- Email: [email protected]
Dominant foot could affect the postural control in vestibular neuritis perceived by dynamic body balance
Gait & Posture 59 (2018) 157–161
Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
Dominant foot could affect the postural control in vestibular neuritis perceived by dynamic body balance
MARK
⁎
Tomoe Yoshida , Toshitake Tanaka, Yuya Tamura, Masahiko Yamamoto, Mitsuya Suzuki Department Otorhinolaryngology, Toho University, Sakura City, Japan
A R T I C L E I N F O
A B S T R A C T
Keywords: Vestibular neuritis Stabilometry Body tracking test Principal component analysis Tilt phenomenon
During attacks of vestibular neuritis (VN), patients typically lose postural balance, with resultant postural inclination, gait deviation toward the lesion side, and tendency to fall. In this study, we examined and analyzed static and dynamic postural control during attacks of VN to characterize differences in postural control between right and left VN. Subjects were patients diagnosed with VN at the Department of Otolaryngology, Toho University Sakura Medical Center, and underwent in-patient treatment. Twenty-five patients who had spontaneous nystagmus were assessed within 3 days after the onset; all were right-foot dominant. Right VN was detected in nine patients (men: 4, women: 5; mean age: 57.6 ± 17.08 years [range: 23–82]) and left VN in 16 patients (men: 10, women: 6; mean age: 58.4 ± 14.08 years [range: 23–85 years]); the percentages of canal paresis of right and left VN were 86.88 ± 18.1% and 86.02 ± 15.0%, respectively. Statistical comparisons were conducted using the independent t-test. In stabilometry, with eyes opened, no significant differences were found between patients with right and left VN. However, with eyes closed, the center of horizontal movement significantly shifted ipsilateral (p < 0.01). The differences in the lateral and anteroposterior body tracking test (BTT) were statistically significant (p = 0.0039 and p = 0.0376, respectively), with greater changes in cases with right VN. Thus, the dominant foot might contribute to the postural control mechanism.
1. Introduction Key signs and symptoms of vestibular neuritis include acute onset of rotatory vertigo lasting several days, horizontal spontaneous nystagmus (mostly with a rotatory component) toward the unaffected ear, a deviation of the subjective visual vertical toward the affected ear, postural imbalance with a tendency to fall toward the affected side of the ear, and nausea [1]. A definitive diagnosis of VN should be made by demonstrating canal paresis or paralysis on caloric testing. During stabilometry, patients with VN show a significantly greater outer circumferential area with eyes open than that in healthy individuals [2]. Values of total length of the movement and outer circumferential area increased in our results of stabilometry, suggesting the importance of visual information to stabilize balance. Gagey analyzed body balance function in patients with VN by measuring the sway of the center of gravity, and demonstrated that the sway distance and area in patients with VN was significantly greater than that of healthy individuals and that the horizontal center of gravity deviated more when compared to healthy individuals [3]. It has been reported that, during attacks, patients with VN showed ipsilateral deviation of their
⁎
center of gravity with eyes closed [4]. Angunsri et al. conducted gait analysis to assess dynamic body balance function in 92 patients, which included patients with VN [5]. As for integrated plantar pressure, in most cases with VN, it increases in the ipsilateral foot, suggesting that the body’s center of gravity could shift ipsilaterally during gait, as well. All of the reports have supported Fukuda’s deviation phenomenon. The righting reflex test is a fundamental test to examine postural control. Both dynamic and static body balance function tests have been introduced for the clinical evaluation of functional body balance. Stabilometry is used to examine and evaluate the static postural reflex. Dynamic body balance tests include Fukuda’s stepping test, the vertical writing test with eyes closed, the walking test, the tandem gait test, and others [6], and these are used in the clinical setting to primarily evaluate the deviation phenomenon and changes of plantar pressure and foot kinematics during the stance when walking [5]. During these attacks, patients typically lose postural balance, with resultant postural inclination, ipsilateral gait shift, and tendency to fall. We used equipment that applied both stabilometry and the body tracking test (BTT), a novel examination system, for the assessment of static and dynamic body balance function in patients with VN [7]. This system records and analyzes, in detail, center of pressure (COP)
Corresponding author at: Department of Otorhinolaryngology, Toho University Sakura Medical Center, Shimoshizu 564-1, Sakura City, Chiba, Japan. E-mail address: [email protected] (T. Yoshida).
http://dx.doi.org/10.1016/j.gaitpost.2017.10.001 Received 17 April 2017; Received in revised form 27 September 2017; Accepted 2 October 2017 0966-6362/ © 2017 Elsevier B.V. All rights reserved.
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
movements initiated while the subject tracks the movement of a visual target that moves on a screen at a constant speed in the vertical plane (anteroposterior [AP] BTT) or lateral direction (lateral BTT). BTT has been applied to estimate the overall dynamic postural control function using visual tracking and a spinal postural control system [7]. Few studies have explored procedures for assessing dynamic body balance function using moving visual stimuli and COP assessment. Therefore, in this study, we analyzed static and dynamic postural control during attacks of VN to characterize differences in posture control characteristics between right and left VN and the correlation with the patient’s dominant foot. Therefore, in this study, we examined and analyzed static and dynamic postural control during attacks of VN to compare the differences in posture control characteristics between right and left VN.
