and without scoliosis may result in a difference in head orientation. Methods 25 girls with IS and 16 girls without scoliosis (NS) between the age of 10–16 years stand in a special constructed box on a roll-tilting platform (tilt -14° to ?14°). Results NS and IS subjects behave quite similarly if there is no sensory conflict, but if there is conflict, the differences between the two groups are greater, especially within the 13- to 14-year-old category. Conclusions The differences between groups for different age categories suggest that the process of development of sensory integration for estimation of verticality appears to be different for girls with scoliosis. Keywords Idiopathic scoliosis Head orientation Perception of verticality Tilted room P. N. Eijgelaar Human Movement Sciences, Groningen, The Netherlands F. H. Wapstra A. G. Veldhuizen (&) Department of Orthopaedics, University Medical Center of Groningen, University of Groningen, Po.box: 30.001, 9700 RB Groningen, The Netherlands e-mail: [email protected] E. Otten Center for Human Movement Sciences, University Medical Center of Groningen, University of Groningen, Groningen, The Netherlands
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Introduction Idiopathic scoliosis (IS) is the most common spinal deformity in adolescents [1]. Although the ancient Greeks first made good anatomic descriptions of the structural changes seen in scoliosis, we have not as yet elucidated its pathogenesis. The deformity always develops from a straight spine into a curved spine, usually accompanied by a rib cage deformity, during the growth period in general, and in particular in the rapid growth period [2, 3]. Awareness of the position of the body in space is a highly developed sense in humans. The vestibular information is combined with incoming somatosensory and visual information, which enables the formation of a central representation of head position and body posture [4–6]. This representation is important in the maintenance of balance and therefore in the control of posture as well. With this sensory information, healthy subjects are able to determine the true vertical and horizontal, even when the head or body is tilted [7]. The functional ranges of the three systems overlap, so that they are able to compensate in part for each other’s deficiencies [8, 9]. Defective postural equilibrium has been proposed as a contributing factor in the development of scoliosis [10]. Several findings give reason to believe that patients with IS are less capable of making accurate estimations of verticality of their bodies. IS patients present perceptual impairments and deficits in sensorimotor adaptation, learning and balance control [1, 11]. These impairments are indicative of disorders at higher integrative levels of the central nervous system [11]. Since various patients with IS present longer somatosensory cortical potentials compared to healthy individuals, their balance instabilities could be associated with alteration in sensory signal processing [12].
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The occurrence of vestibular-related deficits in IS patients is well established [11, 13]. It is unclear whether a vestibular pathology is the common cause for the scoliotic syndrome and gaze and posture deficits, or if the latter behavioural deficits are a consequence of the scoliotic deformations. A possible vestibular origin was tested in the frog Xenopus laevis by unilateral removal of the labyrinthine end organs at larval stages. After metamorphosis into young adult frogs, X-ray images and three-dimensional reconstructed microcomputer tomographic scans of the skeleton showed deformations similar to those of scoliotic patients [14]. Furthermore, Wiener-Vacher and Mazda [15] found in their study that 66.7 % of the IS patients have greater asymmetry in their otolith responses than matched control subjects with congenital scoliosis or without scoliosis. Also, several studies examining vibratory sensitivity—which is used as an estimate of proprioceptive function—found a significant asymmetry between right and left detection thresholds in subjects with IS and/or a lower [16] or higher [17, 18] vibratory sensitivity in subjects with IS compared to healthy subjects, which could also be of influence in the estimation of verticality made by people with IS. The hypothesis is that patients with IS form their head orientations in a different manner from individuals without scoliosis. Whether the deviating aspect lies within the integration of the sensory systems or within one of the systems itself will not be answered directly by the outcome of this study; it mostly serves to answer the question whether individuals with IS do indeed have a different neural regulation for head position.
