Immediate Effect of an Intervention Using a Head-mounted Display with a Modified Pitch Angle on Spatial Awareness and Standing Balance in Stroke Hemiparesis

ABSTRACT

Objectives: This study aimed to clarify the effect of an intervention using a head-mounted display with a web camera set at a modified pitch angle on spatial awareness, sit-to-stand movement, and standing balance in patients with left and right hemisphere damage.

Methods: The participants were 12 patients with right hemisphere damage and 12 patients with left hemisphere damage. The line bisection test, a sit-to-stand movement, and balance assessment were performed before and after the intervention. The intervention task involved pointing at targets 48 times in an upward bias condition.

Results: Significant upward deviation on the line bisection test was noted in patients with right hemisphere damage. The load on the forefoot during the sit-to-stand movement was significantly increased. The range of anterior–posterior sway during forward movement in the balance assessment was reduced.

Conclusions: An adaptation task performed in an upward bias condition may produce an immediate effect on upward localization, sit-to-stand movement, and balance performance in patients with right hemisphere stroke.

INTRODUCTION

Patients with cerebrovascular disease have difficulty performing sit-to-stand (STS)¹⁾ movements and maintaining their balance.²⁾ Patients with right hemisphere damage are more likely to have impaired perception of their visual and postural vertical space^3,4) than patients with left hemisphere damage. They are also more likely to have an unstable sitting posture and more frequent falls than those with left hemisphere damage.⁵⁾ Bonuzzi et al. studied motor learning in healthy older adults and patients with right or left hemisphere damage and reported that those with right hemisphere damage had difficulty in learning motor skills.⁶⁾

Right hemisphere damage often induces unilateral spatial neglect (USN). It is characterized by impaired responses to stimuli on the contralateral side of the injured hemisphere.⁷⁾ In the line bisection test, patients with left USN often show deviation to the right.⁸⁾ Mihulowicz et al. assessed vertical localization in the line bisection test in patients with USN and reported that the localization position was above the midline.⁹⁾ A vertical localization above the midline has been observed in healthy older adults,¹⁰⁾ patients with right hemisphere damage,¹¹⁾ and patients with USN. Among them, patients with USN are especially prone to loss of sitting balance¹²⁾ and may require assistance for performing their daily activities.

Prism adaptation (PA) is a method developed by Rossetti et al. in which the participant repeatedly touches a target while wearing prismatic glasses that “deflect the visual field to the right by 10 degrees”.¹³⁾ Straight-ahead pointing (SAP) is performed to confirm the establishment of PA. In SAP, the participant is asked to point their right index finger straight ahead after they touch it to the center of their sternum with their eyes closed. The participant then points to a position in the horizontal plane that they perceive to be in front of the middle of the trunk.¹⁴⁾ Rossetti et al. reported that in patients with USN, SAP positions localized to the right became changed to the left after PA.¹³⁾ Tilikete et al. reported that the center of pressure (COP) in the upright position in patients with left hemiplegia was improved from the right to the left after PA.¹⁵⁾ Frassinetti et al. proposed that PA involves the reorganization of higher-order spatial representation through adaptation between vision and motion.¹⁶⁾ Jacquin-Courtois et al. indicated that PA could be generalized to other sensory modalities such as auditory orientation and tactile perception,¹⁷⁾ while Bultitude et al. reported an improvement in local attention bias, a non-directional attentional function, after PA.¹⁸⁾

Many studies of PA in cases of USN have been performed by deflecting the visual field in the horizontal plane (yaw angle); however, there are no studies on adaptation achieved by deflecting the visual field in the sagittal plane (pitch angle). Using a head-mounted display (HMD) with a web camera, it is possible to deflect the visual field in the sagittal plane. It is important to examine the effects on spatial awareness, STS movement, and standing balance when performing the adaptation task with deflection not only in the horizontal plane but also in the sagittal plane.

Forward movement of the COP is needed to control the balance as the buttocks are lifted from the seat in the extension phase of a STS movement.¹⁹⁾ Given that PA in the horizontal plane can affect the COP movement in the left–right direction, PA in the sagittal plane may facilitate COP movement in the anterior–posterior direction. This study aimed to clarify the effect of an intervention using HMD with an upward bias condition on spatial awareness, STS movement, and standing balance in patients with left and right hemisphere stroke.

MATERIALS AND METHODS

Participants

Of the 24 participants, 12 patients had right hemisphere damage and 12 had left hemisphere damage. The included patients had stable neurological and general conditions, were able to stand up from a wheelchair, did not have severe dementia, could understand the instructions, and provided consent to the attending physician. USN was defined as a score of 1 or greater on the Catherine Bergego Scale. The clinical characteristics are presented in Table 1. This study was conducted with the approval of the Research Ethics Committee of Tokyo Metropolitan University (approval No. 19106) and the Ethics Committee of Niiza Hospital (approval No. 2019–11). Written informed consent was obtained from the participants after explaining that participation in the research was voluntary and that it was possible to withdraw with no consequence at any time after consent.

