visuo-oculomotor deficiency at early-stage idiopathic scoliosis in adolescent girls

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DEFORMITY SPINE Volume 38, Number 3, pp 238–244 ©2013, Lippincott Williams & Wilkins 238 www.spinejournal.com February 2013 Visuo-Oculomotor Deciency at Early-Stage Idiopathic Scoliosis in Adolescent Girls Alexis Lion, PhD,*† Thierry Haumont, MD, PhD,*†‡§ Gérome C. Gauchard, PhD,*† Sylvette R. Wiener-Vacher, MD, PhD, Pierre Lascombes, MD, PhD,‡§ and Philippe P. Perrin, MD, PhD*†¶ Study Design. Cross-sectional study. Objective. To determine whether adolescent idiopathic scoliosis (AIS) at onset is associated with oculomotor dysfunction and whether these oculomotor anomalies are correlated to the amplitude of the spine deformation. Summary of Background Data. AIS is related to abnormalities of postural control. To date, few studies have focused on visuo- oculomotor and vestibulo-ocular functions at early-stage AIS. Methods. Fifty-three adolescent girls were diagnosed with AIS (mean age: 11.6 ± 2.1 yr) on clinical and radiological criteria (mean Cobb angle: 14.8 ° ± 5.0 °). Visuo-oculomotor and vestibulo-ocular functions were studied with video-oculography, including saccades, smooth pursuit, caloric test, and pendular rotation, with visual vestibular ocular reex and vestibulo-ocular reex sequences. Two patient groups were dened according to the mean Cobb angle: group 1 included 29 patients with a Cobb angle from 5 ° to 14 ° and group 2 included 24 patients with a Cobb angle from 15 ° to 25 °. Results. The group 2 showed different saccade characteristics than group 1: higher latencies for saccade sequences characterized by temporal uncertainty and predictive direction; lower velocity regardless of the type of the saccades. No difference was observed for saccadic accuracy and smooth-pursuit gain. For the visual vestibular ocular reex, group 2 showed lower total maximal slow- A dolescent idiopathic scoliosis (AIS) is one of the most common skeletal deformations in humans, affecting about 4% of the adolescent population worldwide. AIS is a 3-dimensional spinal deformation involving all or part of the vertebral column, predominantly affecting girls, 1 ,2 and mainly develops during pubertal growth. 3 ,4 Although AIS does not seem to limit the practice of sports, 5 ,6 untreated progressive AIS may induce back pain and respiratory problems which could affect overall activities and self-esteem. 7 To avoid these physical and psychological com- plications related to the possible progression of the scoliosis, several treatments can be proposed. Identification of etio- pathogenetic factors specific to progressive AIS and detectable at its onset could help prevent the development of the spine deformity. 7 Many factors have been incriminated in the patho- genesis of AIS, suggesting that this disease is multifactorial. 7 ,8 Among the different factors possibly involved in AIS are senso- rimotor dysfunctions and, in particular, postural impairments when the amplitude of the spinal curve was progressive. 9 11 Accurate postural control requires an efficient central process- ing of neurosensorial information provided by the visual, ves- tibular, and somesthetic sensors. This processing is necessary to generate appropriate motor responses including compensa- tory eye movements and body adjustments. 12 16 Abnormalities at each level of the postural control regulation could trigger AIS. The somesthetic sensitivity was found altered in AIS 17 21 and could be a causative factor of spinal asymmetry. 22 More- over, a high rate of trunk deformity was observed in a young blind population, 23 highlighting a possible role of vision in AIS. A decreased incidence of scoliosis was found in children From the *Balance Control & Motor Performance, University of Lorraine, UFR STAPS, Villers-lès-Nancy, France; †INSERM U 954, Faculty of Medicine, Vandoeuvre-lès-Nancy, France; ‡Department of Pediatric Orthopedic Surgery, University Hospital of Nancy, Children Hospital, Vandoeuvre-lès-Nancy, France; §Department of Anatomy, Faculty of Medicine, Vandoeuvre-lès-Nancy, France; Unité d’exploration des troubles de l’équilibre chez l’enfant, Hôpital Robert Debré, Paris, France; and ¶Department of Oto-rhino-laryngology, University Hospital of Nancy, Children Hospital, Vandoeuvre-lès-Nancy, France. Acknowledgment date: November 2, 2011. First revision date: April 17, 2012. Acceptance date: July 12, 2012. The manuscript submitted does not contain information about medical device(s)/drug(s). “Fondation Yves Cotrel,” Institut de France, Académie des Sciences, Paris, grant funds were received to support this work. No benets in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Address correspondence and reprint requests to Philippe P. Perrin, MD, PhD, Equilibration et Performance Motrice, Université de Lorraine, UFR STAPS, 30, rue du Jardin Botanique, 54 600 Villers-lès-Nancy, France; E-mail: Philippe. [email protected] phase velocity than group 1, whereas the vestibulo-ocular reex (tested in dark) did not differ between groups. No difference was observed concerning the caloric vestibular test. Conclusion. Patients with a Cobb angle of 15 ° or more presented normal vestibulo-ocular responses but altered visuo-oculomotor functions, especially for the saccadic latency and velocity. This could be the result of a dysfunction of oculomotor pathways at cerebellar and/or brainstem level. These central disorders may be incriminated in the development of AIS. Key words: idiopathic scoliosis, visuo-oculomotor function, Cobb angle, early stage, videonystagmography. Spine 2013;38: 238–244 DOI: 10.1097/BRS.0b013e31826a3b05 Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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DEFORMITY