(Kyoto, Japan) [10]. Gain of the COP movement displayed on the screen is two times greater than the actual COP movement value according to past research [11]. Subjects were instructed to set their COP at the center of the coordinate, maintain foot position, and track the target in an upright posture. The actual recording was started 8 s after beginning the exercise.
2. Subjects and methods
2.3.2. BTT In the AP BTT and lateral BTT, the tracking of the visual stimulus for movement was displayed on a straight line, and the subjects tried to control their COP so COP movement was tracked in accordance with the movement of the target. Two-dimensional coordinates of the COP (x-axis: lateral direction, and y-axis: AP direction) sampled in each experimental session were analyzed using principal component analysis. The main axis of the tracking performance was evaluated as an eigenvector corresponding to the first principal component. In the lateral BTT, the subject’s tilt during the task was expressed as a displacement angle of the main axis from the x-axis, with clockwise tilt considered to be positive and counterclockwise tilt considered to be negative (Fig. 1, right figure). In the AP BTT, the subject’s tilt during the task was expressed as a displacement angle of the main axis from the yaxis, with clockwise and counterclockwise tilts considered to be positive and negative, respectively (Fig. 2).
2.3. Analysis 2.3.1. Stabilometry We checked the total length of the movement (cm), outer circumference area (enveloped area; cm2), locus length per unit area (1/ cm2), center of left-to-right movement (cm), and center of anteroposterior movement (cm).
2.1. Participants This retrospective study included patients who were diagnosed with VN and underwent inpatient treatment at a university medical center. Of the 102 patients with VN who were examined between May 2011 and September 2016, we investigated 25 patients who had spontaneous nystagmus and were assessed within 3 days of VN onset. All patients were right-foot dominant; the dominant foot was determined by interviewing subjects to confirm which foot was used to kick a ball [8]. Right VN was observed in nine patients (men: 4, women: 5; mean age: 57.6 ± 17.08 years [range: 23–82 years]) and left VN in 16 patients (men: 10, women: 6; mean age: 58.4 ± 14.08 years [range: 23–85 years]). The percentages of canal paresis (CP%) of right and left VN were 86.88 ± 18.1% and 86.02 ± 15.0%, respectively. The study protocol was approved by the ethics committee of our university (#S16044). We provided information to the patients on how to opt out of the research through our medical center’s website. For this type of study, formal consent was not required.
2.4. Statistical analysis Statistical comparisons were conducted using the independent t-test (Ekuseru–Toukei 2015, Social Survey Research Information Co., Ltd Tokyo, Japan). A p-value of < 0.05 was considered to be statistically significant.
2.2. Evaluation 3. Results In patients with VN, stabilometry was conducted with eyes open and closed, and BTT was conducted with eyes open. The method for BTT has been reported previously [7]. Briefly, the BTT equipment, as shown in Fig. 1, is composed of a stabilometer (ANIMA-G620, ANIMA Co. Tokyo, Japan) and a visual stimulus monitor. Although various recording conditions can be set for conducting a detailed examination, in the present study, we only applied the BTT to evaluate body tracking function in the AP and lateral directions. On the monitor screen, the moving visual stimulus was shown in green, whereas the position of the subject’s COP was shown in red. The moving visual stimulus and the subject’s COP appeared side-by-side on the display (Fig. 1, left figure). Each patient was asked to move his/her COP in accordance with the movement of the visually moving target, and the position of each movement was assessed. An upward movement on the AP BTT monitor reflected a forward direction of the COP, whereas a downward movement reflected a posterior direction. In the lateral BTT, right and left movements on the display reflected the same corresponding movements of the COP. Visual stimulation was administered at a constant frequency of 0.125 Hz, determined from previous experimental reports [9]. The analog/digital (A/D) converter recorded samples every 50 ms (20 Hz), and the AP BTT and lateral BTT were recorded for 60 s each. The distance between the target and the subject was set at 100 cm, and subjects stood with their feet closed parallel, while maintaining an upright posture. These test conditions are recommended by the Japan Society for Equilibrium Research
3.1. Stabilometry The results are shown in Table 1. With eyes open, no significant differences were detected between right and left VN with respect to the total length of the movement (cm), outer circumference area (enveloped area; cm2), locus length per unit area (l/cm), center of left-to-right movement (cm), and center of anteroposterior movement (cm). With eyes closed, significant differences in inclination were found with respect to the center of left-to-right movement (cm) on the ipsilateral side in patients with right or left VN (p < 0.01). Deviation was seen toward the affected side in stabilometry. 3.2. BTT Lateral BTT in the left VN group presented a clockwise tilt with a mean displacement angle of 2.6° ± 8.37°, whereas the group with right VN presented a somewhat counterclockwise tilt, with a mean displacement angle of −12.0° ± 10.2°; Fig. 3. This difference was found statistically significant with the independent t-test (p = 0.0039). However, the AP BTT in the left VN group presented a clockwise tilt with a mean displacement angle of 7.7° ± 9.6° whereas the group with right VN presented a somewhat counterclockwise tilt, with a mean displacement angle of −2.2° ± 9.5°; Fig. 4. This difference was statistically significant when evaluated with the independent t-test (p = 0.0376). 158
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Fig. 1. Body Tracking Test System and Monitor screen of BTT. A block diagram of the body tracking test (left figure) Monitor screen of the body tracking test system. The moving visual target is shown in green and the subject’s center of pressure (tracking graphic position) is shown in red (right figure). AP, anteroposterior.