Table 1. Clinical characteristics of participants

Characteristic		RHD	LHD
Female/male		2/10	3/9
Diagnosis	Thalamic hemorrhage	1	2
	Putamen hemorrhage	2	-
	Middle cerebral artery infarction	8	9
	Subcortical hemorrhage	1	1
Age (years)		69.1±11.9	62.8±9.7
Days from onset to hospitalization (days)		27.4±7.8	28.3±18.5
Days from onset to study (days)		98.4±52.4	106.5±45.6
Br. stage	Upper limbs	5	4.5
	Fingers	5	4
	Lower limbs	5	5
Sensory deficit	Normal	2	2
	Mild	9	8
	Moderate degree	1	2
MAS		1	1
HDS-R		27.9±2.1	28.8±2.5
CBS		6±3.3 (6 people)	―
FBS		49.3±6	45.9±6.6
CS30 (count)		12.2±3.2	11.8±3.3
FIM	Motor	69.6±12.6	70.3±8.5
	Cognitive	29.3±5	28.1±6.5
	Total	98.9±14.5	98.4±12.6

Data given as number or mean ± standard deviation; data for Br. stage and MAS given as median.

RHD, right hemisphere damage; LHD, left hemisphere damage; Br. stage, Brunnstrom Recovery Stage; MAS, Modified Ashworth Scale; HDS-R, Hasegawa Dementia Scale-revised; CBS, Catherine Bergego Scale; FBS, Functional Balance Scale; CS30, 30-s Sit–Stand Test; FIM, Functional Independence Measure.

The sample size was verified by G-power using the values taken for healthy adults as reference. The sample size was calculated to be 11 participants based on an effect size of 0.98, an error of 0.05, and a power of 0.8. Because of the two groups in this study for the right and left hemispheres, a total of 22 participants were considered.

Line Bisection Test

The line bisection test was performed in the horizontal and frontal plane on an A4 test sheet. The participant was to locate the midpoint of 200-mm-long line, and deviations from the midpoint were evaluated. The line bisection test was performed at eye level in the frontal plane (Z axis) and at the umbilical level in the horizontal plane (Y axis). The midline was given a value of 0, points above the midline were denoted by positive values, and points below it were denoted by negative values.

STS Movement

For the STS task, the participants sat with their lower legs perpendicular to the floor and the soles of the feet placed shoulder-width apart on the center-of-gravity sway meter (400×680×20 mm) (Zebris Medical, Isny im Allgäu, Germany). The participants were instructed to cross their arms in front of their chest. An explanation was given with gestures to participants to stand in such a way that their body would not go backward and forward with respect to recoil. We encouraged the participants to stand up three times at their own pace, explaining that each time they should start from a sitting position with the trunk in the midline. We did not set a movement time, but if the process took longer than 20 s, we re-measured. The maximum pressure (horizontal plane, Y axis) on the forefoot in the extension phase of the STS movement was measured three times each before and after the intervention (Fig. 1), and the average of the maximum pressure on the left and right sides was used in the analyses. The loading rates (horizontal plane, X axis) were calculated for the affected and non-affected sides. The results of these data measurements were automatically calculated on the Zebris system and processed as a 95% confidence ellipse.

Fig. 1.

Measurement of sit-to-stand movements. The maximum pressure on the forefoot and loading rate (right and left) in the extension phase were extracted.

Balance Assessment

Balance assessment was performed by measuring the center of gravity using the sway meter (400×680×20 mm) (Zebris Medical). Participants stood with arms by their sides and with feet set shoulder width apart. The participants were asked to remain standing for 10 s in each of the following positions: the most stable position in which their center of posture was near the center of the base of support and after voluntarily moving the center of posture to the front, back, right, and left.²⁰⁾ The participants were instructed to remain as still as possible and look forward while maintaining a stable standing position. Measurements were taken after confirming that the subject was stable in each position. If the subject lost balance and fell during the measurement, the measurement was taken again. The range of anterior–posterior sway (horizontal plane, Y axis) was measured. Measurements were made at a sampling frequency of 60 Hz and no preprocessing was performed. The results of these data measurements were automatically calculated on the Zebris system and processed as a 95% confidence ellipse.

Intervention

The participants sat in a chair wearing the HMD with their feet on the floor and their trunk in contact with the backrest. Four targets were displayed in front of the participants at chest level, and the participants were asked to point at one of them at random while looking at them. This movement was performed 48 times. Any change in posture was rectified, and rest was provided when fatigue was observed. The intervention task was performed in the upward bias condition (Fig. 2), with the visual field tilted upward in the sagittal plane (Z axis) by 10 degrees. Patients with right hemisphere damage performed the pointing task with their right hand, and patients with left hemisphere damage performed the pointing task with their left hand.