SPINE Volume 38, Number 3, pp 238–244©2013, Lippincott Williams & Wilkins

238 www.spinejournal.com February 2013

Visuo-Oculomotor Defi ciency at Early-Stage Idiopathic Scoliosis in Adolescent Girls

Alexis Lion , PhD , * † Thierry Haumont , MD, PhD , * † ‡ § Gérome C. Gauchard , PhD , * † Sylvette R. Wiener-Vacher , MD, PhD , � Pierre Lascombes , MD, PhD , ‡ § and Philippe P. Perrin , MD, PhD * † ¶

Study Design. Cross-sectional study. Objective. To determine whether adolescent idiopathic scoliosis (AIS) at onset is associated with oculomotor dysfunction and whether these oculomotor anomalies are correlated to the amplitude of the spine deformation. Summary of Background Data. AIS is related to abnormalities of postural control. To date, few studies have focused on visuo-oculomotor and vestibulo-ocular functions at early-stage AIS. Methods. Fifty-three adolescent girls were diagnosed with AIS (mean age: 11.6 ± 2.1 yr) on clinical and radiological criteria (mean Cobb angle: 14.8 ° ± 5.0 ° ). Visuo-oculomotor and vestibulo-ocular functions were studied with video-oculography, including saccades, smooth pursuit, caloric test, and pendular rotation, with visual vestibular ocular refl ex and vestibulo-ocular refl ex sequences. Two patient groups were defi ned according to the mean Cobb angle: group 1 included 29 patients with a Cobb angle from 5 ° to 14 ° and group 2 included 24 patients with a Cobb angle from 15 ° to 25 ° . Results. The group 2 showed different saccade characteristics than group 1: higher latencies for saccade sequences characterized by temporal uncertainty and predictive direction; lower velocity regardless of the type of the saccades. No difference was observed for saccadic accuracy and smooth-pursuit gain. For the visual vestibular ocular refl ex, group 2 showed lower total maximal slow-

Adolescent idiopathic scoliosis (AIS) is one of the most common skeletal deformations in humans, affecting about 4% of the adolescent population worldwide.