COMPUTER
ANIMA G5500
Visual moving target
STABILOMETER
Lateral BTT
4. Discussion
anteroposterior spreading for horizontal tracking. In patients with VN, severely decreased or absent inner ear function is noted on the ipsilateral side. Moreover, muscle tonus on this side decreases mainly through the lateral vestibulospinal tract, and ipsilateral deviation is observed on stabilometry. Fujimoto reported that patients with VN show poor postural performance, which is affected by age, residual vestibular function, and disease duration [14]. Therefore, in this study, we included only patients with spontaneous nystagmus who had undergone testing within 3 days of VN onset. There was no significant difference between age and CP% in left and right VN. Ramon et al. conducted studies using the posturographic NedSVE/IBV system, combining static (Romberg) and dynamic (stability limits and rhythmic weight shifts) tests and stated that rhythmic weight-shift tests and the static posturography test parameters used were useful in differentiating between normal and pathological subjects [15]. Alessandrini et al. [16] investigated vestibular compensation in cases of unilateral VN. They reported that with the onset of VN, the patients exhibited significantly increased classic posturographic parameters (e.g., length, surface area, and mean velocity of COP) compared to controls. Reflex activity is the basis of postural control and contraction of muscles in the lower limbs mostly causes postural sway [16]. Our spectral frequency analysis indicated
In our analysis of static and dynamic postural control during attacks of VN, we demonstrated differences in posture control between right and left VN. Kasahara et al. conducted an investigation using the same visual feedback. This method required that the target and their weight loads should be matched using visual feedback displayed on a computer monitor [12]. The subject’s COP tracking function of the moving visual stimulus is important for evaluation of dynamic balance. In a previous experiment, it was shown that the AP BTT in healthy subjects with right foot dominance had a clockwise tilt [13]. The AP BTT showed that the dominant foot could affect the tilt angle of the sway movement, as elucidated by principal component analysis. In another previous study, in order to confirm the mechanism by which the subject adjusted the COP while tracking a visual target, principal component analysis was employed. Movements of the visual target were only displayed on x- or y-axes (i.e., purely vertical and horizontal planes), and subjects could not recognize the tilt of their own movement axis. However, the actual COP position is recorded in two dimensions (Y and X axes). Therefore, COP movement exhibits an elliptical statokinesigram (Skg), with some horizontal spreading for anteroposterior tracking, and an elliptical Skg, with some
Fig. 2. Representative schemata of center of pressure movement obtained by the anteroposterior (AP) body tracking test (BTT) (a) and lateral BTT (b) in a patient with right-foot dominance. The tilt angle calculated by principal component analysis in each figure is indicated by a red line. In this case, clockwise tilt is shown in both AP BTT and lateral BTT. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Main axis analysis (principal component analysis) is an analytical method for determining the direction of the tilt of the main axis of COP locus during tracking (first principal component). The sample is showing a clockwise rotation axis (displacement angle is positive).
159
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Table 1 Results of stabilometry. Affected side
right left
right left
total length of the movement (cm)
locus length per unit area (1/cm2)
outer circumference area (cm2)
center of left to right movement (cm)
center of anterior to posterior movement (cm)
mean SD mean SD
Eyes open 134.7 71.6 131.9 48.2
22.7 9.3 20.7 5.8
6.4 2.8 6.0 2.3
−0.4 0.4 0.1 0.7
−0.8 1.3 −0.4 1.0
mean SD mean SD
Eyes closed 231.0 143.0 206.9 93.0
20.0 8.9 20.9 13.7
14.3 9.5 14.6 12.3
0.6 0.9 −0.7 0.8
−0.5 1.9 −0.1 1.3
Note: With eyes closed, significant differences (p < 0.01) were found with respect to the center of left-to-right movement (cm) between subjects with right and left VN.
the postural control mechanism with a unilateral peripheral vestibular lesion can be modulated by the dominant foot, especially when the lesion is ipsilateral to the dominant foot. Moreover, this factor may affect the prognosis of postural balance function to some extent in patients with VN. Therefore, these aspects must be taken into consideration to understand the postural control mechanism.
significantly increased body sway in the x and y planes at low frequencies. Lateral BTT and AP BTT revealed that tilt in patients with left VN is positive and forms a clockwise displacement angle, whereas tilt in patients with right VN is negative and forms a counterclockwise displacement angle. This phenomenon may be associated with conducting tracking while correcting the deviation phenomenon associated with ipsilateral lesions. We believe that during the performance of lateral BTT, the toe primarily has a role in maintaining balance for this task. As shown in Fig. 3, no marked change occurred with regard to the rotation of the axis in patients with left VN, whereas the axis significantly rotated in a counterclockwise direction in patients with right VN. These results may reflect the following mechanism. In patients with right VN, the dominant toe cannot completely control balance due to ipsilateral decrement in muscle tonus owing to lesions in the vestibulospinal tract. Therefore, fine control should be entrusted to the nondominant left toe. However, in patients with left VN, lesion-induced postural compromise can be well controlled by the intact dominant toe. Therefore, this parameter had only minute differences in affected compared to unaffected individuals [7]. Furthermore, we propose that during AP BTT, the main control of posture is mediated by the toe and heel. This process results in a similar tendency for axis rotation as with lateral tracking (Fig. 4). Postural control by the dominant right foot may be exaggerated to some extent in patients with left VN, which may result in a greater clockwise rotation of the axis to some extent compared to controls with right-foot dominance [7]. In patients with right VN, the COP control during this task may be shifted to the left non-dominant forefoot. Thus,
5. Conclusion Static and dynamic postural control during attacks in VN in patients with spontaneous nystagmus and right-foot dominance showed a significant ipsilateral shift in the center of horizontal movement. Thus, the dominant foot might modulate the postural control mechanism. The incidence of left-foot dominance is generally very low in the population; consequently, the number of left-foot dominant patients would be small. Therefore, a limitation of this study was that we could not include any left-foot dominant patients with VN. Future research should be aimed at investigating differences in the prognosis, based on the affected side, in right-foot dominant patients. Patient details Patients diagnosed with VN underwent inpatient treatment at the Department of Otolaryngology, at Toho University Sakura Medical Center (Chiba, Japan). This retrospective study included patients who were diagnosed with VN and underwent inpatient treatment at the Department of Otolaryngology in Toho University Sakura Medical Center (Chiba, Japan). The study protocol was approved by the ethics Fig. 3. Main axis analysis of left and right VN (lateral BTT). The differences in lateral BTT between right and left VN was statistically significant on analysis using the independent ttest (p = 0.0039).