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Fig. 1 The experimental setting of condition 1. The subject is standing inside the tilting room on the platform. Condition 3 has the same circumstances minus the box and condition 4 equals condition 3 with eyes closed
Methods For this study, 25 girls with thoracic, thoracolumbar or lumbar IS (Cobb angle 33.5° ± 16°, age 13.5 ± 2) and 16 girls without scoliosis (NS) (age 13.2 ± 2) between the ages of 10–16 years stand in a special constructed box on a roll-tilting platform (tilt -14° to ?14°). Criteria for exclusion from the study are the presence of any vestibular disorders or motor impairments in an individual, and/or a height over 1.78 m. The box (112 9 112 9 180 cm) is constructed out of blackpainted wooden pergolas and white Chinese paper to obscure the outside world (Fig. 1). A Canon HF-100 HD digital video camera (with a frame rate frequency set at 25 Hz) is used to record the subjects on video while undergoing the experimental conditions (Figs. 1, 2). Protocol Markers are placed on the head cap (Fig. 3) and additional markers are placed on the box or on an upside down table
Fig. 2 The experimental setting of condition 2. The subject is sitting inside the tilting room, but is supported by a table that does not tilt along with the platform
(depending on the condition) to determine head and platform positions. The subjects were instructed to look straightforward and to relax and, if wearing a brace in daily life, to do so during the experiment. The following four conditions are investigated:
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Fig. 3 The positions of the markers on the subject’s cap
1.
2.
3.
4.
Inbox: subject is standing inside the box with her eyes open (the box and subject’s support surface are rolltilting along with the platform). Inbox sit: subject is sitting on the table inside the box with her eyes open (the box is roll-tilting along with the platform, but the subject’s support surface is not). Outbox open: subject is standing on the platform without the box with her eyes open (subject’s support surface is roll-tilting along with the platform). Outbox closed: subject is standing on the platform without the box with her eyes closed (subject’s support surface is roll-tilting along with the platform).
In 60 s the platform roll-tilts 14° to the right, stops, and tilts back to the 0° starting position, where it pauses shortly and then continues to tilt 14° to the left and then returns to the 0° position again. Half of the subjects start the cycle with roll-tilting to the right and half of them start roll-tilting to the left. Also, the order of conditions is varied per subject.
also used to calculate the mentioned cross-correlation coefficients, delays, and slopes and head angular velocities. For every subject in every condition, head angle graphs are used to determine what different behavioural patterns of head angles are present among subjects, and the subjects are categorised based on their head angle pattern. SPSS version 16.0 is used for concordance analysis between groups (NS and IS) and portrayed patterns and also within NS and IS groups between age categories (10–12, 13–14 and 15–16 years old) and portrayed patterns. Furthermore, multivariate analysis of variance (MANOVA) is conducted between groups for every condition for dependent variables’ cross-correlation coefficient, delay, slope and head angular velocity and repeated measures MANOVAs between and within groups over all conditions. The effects of hand preference and age category are determined for both groups, and for the IS group the effects of convexity (right, left and right/left), location (thoracic, lumbar and thoraco-lumbar) and Cobb angle (B40° and [40°) are also determined. If a significant effect of any of these betweensubjects factors is found, and the factor has at least three categories, a post hoc test with Bonferroni correction is conducted to determine between which of the categories the variables are significantly different.
Results Analysis of head angle conducts provides us with six categories of head angle patterns:
Variables 1. The video recordings provide us with footage of the marker positions of the head cap worn by the subjects. These video recordings are converted into mp4-files, which are entered into the analysis program Nbody Project A, written especially for this study. This software is used to track the marker positions of the head cap and these positions are used for calculating head angles. The platform angle is calculated using markers at the edges of the box (condition 1 and 2) or markers at the legs of an upside down table on the platform (condition 3 and 4). Cross-correlation and delay between the platform angle and head angle are calculated and used as measures to describe characteristic behaviour of subjects in all conditions in terms of accuracy and delay of coupling, respectively. Two other measures calculated are slope of the head angle signal and average head angular velocity.
2.
Static: the head angle does not follow the platform angle, but remains close to zero. (Fig. 4) (Partially) trailing: the head angle follows the platform angle during both the leftward and rightward tilts, albeit to different extents. (Fig. 5)
Data analysis The marker positions signals are filtered with a 2 Hz low pass zero lag filter, using Matlab version 2007b. Matlab is
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Fig. 4 Static head angle signal (condition 2 for NS 2, age 15 years old)
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Fig. 5 Trailing head angle signal (condition 1 for IS 23; Cobb angle 20°, age 15 years)
Fig. 7 Delayed trailing head angle signal (condition 1 for IS 12; Cobb angle 43°, age 10 years old)
Fig. 6 Partially trailing head angle signal (condition 2 for NS 6, age 14 years old)
Fig. 8 Leading head angle signal (condition 3 for IS 16; Cobb angle 40°, age 11 years old)
3.