AIS is a 3-dimensional spinal deformation involving all or part of the vertebral column, predominantly affecting girls, 1 , 2 and mainly develops during pubertal growth. 3 , 4

Although AIS does not seem to limit the practice of sports, 5 , 6 untreated progressive AIS may induce back pain and respiratory problems which could affect overall activities and self-esteem. 7 To avoid these physical and psychological com-plications related to the possible progression of the scoliosis, several treatments can be proposed. Identifi cation of etio-pathogenetic factors specifi c to progressive AIS and detectable at its onset could help prevent the development of the spine deformity. 7 Many factors have been incriminated in the patho-genesis of AIS, suggesting that this disease is multifactorial. 7 , 8 Among the different factors possibly involved in AIS are senso-rimotor dysfunctions and, in particular, postural impairments when the amplitude of the spinal curve was progressive. 9 – 11 Accurate postural control requires an effi cient central process-ing of neurosensorial information provided by the visual, ves-tibular, and somesthetic sensors. This processing is necessary to generate appropriate motor responses including compensa-tory eye movements and body adjustments. 12 – 16 Abnormalities at each level of the postural control regulation could trigger AIS. The somesthetic sensitivity was found altered in AIS 17 – 21 and could be a causative factor of spinal asymmetry. 22 More-over, a high rate of trunk deformity was observed in a young blind population, 23 highlighting a possible role of vision in AIS. A decreased incidence of scoliosis was found in children

From the * Balance Control & Motor Performance, University of Lorraine, UFR STAPS, Villers-lès-Nancy, France; † INSERM U 954, Faculty of Medicine, Vandoeuvre-lès-Nancy, France; ‡ Department of Pediatric Orthopedic Surgery, University Hospital of Nancy, Children Hospital, Vandoeuvre-lès-Nancy, France; § Department of Anatomy, Faculty of Medicine, Vandoeuvre-lès-Nancy, France; � Unité d’exploration des troubles de l’équilibre chez l’enfant, Hôpital Robert Debré, Paris, France; and ¶ Department of Oto-rhino-laryngology, University Hospital of Nancy, Children Hospital, Vandoeuvre-lès-Nancy, France .

Acknowledgment date: November 2, 2011. First revision date: April 17, 2012. Acceptance date: July 12, 2012.

The manuscript submitted does not contain information about medical device(s)/drug(s).

“Fondation Yves Cotrel,” Institut de France, Académie des Sciences, Paris, grant funds were received to support this work.

No benefi ts in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.

Address correspondence and reprint requests to Philippe P. Perrin, MD, PhD, Equilibration et Performance Motrice, Université de Lorraine, UFR STAPS, 30, rue du Jardin Botanique, 54 600 Villers-lès-Nancy, France; E-mail: [email protected]

phase velocity than group 1, whereas the vestibulo-ocular refl ex (tested in dark) did not differ between groups. No difference was observed concerning the caloric vestibular test. Conclusion. Patients with a Cobb angle of 15 ° or more presented normal vestibulo-ocular responses but altered visuo-oculomotor functions, especially for the saccadic latency and velocity. This could be the result of a dysfunction of oculomotor pathways at cerebellar and/or brainstem level. These central disorders may be incriminated in the development of AIS. Key words: idiopathic scoliosis , visuo-oculomotor function , Cobb angle , early stage , videonystagmography . Spine 2013 ; 38 : 238 – 244

DOI: 10.1097/BRS.0b013e31826a3b05

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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with hearing impairment, a group known to have a higher incidence of vestibular damage. 24 However, spontaneous and positional nystagmus is more common in AIS. 25 Furthermore, the side of spine deformation was related to the side of ves-tibular hyporefl ectivity 25 and to the morphoanatomic asym-metry of semicircular canals. 26 In an animal model, the removal of the vestibular end organs at larval stage induces the development of skeletal distortion though the persistence of an asymmetric muscular tonus resulting from the lesion-induced asymmetric activity in descending spinal pathways. 27 Asymmetric sensitivity in the labyrinth was suggested to be one of the factors for AIS and postural impairments observed during caloric vestibular stimulations in an erect posture. 28 However, dysfunction in the postural control mechanisms at brainstem level could be also involved. 28 Bilateral imbalance of the activity in central vestibular pathways was proposed in AIS development, 29 , 30 as well as a dysfunction in the central information processing. 9 , 31 – 34 Indeed, a less effective central information processing was evidenced by diffi culties to man-age properly sensory input, especially vestibular input, in sen-sory confl icting situations. 31 , 34 The possible relations between AIS and postural control are therefore well documented in the literature, yet the relation with eye movements remains still unclear.