160
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Fig. 4. Main axis analysis of left and right VN (AP BTT). Differences between AP BTT in subjects with right or left VN were statistically significant on analysis using the independent t-test (p = 0.0376).
[5] N. Angunsri, K. Ishikawa, M. Yin, E. Omi, Y. Shibata, T. Saito, Y. Itasaka, Gait instability caused by vestibular disorders-analysis by tactile sensor, Auris Nasus Larynx 38 (2011) 462–468. [6] T. Fukuda, Statokinetic Reflexes in Equilibrium and Movement, University of Tokyo Press, 1984, pp. 110–123. [7] T. Yoshida, F. Ikemiyagi, Y. Ikemiyagi, T. Tanaka, M. Yamamoto, M. Suzuki, The dominant foot affects the postural control mechanism: examination by body tracking test, Acta Otolaryngol. 134 (2014) 1146–1150. [8] A.G. Schneiders, S.J. Sullivan, K.J. O'Malley, S.V. Clarke, S.A. Knappstein, L.J.A. Taylor, Valid and reliable clinical determination of footedness, PM. R. 2 (2010) 835–841. [9] T. Yoshida, M. Oda, C. Koike, R. Ichijima, M. Yamamoto, J. Takeuchi, The optical target speed of the Body Tracking Test (BTT)-The test condition for the BTT-No2-, Equilib. Res. 55 (1996) 436–441. [10] Japan Society of Equilibrium Research, Standard of center of gravity sway evaluation, Equilib. Res. 42 (1983) 367–369. [11] T. Yoshida, M. Oda, H. Takahashi, S. Sasaki, M. Yamamoto, J. Takeuchi, The relationship for target and tracking of the body tracking test (BTT)—the test condition for the BTT-No1, Equilib. Res. 55 (1996) 343–348. [12] S. Kasahara, H. Saito, Effect of loading parameters on motor performance during a dynamic weight-shift task, Gait Posture 41 (2015) 100–105. [13] T. Yoshida, F. Ikemiyagi, Y. Ikemiyagi, T. Tnaka, T. Takanami, Y. Tamura, M. Yamamoto, M. Suzuki, Tracking axis of the body tracking test (BTT), Nihon Jibiinkoka Gakkai Kaiho 116 (2013) 1308–1313. [14] C. Fujimoto, N. Egami, M. Kinoshita, K. Sugasawa, T. Yamasoba, S. Iwasaki, Postural stability in vestibular neuritis: age, disease duration, and residual vestibular function, Laryngoscope 124 (2014) 974–979. [15] R. Ramón Balaguer García, S. Pitarch Corresa, J.M. Baydal Bertomeu, M.M. Morales Suárez-Varela, Static posturography with dynamic tests. Usefulness of biomechanical parameters in assessing vestibular patientsl, Acta Otorrinolaringol. Esp. 63 (2012) 332–338. [16] M. Alessandrini, G. D'Erme, E. Bruno, B. Napolitano, A. Magrini, Vestibular compensation: analysis of postural re-arrangement as a control index for unilateral vestibular deficit, Neuroreport 14 (2003) 1075–1079.
committee of our university (approval number #S16044). We had provided opt out information about this research on the homepage of Toho University Sakura Medical Center (Chiba, Japan). Funding None. Conflict of interest statement There are no conflicts of interest to declare. Acknowledgement We would like to thank Editage (www.editage.com) for English language editing and Publication Support. References [1] M. Strupp, T. Brandt, Vestibular neuritis, Semin. Neurol. 29 (2009) 509–519. [2] S. Ota, Study on center of gravity sway test results in patients with unilateral peripheral vestibular disorder-focusing on the characteristics of center of gravity sway in various nystagmus expression period, J. Otolaryng. Japn. 90 (1987) 80–89. [3] P.M. Gagey, M. Toupet, Orthostatic postural control in vestibular neuritis: a stabilometric analysis, Ann. Otol. Rhinol. Laryngol. 100 (1991) 971–975. [4] T. Yoshida, M. Yamamoto, T. Nomura, S. Ohwada, R. Takazawa, Y. Ikemiyagi, F. Shigeta, Examination of dynamic body balance using the body tracking test in cases of vestibular neuronitis, Nihon Jibiinkoka Gakkai Kaiho 111 (2008) 617–622.