Fig. 2.

Bias and pointing task with web camera. (a) Upward bias condition: tilting the web camera up. (b) Pointing task: participants pointed to the targets in front of them. (c) Structure in HMD: the image from the web camera was projected into the HMD.

Statistical Analyses

Participants were divided into two groups based on the side of hemisphere damage, and pre- and post-intervention values were compared using the Friedman test. Statistical analysis was performed using SPSS version 26 (IBM, Armonk, NY, USA). Statistical significance was set at P<0.05.

RESULTS

Twelve patients with right hemisphere damage and 12 patients with left hemisphere damage participated in this study. There were 6 patients with USN among the right hemisphere cases. No significant differences were observed in clinical characteristics between the right and left hemisphere cases. All data for damage in the right and left hemispheres are noted in Table 2.

Table 2. All data collected from participants before and after the intervention

		Line bisection test (mm)				Sit-to-stand movement (%)				Range of anterior–posterior sway (mm)
		Eye level		Navel level		Maximum pressure on the forefoot		Loading rate		Center		Anterior		Posterior		Right		Left
	Patient	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post
RHD	a	6	8	10	5	34.7	37.1	1.4	0.9	11.7	12.0	13.1	13.0	38.1	32.5	38.7	27.4	20.5	26.6
	b	9	5	−1	2	49.1	66.3	0.2	0.7	41.2	17.5	16.0	11.9	33.7	28.0	14.0	14.4	15.2	9.5
	c	7	7	2	6	68.0	77.7	1.2	1.1	13.7	15.6	25.0	12.8	18.9	20.9	21.0	26.3	32.2	28.8
	d	−3	11	16	16	74.5	79.0	0.6	0.6	39.1	19.1	45.0	31.7	28.1	29.5	33.5	39.1	54.6	45.6
	e	5	8	10	11	35.3	30.5	0.9	1.0	12.0	11.1	32.0	16.4	13.7	16.6	14.1	16.7	26.3	21.8
	f	11	12	10	6	58.8	58.8	0.9	0.9	19.5	15.1	23.8	11.9	38.2	17.3	26.5	17.6	44.3	38.9
	g	−2	11	−1	−2	68.1	77.4	0.5	0.6	12.8	21.8	26.4	24.8	11.9	12.2	7.7	18.3	15.9	15.8
	h	2	5	6	8	61.6	74.3	0.7	1.6	23.8	16.7	28.0	31.8	35.4	30.8	31.9	21.1	30.8	22.8
	i	2	14	1	10	41.8	46.9	0.5	1.2	11.9	17.7	17.0	13.0	22.9	23.8	24.2	25.3	20.9	41.9
	j	8	14	19	11	57.4	71.5	0.6	0.4	10.0	12.0	42.6	23.7	30.0	25.4	51.5	24.1	40.2	26.6
	k	7	13	7	15	75.6	73.8	0.5	0.4	28.7	27.8	22.5	26.8	28.8	22.0	15.0	17.2	22.5	30.5
	l	−1	4	6	13	36.8	47.1	0.4	0.2	12.1	16.6	21.6	11.6	23.0	15.2	13.1	14.6	9.7	10.8
Average		4.3	9.3	7.1	8.4	55.1	61.7	0.7	0.8	19.7	16.9	26.1	19.1	26.9	22.9	24.3	21.8	27.8	26.6
SD		4.6	3.6	6.3	5.3	15.2	17.2	0.3	0.4	11.1	4.6	9.8	8.1	8.9	6.6	12.8	7.1	13.3	11.5
LHD	m	−4	4	5	13	63.2	71.0	0.6	0.4	23.5	19.5	23.4	22.5	36.3	35.8	21.5	25.2	25.0	21.6
	n	0	7	6	7	64.2	68.2	0.3	0.2	23.7	33.7	22.0	28.0	25.3	37.3	35.0	41.2	23.0	19.7
	o	9	10	11	12	72.4	69.1	0.6	0.3	28.5	21.5	31.5	36.6	29.9	24.4	20.8	21.7	32.9	33.7
	p	27	11	17	7	63.7	65.1	1.9	2.3	28.0	19.0	26.6	17.7	24.1	20.4	28.9	22.4	19.3	17.8
	q	22	15	9	9	70.0	68.4	0.7	0.5	19.3	14.4	10.9	12.6	19.5	22.6	32.0	20.2	10.3	17.2
	s	2	2	11	13	54.9	72.5	0.5	1.0	11.6	13.5	20.2	16.7	24.6	17.0	17.9	11.0	24.8	14.1
	s	−5	0	10	8	64.4	60.5	0.9	0.7	30.3	25.3	32.8	31.6	19.6	35.7	17.9	31.8	20.0	15.9
	t	−1	3	1	0	68.9	73.9	0.9	0.4	19.6	23.2	26.7	21.1	40.1	22.9	30.5	20.9	22.0	19.8
	u	4	3	7	8	57.3	49.6	0.8	0.8	12.3	13.0	8.7	12.7	7.0	6.8	17.0	15.3	10.5	6.4
	v	8	15	12	14	73.9	76.7	0.3	0.6	12.7	8.8	10.3	13.1	11.3	15.8	18.7	27.8	18.6	19.0
	w	21	6	2	8	48.8	58.9	0.3	0.4	20.8	17.4	20.0	28.0	25.0	23.2	42.4	40.0	23.5	28.0
	x	12	4	0	0	41.7	33.6	0.9	1.4	12.2	12.0	22.4	21.4	8.4	9.0	8.8	9.8	14.0	15.0
Average		7.9	6.7	7.6	8.3	62.0	64.0	0.7	0.8	20.2	18.4	21.3	21.8	22.6	22.6	24.3	23.9	20.3	19.0
SD		10.7	5.0	5.1	4.6	9.7	12.1	0.4	0.6	6.8	6.9	7.9	7.9	10.3	9.9	9.5	10.0	6.5	6.9