To our knowledge, no study has been done for early-stage AIS, evaluating voluntary and vestibular eye movements. The aim of this study was to investigate whether, in early-stage AIS, there is a signifi cant difference in visuo-oculomotor func-tions in children with mild and very mild spine deformation.

MATERIALS AND METHODS

Patients Fifty-three female teenagers (mean age: 11.6 ± 2.1 yr) agreed to participate in this study. All patients were recruited at their fi rst visit in the clinic for AIS screening. The Medical Ethics Committee (Comité de Protection des Personnes de Lorraine) approved the study and both parents and children gave writ-ten consent prior to the study. All radiographical and Cobb angle measurements 35 were performed for each patient’s spinal curve by the same orthopedic surgeon. Likewise, all clinical evaluations, including age, height, weight, body mass index, and curve type (thoracic, thoracolumbar, lumbar, and double major) were performed by the same physiotherapist. The orthopedic surgeon and the physiotherapist were not informed about the results of the visuo-oculomotor and ves-tibulo-ocular testing.

In our population, the mean Cobb angle of the primary curve was 14.8 ± 5.0 ° . Patients were split into 2 groups 34 : group 1 (n = 29) presented a Cobb angle from 5 ° to 14 ° (very mild scoliosis), and group 2 (n = 24) from 15 ° to 25 ° (mild scoliosis) ( Table 1 ).

Visuo-Oculomotor Tests Visuo-oculomotor responses were evaluated with a video-oculographic system (Synapsys, Marseille, France). This system included a standard video camera mounted on goggles, which

allows eye movements recording in real time. The subjects were seated in a chair in a totally darkened room at a distance of 1.2 m of the center of a screen, head in a fi xed position. A white dot projected by a video projector was presented on this screen. The subjects were instructed to fi x on and follow the dot as quickly and accurately as possible with the dominant eye. Target motion was controlled by a computer-generated waveform. Each session started with a calibration.

Several saccade tasks were performed: the subjects were instructed to look at a central fi xation point and then, after it disappeared, to look at a second target that could appear eccentric (20 ° left or 20 ° right) or central (in the middle of the screen [0 ° ]) according to a designed sequence. Three differ-ent sequences were used. The fi rst sequence (Freyss sequence) involved the randomly timed appearance of the target in a known direction (20 ° left or 20 ° right). The second sequence (alternated crenels) is a pseudorandom sequence with predic-tive direction (middle or 20 ° left or 20 ° right) with a tempo-ral uncertainty. This sequence offers successively movement of the target from the center to both extremities. The third sequence (fi xed sequence) was characterized by the regular disappearance of a target (frequency: 0.30 Hz), which reap-peared 20 ° to the left or right. This sequence was charac-terized by a predictive timing and direction of appearance. Three parameters were recorded. Latency is the time delay (in milliseconds) between each target jump and the onset of saccade. Velocity is the speed of the eyes displacements (in degrees per second). Accuracy is the ratio of the initial

TABLE 1. Characteristics for Groups I (Very Mild Scoliosis) and II (Mild Scoliosis). Mean Values and Standard Deviation for Age, Height, Weight, Body Mass Index, and for Curve Type of Idiopathic Scoliosis

Group 1, n = 29

(Mean ± SD)

Group 2, n = 24

(Mean ± SD)Intergroup

Comparison

Age (yr) 11.59 ± 2.17 11.76 ± 1.85 t = − 0.30, NS

Height (m) 1.48 ± 0.12 1.52 ± 0.13 t = − 1.07, NS

Weight (kg) 37.83 ± 7.78 38.79 ± 9.03 t = − 0.42, NS

BMI (kg/m 2 ) 17.02 ± 1.78 16.56 ± 2.05 t = 0.87, NS

Curve type

Thoracic curve

n = 0 n = 1 χ 2 = 1.94, NS

Thoracolumbar curve

n = 10 n = 6

Lumbar curve n = 6 n = 4

Double major curve

n = 13 n = 13

NS indicates not signifi cant.