161
Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
Dominant foot could affect the postural control in vestibular neuritis perceived by dynamic body balance
MARK
⁎
Tomoe Yoshida , Toshitake Tanaka, Yuya Tamura, Masahiko Yamamoto, Mitsuya Suzuki Department Otorhinolaryngology, Toho University, Sakura City, Japan
A R T I C L E I N F O
A B S T R A C T
Keywords: Vestibular neuritis Stabilometry Body tracking test Principal component analysis Tilt phenomenon
During attacks of vestibular neuritis (VN), patients typically lose postural balance, with resultant postural inclination, gait deviation toward the lesion side, and tendency to fall. In this study, we examined and analyzed static and dynamic postural control during attacks of VN to characterize differences in postural control between right and left VN. Subjects were patients diagnosed with VN at the Department of Otolaryngology, Toho University Sakura Medical Center, and underwent in-patient treatment. Twenty-five patients who had spontaneous nystagmus were assessed within 3 days after the onset; all were right-foot dominant. Right VN was detected in nine patients (men: 4, women: 5; mean age: 57.6 ± 17.08 years [range: 23–82]) and left VN in 16 patients (men: 10, women: 6; mean age: 58.4 ± 14.08 years [range: 23–85 years]); the percentages of canal paresis of right and left VN were 86.88 ± 18.1% and 86.02 ± 15.0%, respectively. Statistical comparisons were conducted using the independent t-test. In stabilometry, with eyes opened, no significant differences were found between patients with right and left VN. However, with eyes closed, the center of horizontal movement significantly shifted ipsilateral (p < 0.01). The differences in the lateral and anteroposterior body tracking test (BTT) were statistically significant (p = 0.0039 and p = 0.0376, respectively), with greater changes in cases with right VN. Thus, the dominant foot might contribute to the postural control mechanism.
1. Introduction Key signs and symptoms of vestibular neuritis include acute onset of rotatory vertigo lasting several days, horizontal spontaneous nystagmus (mostly with a rotatory component) toward the unaffected ear, a deviation of the subjective visual vertical toward the affected ear, postural imbalance with a tendency to fall toward the affected side of the ear, and nausea [1]. A definitive diagnosis of VN should be made by demonstrating canal paresis or paralysis on caloric testing. During stabilometry, patients with VN show a significantly greater outer circumferential area with eyes open than that in healthy individuals [2]. Values of total length of the movement and outer circumferential area increased in our results of stabilometry, suggesting the importance of visual information to stabilize balance. Gagey analyzed body balance function in patients with VN by measuring the sway of the center of gravity, and demonstrated that the sway distance and area in patients with VN was significantly greater than that of healthy individuals and that the horizontal center of gravity deviated more when compared to healthy individuals [3]. It has been reported that, during attacks, patients with VN showed ipsilateral deviation of their
⁎
center of gravity with eyes closed [4]. Angunsri et al. conducted gait analysis to assess dynamic body balance function in 92 patients, which included patients with VN [5]. As for integrated plantar pressure, in most cases with VN, it increases in the ipsilateral foot, suggesting that the body’s center of gravity could shift ipsilaterally during gait, as well. All of the reports have supported Fukuda’s deviation phenomenon. The righting reflex test is a fundamental test to examine postural control. Both dynamic and static body balance function tests have been introduced for the clinical evaluation of functional body balance. Stabilometry is used to examine and evaluate the static postural reflex. Dynamic body balance tests include Fukuda’s stepping test, the vertical writing test with eyes closed, the walking test, the tandem gait test, and others [6], and these are used in the clinical setting to primarily evaluate the deviation phenomenon and changes of plantar pressure and foot kinematics during the stance when walking [5]. During these attacks, patients typically lose postural balance, with resultant postural inclination, ipsilateral gait shift, and tendency to fall. We used equipment that applied both stabilometry and the body tracking test (BTT), a novel examination system, for the assessment of static and dynamic body balance function in patients with VN [7]. This system records and analyzes, in detail, center of pressure (COP)
Corresponding author at: Department of Otorhinolaryngology, Toho University Sakura Medical Center, Shimoshizu 564-1, Sakura City, Chiba, Japan. E-mail address: [email protected] (T. Yoshida).
http://dx.doi.org/10.1016/j.gaitpost.2017.10.001 Received 17 April 2017; Received in revised form 27 September 2017; Accepted 2 October 2017 0966-6362/ © 2017 Elsevier B.V. All rights reserved.
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
movements initiated while the subject tracks the movement of a visual target that moves on a screen at a constant speed in the vertical plane (anteroposterior [AP] BTT) or lateral direction (lateral BTT). BTT has been applied to estimate the overall dynamic postural control function using visual tracking and a spinal postural control system [7]. Few studies have explored procedures for assessing dynamic body balance function using moving visual stimuli and COP assessment. Therefore, in this study, we analyzed static and dynamic postural control during attacks of VN to characterize differences in posture control characteristics between right and left VN and the correlation with the patient’s dominant foot. Therefore, in this study, we examined and analyzed static and dynamic postural control during attacks of VN to compare the differences in posture control characteristics between right and left VN.
(Kyoto, Japan) [10]. Gain of the COP movement displayed on the screen is two times greater than the actual COP movement value according to past research [11]. Subjects were instructed to set their COP at the center of the coordinate, maintain foot position, and track the target in an upright posture. The actual recording was started 8 s after beginning the exercise.