4.
5.
6.
Delayed trailing: the head angle remains close to zero, until the platform reaches a certain angle, at which point the head angle starts to follow the platform angle. This is the case in both leftward and rightward tilts. (Fig. 6) Leading: the head angle follows the platform angle; however, around or shortly before reaching the maximum platform angle, the head angle starts decreasing before the platform angle does. This is the case in both leftward and rightward tilts. (Fig. 7) Mirroring: as the platform angle increases towards one side and decreases again, the head angle increases towards the opposite side and decreases again. This is the case in both leftward and rightward tilts. (Fig. 8) Residual: no specific head angle pattern. (Fig. 9)
Fig. 9 Mirroring head angle signal (condition 3 for IS 19; Cobb angle 25°, age 14 years old)
Condition 1: inbox Descriptive statistics See Tables 1 and 2.
All subjects—of both the NS and IS groups—show a (partially) trailing pattern. None of the dependent variables
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Table 1 Frequencies of head angle patterns in NS and IS groups and among different age groups NS All
IS 10–12 years
13–14 years
15–16 years
All
10–12 years
13–14 years
15–16 years
Condition 1 N
16
6
7
3
25
11
6
8
(Partially) trailinga
100.0
100.0
100.0
100.0
88.0
100.0
50.0
100.0
Otherb
0.0
0.0
0.0
0.0
12.0
0.0
50.0
0.0
Condition 2 N
15
6
6
3
25
11
6
8
Staticc (Partially) trailinga
40.0 33.3
0.0 50.0
33.3 33.3
66.7 33.3
28.0 24.0
9.1 27.3
83.3 0.0
12.5 37.5
Delayed trailingd
13.3
33.3
16.7
0.0
32.0
36.4
16.7
37.5
Otherb
13.3
16.7
16.7
0.0
16.0
27.3
0.0
12.5
Condition 3 N
16
6
7
3
25
11
6
8
Staticc
18.8
0.0
14.3
66.7
20.0
9.1
16.7
37.5
Leadinge
50.0
50.0
57.1
33.3
48.0
72.7
50.0
12.5
Mirrorringf
31.2
50.0
28.6
0.0
20.0
9.1
33.3
25.0
Otherb
0.0
0.0
0.0
0.0
12.0
9.1
0.0
25.0
Condition 4 N
16
6
7
3
25
11
6
8
Leadinge
81.2
83.3
71.4
100.0
80.0
81.8
83.3
75.0
Otherb
18.8
16.7
28.6
0.0
20.0
18.2
16.7
25.0
Frequencies are displayed in percentages NS no scoliosis, IS idiopathic scoliosis a
The head angle follows the platform angle during both the leftward and rightward tilt, albeit to different extents
b
The subjects show no specific pattern
c
The head angle does not follow the platform angle, but remains close to zero
d
The head angle remains close to zero, until the platform reaches a certain angle, at which point, the head angle starts to follow the platform angle
e
The head angle follows the platform angle, until around or shortly before reaching the maximum platform angle, at which point the head angle starts decreasing before the platform angle does
f
As the platform angle increases towards the one side and decreases again, the head angle increases towards the other side and decreases again
are significantly different between the NS and IS groups. In the IS group, age appears to be a significant factor in conduct; the 13- to 14-year category has a significantly lower right cross-correlation (p = 0.002 and p = 0.005, respectively) and smaller right slope (p = 0.026 and p = 0.039, respectively) than the 10- to 12-year and 15- to 16-year age categories. Their average head angular velocity, on the other hand, is greater, which, all together, implies that their head angle signals are noisier than the other two categories. Head angle graphs confirm this: although all subjects follow a pattern roughly similar to that of Fig. 5, 10 shows the variation on this, which three out of the six 13- to 14-year-olds of the IS group show. Note that—in all three cases—the sudden switch of the head angle towards the other side as the platform angle approaches its maximum only happens when the roll-tilt of