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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saccade amplitude divided by the target displacement ampli-tude times 100 ( Figure 1 ).

For the smooth-pursuit task, the subject had to track a pre-dictable target moving horizontally and following a sinusoi-dal (amplitude: 45 ° , frequency: 0.30 Hz). The average veloc-ity of the smooth-pursuit eye movements for each participant was determined and the ratio between this average velocity and the target velocity gave the gain ( Figure 2 ). 36 , 37

Vestibulo-Ocular Tests These tests evaluate vestibulo-ocular responses to vestibular stimulation, recorded by videonystagmography. All subjects were tested with pendular rotation and caloric tests that stim-ulate horizontal semicircular canals.

Pendular rotary vestibular testing 38 consists in a stimu-lation of the horizontal semicircular canals by means of an angular acceleration in the horizontal plane. Rotational stim-uli affect both horizontal semicircular canals simultaneously. The subject sits on a chair mounted on a motorized rotating platform, with head tilted forward at 30 ° angle to place the horizontal canal in a horizontal plane. The stimulation is done by rotating the chair at a frequency of 0.05 Hz, with maxi-mal amplitude of 180 ° . Four sequences were used. During the fi rst sequence (visual vestibular ocular refl ex sequence), rotations were performed in the light without gaze fi xation adding the vestibulo-ocular responses from vestibular origin to the optokinetic refl ex from visual origin. The second and the last sequences were performed in the dark to evaluate the vestibulo-ocular refl ex (VOR1 and VOR2 sequences). The third sequence consisted in a gaze fi xation (fi xation sequence), where the participants were asked to look at their thumbs put together and their arms straightened forward during the rota-tion. Per-rotatory horizontal nystagmus was characterized by the total maximal slow phase velocity (in degrees per second) and the directional preponderance (in degrees per second) ( Figure 3 ). 39

The caloric vestibular test 38 , 40 is a nonphysiological stimu-lus of unilateral horizontal semicircular canal. The subject was supine with the head elevated to 30 ° to place the semi-circular canals in a vertical position. Each ear was irrigated for 30 seconds at a constant fl ow rate of 125 mL of water successively at 30 ° C and 44 ° C. The irrigation of the exter-nal auditory canal with water induces endolymphatic fl ow in the semicircular canal by creating a temperature gradient

Figure 1. Horizontal saccadic eye movements induced by a target moving in steps (fi xed sequence). Abscissa: time, ordinate: amplitude of the saccade. Upper curve: target; lower curve: eye movements, latency: 170 ms, velocity: 460 ° /s, accuracy: 95%.

Figure 2. Horizontal smooth pursuit of a target moving with a sinusoi-dal waveform. Abscissa: time, ordinate: amplitude of the pursuit. Up-per curve: target; lower curve: eye movements, gain (ratio eye move-ment velocity/target velocity): 0.80.

Figure 3. Pendular rotary vestibular testing. Abscissa: time, ordinate: amplitude of the pendular rotary vestibular testing for visual vestibular ocular refl ex ( A ), vestibulo-ocular refl ex ( B ), and gaze fi xation ( C ) sequences. Upper curve: chair’s movements; middle curve: maximal slow phase velocity; lower curve: eye movements.

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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t test. Statistically signifi cant differences were accepted for a probability level of P ≤ 0.05.

RESULTS Data on age, height, weight, body mass index, and curve type for both groups are presented in Table 1 . No signifi cant differ-ence was found for all these parameters between both groups.

Saccades’ latencies were longer in the group 2 than in the group 1, especially in the Freyss sequence (temporal uncer-tainty and predictive direction) ( t = − 2.14, P = 0.037). Velocities of each type of saccades were signifi cantly slower in the group 2 than in the group 1 (Freyss sequence: t = 2.52, P = 0.014; alternated crenels: t = 2.22, P = 0.031; fi xed sequence: t = 2.19, P = 0.033). No difference was observed between groups concerning saccadic accuracy and smooth-pursuit gain ( Table 2 ).