2. Subjects and methods
2.3.2. BTT In the AP BTT and lateral BTT, the tracking of the visual stimulus for movement was displayed on a straight line, and the subjects tried to control their COP so COP movement was tracked in accordance with the movement of the target. Two-dimensional coordinates of the COP (x-axis: lateral direction, and y-axis: AP direction) sampled in each experimental session were analyzed using principal component analysis. The main axis of the tracking performance was evaluated as an eigenvector corresponding to the first principal component. In the lateral BTT, the subject’s tilt during the task was expressed as a displacement angle of the main axis from the x-axis, with clockwise tilt considered to be positive and counterclockwise tilt considered to be negative (Fig. 1, right figure). In the AP BTT, the subject’s tilt during the task was expressed as a displacement angle of the main axis from the yaxis, with clockwise and counterclockwise tilts considered to be positive and negative, respectively (Fig. 2).
2.3. Analysis 2.3.1. Stabilometry We checked the total length of the movement (cm), outer circumference area (enveloped area; cm2), locus length per unit area (1/ cm2), center of left-to-right movement (cm), and center of anteroposterior movement (cm).
2.1. Participants This retrospective study included patients who were diagnosed with VN and underwent inpatient treatment at a university medical center. Of the 102 patients with VN who were examined between May 2011 and September 2016, we investigated 25 patients who had spontaneous nystagmus and were assessed within 3 days of VN onset. All patients were right-foot dominant; the dominant foot was determined by interviewing subjects to confirm which foot was used to kick a ball [8]. Right VN was observed in nine patients (men: 4, women: 5; mean age: 57.6 ± 17.08 years [range: 23–82 years]) and left VN in 16 patients (men: 10, women: 6; mean age: 58.4 ± 14.08 years [range: 23–85 years]). The percentages of canal paresis (CP%) of right and left VN were 86.88 ± 18.1% and 86.02 ± 15.0%, respectively. The study protocol was approved by the ethics committee of our university (#S16044). We provided information to the patients on how to opt out of the research through our medical center’s website. For this type of study, formal consent was not required.
2.4. Statistical analysis Statistical comparisons were conducted using the independent t-test (Ekuseru–Toukei 2015, Social Survey Research Information Co., Ltd Tokyo, Japan). A p-value of < 0.05 was considered to be statistically significant.
2.2. Evaluation 3. Results In patients with VN, stabilometry was conducted with eyes open and closed, and BTT was conducted with eyes open. The method for BTT has been reported previously [7]. Briefly, the BTT equipment, as shown in Fig. 1, is composed of a stabilometer (ANIMA-G620, ANIMA Co. Tokyo, Japan) and a visual stimulus monitor. Although various recording conditions can be set for conducting a detailed examination, in the present study, we only applied the BTT to evaluate body tracking function in the AP and lateral directions. On the monitor screen, the moving visual stimulus was shown in green, whereas the position of the subject’s COP was shown in red. The moving visual stimulus and the subject’s COP appeared side-by-side on the display (Fig. 1, left figure). Each patient was asked to move his/her COP in accordance with the movement of the visually moving target, and the position of each movement was assessed. An upward movement on the AP BTT monitor reflected a forward direction of the COP, whereas a downward movement reflected a posterior direction. In the lateral BTT, right and left movements on the display reflected the same corresponding movements of the COP. Visual stimulation was administered at a constant frequency of 0.125 Hz, determined from previous experimental reports [9]. The analog/digital (A/D) converter recorded samples every 50 ms (20 Hz), and the AP BTT and lateral BTT were recorded for 60 s each. The distance between the target and the subject was set at 100 cm, and subjects stood with their feet closed parallel, while maintaining an upright posture. These test conditions are recommended by the Japan Society for Equilibrium Research
3.1. Stabilometry The results are shown in Table 1. With eyes open, no significant differences were detected between right and left VN with respect to the total length of the movement (cm), outer circumference area (enveloped area; cm2), locus length per unit area (l/cm), center of left-to-right movement (cm), and center of anteroposterior movement (cm). With eyes closed, significant differences in inclination were found with respect to the center of left-to-right movement (cm) on the ipsilateral side in patients with right or left VN (p < 0.01). Deviation was seen toward the affected side in stabilometry. 3.2. BTT Lateral BTT in the left VN group presented a clockwise tilt with a mean displacement angle of 2.6° ± 8.37°, whereas the group with right VN presented a somewhat counterclockwise tilt, with a mean displacement angle of −12.0° ± 10.2°; Fig. 3. This difference was found statistically significant with the independent t-test (p = 0.0039). However, the AP BTT in the left VN group presented a clockwise tilt with a mean displacement angle of 7.7° ± 9.6° whereas the group with right VN presented a somewhat counterclockwise tilt, with a mean displacement angle of −2.2° ± 9.5°; Fig. 4. This difference was statistically significant when evaluated with the independent t-test (p = 0.0376). 158
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Fig. 1. Body Tracking Test System and Monitor screen of BTT. A block diagram of the body tracking test (left figure) Monitor screen of the body tracking test system. The moving visual target is shown in green and the subject’s center of pressure (tracking graphic position) is shown in red (right figure). AP, anteroposterior.