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the platform is to the right. Besides being 14 years old, these three subjects have in common that they are all righthanded. Their convexities, locations of the scoliosis and Cobb angles are of various categories. Condition 2: inbox sit In condition 2, subjects can be categorised into four groups of head angle patterns: static (Fig. 4), partially trailing (Fig. 6), delayed trailing (Fig. 7) and residual patterns. Subjects in the NS group tend towards the static pattern (40.0 %), while the main pattern in the IS group is the delayed trailing pattern (32.0 %). Correspondence analysis shows that little correspondence exists between age category and head angle pattern within the NS group (v2 = 1.667, p = 0.948), while, on the other hand, great
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Table 2 Descriptive statistics of cross-correlations between head angles and platform angles for NS and IS groups and for different age categories within the NS and IS groups NS
IS a
N
Overall
16
0.955 ± 0.08
Left
b
N
Overalla
Leftb
Rightc
0.970 ± 0.06
25
0.941 ± 0.06
0.952 ± 0.04
0.943 ± 0.10
Right
c
Condition 1 All categories
0.957 ± 0.08
Age category 10–12 years
6
0.972 ± 0.02
0.976 ± 0.02
0.982 ± 0.02
11
0.947 ± 0.05
0.948 ± 0.05
0.967 ± 0.06
13–14 years
7
0.930 ± 0.12
0.933 ± 0.11
0.950 ± 0.09
6
0.905 ± 0.09
0.945 ± 0.04
0.861 ± 0.17
15–16 years
3
0.981 ± 0.01
0.976 ± 0.01
0.991 ± 0.01
8
0.960 ± 0.03
0.964 ± 0.04
0.972 ± 0.02
15
0.825 ± 0.10
0.821 ± 0.15
0.823 ± 0.15
25
0.795 ± 0.17
0.801 ± 0.16
0.821 ± 0.24
Condition 2 All categories Age category 10–12 years
6
0.837 ± 0.08
0.819 ± 0.13
0.837 ± 0.20
11
0.834 ± 0.11
0.830 ± 0.13
0.896 ± 0.09
13–14 years
6
0.818 ± 0.12
0.862 ± 0.08
0.817 ± 0.12
6
0.656 ± 0.26
0.662 ± 0.22
0.610 ± 0.38
15–16 years
3
0.815 ± 0.14
0.742 ± 0.28
0.806 ± 0.17
8
0.828 ± 0.12
0.833 ± 0.12
0.843 ± 0.18
16
0.645 ± 0.21
0.625 ± 0.34
0.511 ± 0.36
25
0.636 ± 0.20
0.551 ± 0.32
0.531 ± 0.30
6
0.601 ± 0.23
0.611 ± 0.40
0.413 ± 0.40
11
0.665 ± 0.21
0.621 ± 0.29
0.591 ± 0.29
Condition 3 All categories Age category 10–12 years 13–14 years
7
0.690 ± 0.20
0.678 ± 0.34
0.623 ± 0.34
6
0.621 ± 0.18
0.507 ± 0.24
0.471 ± 0.21
15–16 years Condition 4
3
0.630 ± 0.26
0.538 ± 0.39
0.481 ± 0.38
8
0.630 ± 0.20
0.493 ± 0.35
0.508 ± 0.32
All categories
16
0.739 ± 0.23
0.802 ± 0.23
0.703 ± 0.28
25
0.777 ± 0.20
0.772 ± 0.25
0.753 ± 0.25
Age category 10–12 years
6
0.752 ± 0.23
0.810 ± 0.19
0.687 ± 0.32
11
0.805 ± 0.21
0.758 ± 0.33
0.764 ± 0.29
13–14 years
7
0.711 ± 0.26
0.796 ± 0.27
0.684 ± 0.29
6
0.722 ± 0.22
0.731 ± 0.24
0.712 ± 0.23
15–16 years
3
0.777 ± 0.25
0.801 ± 0.28
0.779 ± 0.27
8
0.840 ± 0.17
0.867 ± 0.13
0.823 ± 0.21
NS no scoliosis, IS idiopathic scoliosis a
Cross-correlations between head angles and platform angles over whole cycles
b
Cross-correlations between head angles and platform angles over the left half cycles
c
Cross-correlations between head angles and platform angles over the right half cycles
correspondence exists between age group and head angle pattern within the IS group (v2 = 13.225; p = 0.040). In the IS group, five out of seven static pattern subjects are in the 13- to 14-year category. Post hoc tests confirm that, within the IS group, the 13- to 14-year subjects show significantly smaller cross-correlations than the 15- to 16-year category (p = 0.033) and their cross-correlations are smaller, although not significantly smaller, than those of the 10- to 12-year category (p = 0.055). All of the static group subjects are right-handed, but are of various convexity, location and Cobb angle categories (Fig. 5).