Concerning the pendular rotary test, the total maximal slow-phase velocity was slower in the group 2 than in the group 1 for the visual vestibular ocular refl ex sequence ( i.e. , pendular chair rotation in the light without gaze fi xation) ( t = 2.24, P = 0.029). The VOR did not differ between both groups ( Table 3 ). The caloric vestibular test did not show any signifi cant vestibular differences between both groups. The refl ectivity did not differ between groups (right refl ectivity, group 1: 27.18 ± 17.97 ° /s, group 2: 29.91 ± 24.32 ° /s, t = − 0.44, not signifi cant [NS]; left refl ectivity, group 1: 27.31 ± 17.60 ° /s, group 2: 29.38 ± 22.51 ° /s, t = − 0.34, NS; global refl ectivity, group 1: 54.50 ± 35.30 ° /s, group 2: 59.29 ± 46.69 ° /s, t = − 0.40, NS). The directional preponderance did not differ between groups (group 1: 7.13 ± 4.78 ° /s, group 2: 5.45 ± 6.66 ° /s, t = 0.99, NS).

DISCUSSION This study investigated the voluntary and vestibular eye move-ments in 2 groups of female teenagers with mild (group 2) and very mild (group 1) spine deformation. Saccade velocity was lower in teenagers with mild scoliosis than in teenagers with very mild scoliosis. Moreover, the latencies were longer in teenagers with mild scoliosis, especially in saccadic paradigms characterized by temporal uncertainty and known direction of the target. During the visual vestibular ocular refl ex sequence, the total maximal slow-phase velocity of the nystagmus was slower in teenagers with mild scoliosis. VOR in the dark was identical between the 2 groups.

A vestibular dysfunction has been often found in patients with AIS. 43 , 44 In our population, we did not fi nd peripheral vestibular dysfunction: responses to caloric test were normal as well as VOR in dark as it was previously shown. 29 How-ever, anatomical vestibular asymmetries existing at very early stages of embryogenesis could be implicated in AIS genesis. Some studies support this hypothesis: in patients with cranio-facial asymmetries, tonic lateralized hypertonia of spinal mus-cles may induce spine deformation. 44 Lambert et al 27 showed that the unilateral removal of the labyrinthine end organs at larval stages in frogs induces spinal deformities. They con-clude that a permanently imbalanced activity of descending locomotor/posture control pathways might be the common

in the canal. These stimulations produce a horizontal nys-tagmus with a slow component whose direction varies with water temperature. The vestibular refl ectivity, which repre-sents the sensitivity of the vestibular input, was determined for each side by the addition of maximal slow-phase veloci-ties obtained during cold and warm stimulation. Then, the refl ectivity of right and left sides leaded to the calculation of the global refl ectivity. The directional preponderance was also calculated ( Figure 4 ). 41 , 42

Statistical Analysis Qualitative data were expressed as number ( n ) and percentage (%) and compared by χ 2 . Quantitative data were expressed as mean with standard deviation and compared by Student

Figure 4. Caloric vestibular testing. Abscissa: time, ordinate: ampli-tude of eye movements ( A ) and of the maximal slow-phase velocity ( B ) for the 4 stimulations, from up to bottom. First curve: right ear ir-rigated with water at 44 ° C, second curve: right ear irrigated with water at 30 ° C, third curve: left ear irrigated with water at 30 ° C, and fourth curve: left ear irrigated with water at 44 ° C.

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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function or high-frequency canal stimulation. Scoliotic defor-mity may be induced by central otolithic vestibular imbal-ance, leading to an asymmetry of the tonic activity of the spinal muscles as suggested by Wiener-Vacher and Mazda, 29 who reported directional preponderance of the otolith VOR responses in off vertical axis rotation tests in AIS.

The slower velocity and longer latencies of the saccadic eye movements, observed in patients with mild scoliosis, support the hypothesis of a dysfunction at central level of the saccades processing. Saccade production can be altered at the level of the motoneurons. Popov and Gaı̆voronskiı̆ 46 suggested that changes in the spinal cord motoneurons activity are corre-lated to the scoliotic deformity of the spine. Same changes could occur at the level of the motoneurons of the ocular mus-cles and may explain the differences of velocity and latency that we observed in patients with mild and very mild scoliosis. This dysfunction could be progressive and may explain why it is found in mild AIS but not in very mild AIS.