COMPUTER
ANIMA G5500
Visual moving target
STABILOMETER
Lateral BTT
4. Discussion
anteroposterior spreading for horizontal tracking. In patients with VN, severely decreased or absent inner ear function is noted on the ipsilateral side. Moreover, muscle tonus on this side decreases mainly through the lateral vestibulospinal tract, and ipsilateral deviation is observed on stabilometry. Fujimoto reported that patients with VN show poor postural performance, which is affected by age, residual vestibular function, and disease duration [14]. Therefore, in this study, we included only patients with spontaneous nystagmus who had undergone testing within 3 days of VN onset. There was no significant difference between age and CP% in left and right VN. Ramon et al. conducted studies using the posturographic NedSVE/IBV system, combining static (Romberg) and dynamic (stability limits and rhythmic weight shifts) tests and stated that rhythmic weight-shift tests and the static posturography test parameters used were useful in differentiating between normal and pathological subjects [15]. Alessandrini et al. [16] investigated vestibular compensation in cases of unilateral VN. They reported that with the onset of VN, the patients exhibited significantly increased classic posturographic parameters (e.g., length, surface area, and mean velocity of COP) compared to controls. Reflex activity is the basis of postural control and contraction of muscles in the lower limbs mostly causes postural sway [16]. Our spectral frequency analysis indicated
In our analysis of static and dynamic postural control during attacks of VN, we demonstrated differences in posture control between right and left VN. Kasahara et al. conducted an investigation using the same visual feedback. This method required that the target and their weight loads should be matched using visual feedback displayed on a computer monitor [12]. The subject’s COP tracking function of the moving visual stimulus is important for evaluation of dynamic balance. In a previous experiment, it was shown that the AP BTT in healthy subjects with right foot dominance had a clockwise tilt [13]. The AP BTT showed that the dominant foot could affect the tilt angle of the sway movement, as elucidated by principal component analysis. In another previous study, in order to confirm the mechanism by which the subject adjusted the COP while tracking a visual target, principal component analysis was employed. Movements of the visual target were only displayed on x- or y-axes (i.e., purely vertical and horizontal planes), and subjects could not recognize the tilt of their own movement axis. However, the actual COP position is recorded in two dimensions (Y and X axes). Therefore, COP movement exhibits an elliptical statokinesigram (Skg), with some horizontal spreading for anteroposterior tracking, and an elliptical Skg, with some
Fig. 2. Representative schemata of center of pressure movement obtained by the anteroposterior (AP) body tracking test (BTT) (a) and lateral BTT (b) in a patient with right-foot dominance. The tilt angle calculated by principal component analysis in each figure is indicated by a red line. In this case, clockwise tilt is shown in both AP BTT and lateral BTT. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Main axis analysis (principal component analysis) is an analytical method for determining the direction of the tilt of the main axis of COP locus during tracking (first principal component). The sample is showing a clockwise rotation axis (displacement angle is positive).
159
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Table 1 Results of stabilometry. Affected side
right left
right left
total length of the movement (cm)
locus length per unit area (1/cm2)
outer circumference area (cm2)
center of left to right movement (cm)
center of anterior to posterior movement (cm)
mean SD mean SD
Eyes open 134.7 71.6 131.9 48.2
22.7 9.3 20.7 5.8
6.4 2.8 6.0 2.3
−0.4 0.4 0.1 0.7
−0.8 1.3 −0.4 1.0
mean SD mean SD
Eyes closed 231.0 143.0 206.9 93.0
20.0 8.9 20.9 13.7
14.3 9.5 14.6 12.3
0.6 0.9 −0.7 0.8
−0.5 1.9 −0.1 1.3
Note: With eyes closed, significant differences (p < 0.01) were found with respect to the center of left-to-right movement (cm) between subjects with right and left VN.
the postural control mechanism with a unilateral peripheral vestibular lesion can be modulated by the dominant foot, especially when the lesion is ipsilateral to the dominant foot. Moreover, this factor may affect the prognosis of postural balance function to some extent in patients with VN. Therefore, these aspects must be taken into consideration to understand the postural control mechanism.
significantly increased body sway in the x and y planes at low frequencies. Lateral BTT and AP BTT revealed that tilt in patients with left VN is positive and forms a clockwise displacement angle, whereas tilt in patients with right VN is negative and forms a counterclockwise displacement angle. This phenomenon may be associated with conducting tracking while correcting the deviation phenomenon associated with ipsilateral lesions. We believe that during the performance of lateral BTT, the toe primarily has a role in maintaining balance for this task. As shown in Fig. 3, no marked change occurred with regard to the rotation of the axis in patients with left VN, whereas the axis significantly rotated in a counterclockwise direction in patients with right VN. These results may reflect the following mechanism. In patients with right VN, the dominant toe cannot completely control balance due to ipsilateral decrement in muscle tonus owing to lesions in the vestibulospinal tract. Therefore, fine control should be entrusted to the nondominant left toe. However, in patients with left VN, lesion-induced postural compromise can be well controlled by the intact dominant toe. Therefore, this parameter had only minute differences in affected compared to unaffected individuals [7]. Furthermore, we propose that during AP BTT, the main control of posture is mediated by the toe and heel. This process results in a similar tendency for axis rotation as with lateral tracking (Fig. 4). Postural control by the dominant right foot may be exaggerated to some extent in patients with left VN, which may result in a greater clockwise rotation of the axis to some extent compared to controls with right-foot dominance [7]. In patients with right VN, the COP control during this task may be shifted to the left non-dominant forefoot. Thus,
5. Conclusion Static and dynamic postural control during attacks in VN in patients with spontaneous nystagmus and right-foot dominance showed a significant ipsilateral shift in the center of horizontal movement. Thus, the dominant foot might modulate the postural control mechanism. The incidence of left-foot dominance is generally very low in the population; consequently, the number of left-foot dominant patients would be small. Therefore, a limitation of this study was that we could not include any left-foot dominant patients with VN. Future research should be aimed at investigating differences in the prognosis, based on the affected side, in right-foot dominant patients. Patient details Patients diagnosed with VN underwent inpatient treatment at the Department of Otolaryngology, at Toho University Sakura Medical Center (Chiba, Japan). This retrospective study included patients who were diagnosed with VN and underwent inpatient treatment at the Department of Otolaryngology in Toho University Sakura Medical Center (Chiba, Japan). The study protocol was approved by the ethics Fig. 3. Main axis analysis of left and right VN (lateral BTT). The differences in lateral BTT between right and left VN was statistically significant on analysis using the independent ttest (p = 0.0039).