Fig. 10 Head angle signal in condition 1 for subject IS11 (Cobb angle 60°, age 14 years old). The pattern of this signal resembles the patterns of three head angle signals of the 13- to 14-year group of the IS (idiopathic scoliosis) group in condition 1
Condition 3: outbox open Analysis of the head and platform signals allows us to divide the subjects into four categories based on their
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behaviours: static (Fig. 4), leading (Fig. 8), mirroring (Fig. 9) and residual patterns. In both groups, the 15- to 16-year-olds tend towards the static pattern (for NS and IS, 66.7 and 37.5 %, respectively). For the IS group, the majority (72.7 %) of the 10- to 12-year group shows the leading pattern, as does a great share of the 13- to 14-year group (50.0 %). In the NS group, 10- to 12-year-olds show either the leading pattern (50.0 %) or the mirroring pattern (50.0 %), as does the major share of the 13- to 14-year-olds (57.1 and 14.3 %, respectively). Although the correspondence between age group and head angle pattern is considerable, analysis shows that it is not significant (v2 = 6.740, p = 0.346 for NS and v2 = 8.632, p = 0.195 for IS). Differences in patterns between the NS and IS groups are relatively small and multivariate and univariate tests do not show any significant differences between the two groups for any of the dependent variables. Condition 4: outbox closed Condition 4 shows a lot of similarities to condition 3. In condition 4, however, the variance between the subjects is smaller. Most subjects (13 out 16 NS subjects and 20 out of 25 IS subjects) show the leading pattern. Delays of head angle signals confirm that the leading pattern is the main pattern in this condition; both the NS and the IS group show great positive delays, indicating that the head angle precedes the platform angle. However, in the IS group, the 13- to 14-year group shows negative overall, left and right delays, and in the NS group this also is the case for the 15to 16-year group. Multivariate and univariate tests do not show any significant differences for any of the dependent variables between the two groups. Comparison of conditions Some correspondence exists between patterns shown in one condition and those in another condition. For example, 9 out of 13 subjects, showing the static pattern in condition 2, show the leading pattern in condition 3. Also, NS subjects belonging to the residual group in condition 4 show the mirroring pattern in condition 3. For the IS group, residual pattern subjects in condition 4 show either the static, mirroring or residual pattern in condition 3. For both groups, it can be stated that if subjects show the leading pattern in condition 3, they also show the leading pattern in condition 4. All but one static pattern subjects in condition 3 also show the leading pattern in condition 4. Correspondence analysis shows that great correspondence exists between patterns in condition 3 and condition 4 (v2 = 15.265, p = 0.002). Correspondences between patterns of other conditions are much smaller.