The altered saccades that we observed in AIS could also come from the cerebellum that is also involved in saccades production. 47 Sun et al 48 assumed that a lower position of the cerebellar tonsil may play an important role in the etio-pathogenesis of AIS. Tonsillar ectopia is signifi cantly more

origin of the structural and behavioral deformities in humans as in the different animal models of scoliosis. However, in our study, teenagers with mild scoliosis did not show vestibular abnormalities in the tests performed. Teenagers with very mild scoliosis show higher relative directional preponderance without vestibular weakness at the caloric vestibular test that can support the hypothesis of a more central asymmetry. Our results are in accordance with those of Wiener-Vacher and Mazda 29 and Simoneau et al 45 who reported that the VOR was not impaired in patients with AIS. However, the hypoth-esis of a dysfunction of the vestibular end organ in AIS cannot be fully ruled out because we only tested the horizontal semi-circular canal function. Our study did not evaluate otolithic

TABLE 2. Saccades and Smooth-Pursuit Tests for Groups I (Very Mild Scoliosis) and II (Mild Scoliosis)

Group 1, n = 29

(Mean ± SD)

Group 2, n = 24

(Mean ± SD)Student t

Test, P

Saccades

Latency (ms)

Freyss sequence

247.64 ± 27.93 270.14 ± 46.88 t = − 2.14, P = 0.037

Alternated crenels

226.82 ± 36.21 236.79 ± 31.32 t = − 1.06, NS

Fixed sequence

200.50 ± 31.52 216.60 ± 36.83 t = − 1.70, NS

Velocity ( ° /s)

Freyss sequence

471.00 ± 69.47 427.27 ± 52.72 t = 2.52, P = 0.014

Alternated crenels

330.57 ± 57.30 301.98 ± 34.22 t = 2.22, P = 0.031

Fixed sequence

503.32 ± 71.59 464.79 ± 51.60 t = 2.19, P = 0.033

Accuracy (%)

Freyss sequence

95.07 ± 9.28 94.14 ± 5.00 t = 0.44, NS

Alternated crenels

95.75 ± 11.22 96.04 ± 6.00 t = − 0.11, NS

Fixed sequence

92.78 ± 9.49 92.17 ± 4.04 t = 0.30, NS

Smooth pursuit

Gain 0.70 ± 0.09 0.66 ± 0.11 t = 1.16, NS

Mean values and standard deviation for latency, velocity, and accuracy of the 3 saccades sequences (Freyss sequence: temporal uncertainty and predictive direction with only eccentric fi xation; alternated crenels: temporal uncer-tainty and predictive direction with central and eccentric fi xation; and fi xed sequence: predictive time and direction appearance) and for the gain of the smooth pursuit.

NS indicates not signifi cant.

TABLE 3. The Pendular Rotary Vestibular Testing for Groups I (Very Mild Scoliosis) and II (Mild Scoliosis)

Group 1, n = 29

(Mean ± SD)

Group 2, n = 24

(Mean ± SD)Student t

Test, P

Directional preponderance ( ° /s)

VVOR sequence

1.44 ± 1.17 2.08 ± 1.60 t = − 1.65, NS

VOR1 sequence

2.31 ± 1.82 2.69 ± 1.47 t = − 0.80, NS

Fixation sequence

1.18 ± 1.27 1.24 ± 0.75 t = − 0.20, NS

VOR2 sequence

1.78 ± 1.35 2.57 ± 2.01 t = − 1.68, NS

Total maximal slow-phase velocity ( ° /s)

VVOR sequence

103.66 ± 9.23 98.47 ± 6.72 t = 2.24, P = 0.029

VOR1 sequence

55.50 ± 11.83 54.89 ± 16.60 t = 0.15, NS

Fixation sequence

8.60 ± 3.59 9.73 ± 5.89 t = − 0.80, NS

VOR2 sequence

53.21 ± 15.65 57.26 ± 14.72 t = − 0.94, NS

Mean values and standard deviation for the response parameters (directional preponderance, total maximal slow-phase velocity) obtained during the 4 rotational sequences (VVOR, VOR1, fi xation, VOR2).