160
Gait & Posture 59 (2018) 157–161
T. Yoshida et al.
Fig. 4. Main axis analysis of left and right VN (AP BTT). Differences between AP BTT in subjects with right or left VN were statistically significant on analysis using the independent t-test (p = 0.0376).
[5] N. Angunsri, K. Ishikawa, M. Yin, E. Omi, Y. Shibata, T. Saito, Y. Itasaka, Gait instability caused by vestibular disorders-analysis by tactile sensor, Auris Nasus Larynx 38 (2011) 462–468. [6] T. Fukuda, Statokinetic Reflexes in Equilibrium and Movement, University of Tokyo Press, 1984, pp. 110–123. [7] T. Yoshida, F. Ikemiyagi, Y. Ikemiyagi, T. Tanaka, M. Yamamoto, M. Suzuki, The dominant foot affects the postural control mechanism: examination by body tracking test, Acta Otolaryngol. 134 (2014) 1146–1150. [8] A.G. Schneiders, S.J. Sullivan, K.J. O'Malley, S.V. Clarke, S.A. Knappstein, L.J.A. Taylor, Valid and reliable clinical determination of footedness, PM. R. 2 (2010) 835–841. [9] T. Yoshida, M. Oda, C. Koike, R. Ichijima, M. Yamamoto, J. Takeuchi, The optical target speed of the Body Tracking Test (BTT)-The test condition for the BTT-No2-, Equilib. Res. 55 (1996) 436–441. [10] Japan Society of Equilibrium Research, Standard of center of gravity sway evaluation, Equilib. Res. 42 (1983) 367–369. [11] T. Yoshida, M. Oda, H. Takahashi, S. Sasaki, M. Yamamoto, J. Takeuchi, The relationship for target and tracking of the body tracking test (BTT)—the test condition for the BTT-No1, Equilib. Res. 55 (1996) 343–348. [12] S. Kasahara, H. Saito, Effect of loading parameters on motor performance during a dynamic weight-shift task, Gait Posture 41 (2015) 100–105. [13] T. Yoshida, F. Ikemiyagi, Y. Ikemiyagi, T. Tnaka, T. Takanami, Y. Tamura, M. Yamamoto, M. Suzuki, Tracking axis of the body tracking test (BTT), Nihon Jibiinkoka Gakkai Kaiho 116 (2013) 1308–1313. [14] C. Fujimoto, N. Egami, M. Kinoshita, K. Sugasawa, T. Yamasoba, S. Iwasaki, Postural stability in vestibular neuritis: age, disease duration, and residual vestibular function, Laryngoscope 124 (2014) 974–979. [15] R. Ramón Balaguer García, S. Pitarch Corresa, J.M. Baydal Bertomeu, M.M. Morales Suárez-Varela, Static posturography with dynamic tests. Usefulness of biomechanical parameters in assessing vestibular patientsl, Acta Otorrinolaringol. Esp. 63 (2012) 332–338. [16] M. Alessandrini, G. D'Erme, E. Bruno, B. Napolitano, A. Magrini, Vestibular compensation: analysis of postural re-arrangement as a control index for unilateral vestibular deficit, Neuroreport 14 (2003) 1075–1079.
committee of our university (approval number #S16044). We had provided opt out information about this research on the homepage of Toho University Sakura Medical Center (Chiba, Japan). Funding None. Conflict of interest statement There are no conflicts of interest to declare. Acknowledgement We would like to thank Editage (www.editage.com) for English language editing and Publication Support. References [1] M. Strupp, T. Brandt, Vestibular neuritis, Semin. Neurol. 29 (2009) 509–519. [2] S. Ota, Study on center of gravity sway test results in patients with unilateral peripheral vestibular disorder-focusing on the characteristics of center of gravity sway in various nystagmus expression period, J. Otolaryng. Japn. 90 (1987) 80–89. [3] P.M. Gagey, M. Toupet, Orthostatic postural control in vestibular neuritis: a stabilometric analysis, Ann. Otol. Rhinol. Laryngol. 100 (1991) 971–975. [4] T. Yoshida, M. Yamamoto, T. Nomura, S. Ohwada, R. Takazawa, Y. Ikemiyagi, F. Shigeta, Examination of dynamic body balance using the body tracking test in cases of vestibular neuronitis, Nihon Jibiinkoka Gakkai Kaiho 111 (2008) 617–622.
161