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Discussion In situations without sensory conflict, the differences in head angle patterns and dependent variables between NS and IS girls are relatively small. This indicates that, in these situations, the head orientations and presumably the formation of the head orientations are similar for NS and IS girls. When sensory inputs are in conflict with each other, differences between NS and IS groups are greater. In condition 1, the trailing pattern implies that the incorrect static visual information is dominant over the contradictory correct dynamic vestibular and somatosensory systems information, and in condition 2, trailing means that the incorrect dynamic visual information is dominant over the correct static vestibular and somatosensory systems information in determining the head angle. Somehow, the CNS judges the visual information as more reliable than the other two systems in these cases, even though it is actually the other way around. According to the literature, healthy adults primarily rely on somatosensory inputs for posture control in a wellpractised situation, like standing on a stable surface, and under normal sensory conditions, and only in novel situations, such as situations of sensory conflict, visual input becomes more important [19]. However, it is also stated that in those new situations, information provided by the vestibular system is used as a reference and intersensory conflict is resolved by suppressing input that is incongruent with this vestibular information [19]. This is not in agreement with these trailing patterns. Visual motion—in this case rotation of the visual field—often leads to vection, which is the induced perception of self-motion, known to influence postural movement [20]. For most cases, the trailing of the platform angle by the head angle is only to a certain degree, which suggests that the suppression of the vestibular and somatosensory inputs is (partially) lifted at this point and determination of the head angle is based on a weighted combination of the three inputs. The vestibular cortex interacts with the visual cortex by means of reciprocal inhibitory visual–vestibular interaction for adequate self-motion perception [8]. This inhibitory interaction mechanism allows for a shift of the dominant sensorial weight during motion perception from one sensory modality to the other, depending on the prevailing mode of stimulation: acceleration (vestibular input) or constant velocity (visual input) or both [8]. When the platform angle reaches its maximum, the angle velocity of the rotation of the subject is no longer constant; it starts to decrease. When there is acceleration—which, in this case, is deceleration— contribution of vestibular input becomes increasingly important. In the IS group, we can see three 14-year-olds portraying deviating behaviour. One way to explain the sudden
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shift in the right half cycle is that the lift of suppression of the vestibular and somatosensory systems results in an E effect, which is the tendency by one to overcompensate for the body tilt, at moderate lateral body tilts up to 30°. This tilt leads the subjects to erroneously estimate the true vertical [5, 21]. This effect is the result of a dominance of visual–vestibular interaction over the situation [21], while a dominance of proprioceptive and kinesthetic sensations over the situation will cause the opposite effect, an undercompensation for the body tilt, also known as the A (Aubert) effect [5]. The sudden overcompensation found in the three IS subjects can be the result of a delayed ability to appropriately reweigh the inputs of the sensory systems as the suppression of the vestibular and somatosensory inputs is lifted. Further research is required to explain why the variation is only found in the right cycle. A possible explanation may be derived from the finding that girls with a severe scoliosis have a larger left pelvis depth and a wider right pelvis [22]. It is possible that this asymmetry leads to differences in proprioceptive inputs and thereby different results between the left and right cycles. Why the deviating patterns are only found in 14-year-olds is likely due to their stage of development of the sensory systems. Although lower-level processes, such as automatic postural adjustments, develop in early childhood, the higher-level weighing of proprioceptive, vestibular and visual inputs for head orientation is not fully developed to the adult level before the age of 15 or 16 years [23–25]. The visual system provides the most dominant input for controlling posture in young children [26]. When looking at the results of condition 2, this course of development is seen in the NS group, while the IS group deviates from this ‘normal’ development. The differences between the NS and IS groups for different age categories suggest that the process of development of the sensory integration for head orientation appears to be different for girls with scoliosis than for girls without scoliosis.
Conclusions When the sensory inputs are not in conflict with each other, no significant differences are found between the NS and IS groups in cross-correlations, delays or head angular velocities. However, differences are greater when there is conflict, especially for different age categories. When the sensory inputs are in conflict with each other, vision appears to become increasingly important, especially when the body is tilted. The visual system is dominant for most girls; however, all girls have head angle thresholds at which the vestibular and/or somatosensory contribution to head orientation increases. Especially girls with idiopathic scoliosis strongly rely on visual information in the case of
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sensory conflict, except for the 13- to 14-year category in this group, which shows a smaller role for the visual system and a strong reliance on the other perceptual systems. The differences in reliance on the sensory systems between the groups with and without scoliosis suggests that the central nervous systems of girls with scoliosis have a different way of determining how reliable a sensory system is and which system is most reliable. This supports our hypothesis. The differences between the groups for different age categories suggest that the process of development of the sensory integration for head orientation also appears to be different for girls with scoliosis than for girls without scoliosis. Conflict of interest
None.
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