VVOR indicates visual vestibular ocular refl ex; NS, not signifi cant; VOR, vestibulo-ocular refl ex.

Copyright © 2013 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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In conclusion, this study showed in AIS groups with mild spine deformation of less than 25 ° Cobb angle that poorer eye movement performance recorded with commonly used video-oculography technique was related to higher Cobb angle. The latency and the velocity of the saccades were, respectively, higher and lower in the AIS group with larger spine deforma-tion. Alteration of the brainstem may be present and induce an impaired tonic activity of the spinal muscles leading to progressive scoliosis. To consider visuo-oculomotor rehabili-tation to eventually manage AIS, a prospective study is now required to see whether simple videonystagmographic param-eters have predictive value at the onset of AIS on the progres-sion of spinal deformation.

frequently ( ∼ 30%) found in patients with AIS who presented abnormal somatosensory function. 48 , 49 Disorders in the somatosensory function is suggested to be one of the mecha-nisms linking tonsillar ectopia to scoliosis. 49

The velocity of the horizontal saccades is mainly regu-lated by the activity of saccade-related excitatory burst neu-rons located in the brainstem (paramedian pontine reticu-lar formation). 50 These neurons project on vestibular nuclei inhibitory interneurons that inhibit the VOR. 51 , 52 It has been shown that brainstem lesions at the level of the vestibular nuclei induce scoliosis-like spinal deformities in adult rats in the acute phase after lesion but resolve with time. 53 An unbal-anced activity in central vestibular pathways has also been proposed in the AIS development. 29 , 30 Simoneau et al 45 sug-gested that severe spine deformity may develop partly through impaired vestibular signal traveling from the cerebellum to the vestibular cortical network or alteration of vestibular signal through the cortical processing mechanisms. Abnormalities of the saccades and scoliosis are genetically associated in some rare autosomal recessive syndromes, the horizontal gaze palsy with progressive scoliosis in which a congenital gaze restric-tion is coinherited with progressive scoliosis. Patients with horizontal gaze palsy with progressive scoliosis have normal-appearing cerebrum, corpus callosum, and cerebellum but abnormal fl attening of the pons and medulla, with an unusual midline medullary cleft, which results from an absence of nor-mal decussation of sensory and motor tracts on the ventral part of the hindbrain. 54 This congenital syndrome highlights the importance of the brainstem both in the spine and ocu-lomotor abnormalities. It could be suggested that teenagers with AIS yield mild brainstem dysfunction, including abnor-malities of decussation of sensory and motor tracts, which could be involved in scoliosis development. Nevertheless, this hypothesis remains controversial. 55

Oculomotor tasks are now largely used as powerful tools in the analysis of various cognitive processes, such as executive functions. AIS being not just an orthopedic condition, understanding precisely the cortical networks associated with different components of ocular movements can certainly be useful to characterize, test, and eventu-ally detect various kinds of neurological disorders. In this respect, using sophisticated experimental designs, ocu-lomotor tasks could allow a better understanding of AIS functional consequences and participate to the detection of the potential AIS causal factors at higher cerebral levels. In our study, the abnormalities are demonstrated for small deformations of the spine. These results may fi nd a clini-cal interest in the AIS management. The use of prismatic eye lenses has been previously recommended to infl uence posture, spatial perception, and central peripheral organi-zation. Indeed, the modifi cation of the visual information through the application of low-power prismatic lenses has been proposed to modify the skeletal muscle tone and the scoliotic attitude. 56 , 57 Nevertheless, our data cannot sup-port the AIS management through modifi cation of visual information.

➢ Key Points

Few studies have examined early-stage AIS. AIS is associated with an alteration of the visuo-

oculomotor function, especially the saccades, even for mild spine deformation of 15 to 25 ° Cobb angle.

These visuo-oculomotor impairments may refl ect disorders of the central nervous system existing in patients with AIS at disease onset.

These patients do not show vestibular canal abnormalities at low frequencies.

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