RHD, right hemisphere damage; LHD, left hemisphere damage.

Line Bisection Test

The visual field at eye level (frontal plane, Z axis) significantly changed from 4.3±4.6 mm above before the intervention to 9.3±3.6 mm above after the intervention in patients with right hemisphere damage [F (1,24)=0.45; P=0.007]. In contrast, no significant difference was observed in patients with left hemisphere damage (Table 3). There was no significant difference in the visual field at the umbilical level (horizontal plane, Y axis) from before to after the intervention in both groups.

Table 3. Line bisection test and sit-to-stand movement

	Line bisection test (mm)			Sit-to-stand movement (%)
RHD	Eye level	Pre	4.3±4.6	Maximum pressure on forefoot	Pre	55.1±15.2
		Post	9.3±3.6**		Post	61.7±17.2*
	Umbilical level	Pre	7.1±6.3	Loading rate	Pre	0.7±0.3
		Post	8.4±5.3		Post	0.8±0.4
LHD	Eye level	Pre	7.9±10.7	Maximum pressure on forefoot	Pre	62±9.7
		Post	6.7±5		Post	64±12.1
	Umbilical level	Pre	7.6±5.1	Loading rate	Pre	0.7±0.4
		Post	8.3±4.6		Post	0.8±0.6

RHD, right hemisphere damage; LHD, left hemisphere damage.

Eye level (Z axis): bisection of vertical line segment at eye level; Umbilical level (Y axis): bisection of horizontal line segment at umbilical height; Maximum pressure on forefoot (Y axis): average value of left and right forefoot; Loading rate (X axis): paralyzed/non-paralyzed side.

Friedman test: *P<0.05; **P<0.01.

STS Movement

The maximum pressure on the forefoot (horizontal plane, Y axis) was significantly increased from 55.1±15.2% to 61.7±17.2% after the intervention in patients with right hemisphere damage [F (1,24)=0.70; P=0.04], although no significant difference was observed in patients with left hemisphere damage (Table 3). There was no significant difference in the loading rate (horizontal plane, X axis) from before to after the intervention in either group.

Balance Assessment

The range of anterior–posterior sway (horizontal plane, Y axis) during forward movement was significantly reduced from 26.1±9.8 mm to 19.1±8.1 mm after the intervention in patients with right hemisphere damage [F (1,24)=0.52; P=0.02]. In contrast, no significant difference was observed in patients with left hemisphere damage (Table 4).

Table 4. Balance assessment

		Range of anterior–posterior sway (mm)
		RHD	LHD
Center	Pre	19.7±11.1	20.2±6.8
	Post	16.9±4.6	18.4±6.9
Anterior	Pre	26.1±9.8	21.3±7.9
	Post	19.1±8.1*	21.8±7.9
Posterior	Pre	26.9±8.9	22.6±10.3
	Post	22.9±6.6	22.6±9.9
Right	Pre	24.3±12.8	24.3±9.5
	Post	21.8±7.1	23.9±10.3
Left	Pre	27.8±13.3	20.3±6.5
	Post	26.6±11.5	19±6.9

RHD, right hemisphere damage; LHD, left hemisphere damage.

Friedman test: *P<0.05.

DISCUSSION

Line Bisection Test

In patients with right hemisphere damage, there was a significant difference in upward localization after the intervention. This suggests that adaptation to the upward pointing task might have occurred. Lunven et al. reported that eight patients who responded well to a PA task in patients with left USN caused by right hemisphere damage were associated with cortical thickness in the thicker temporo-parietal cortex of the left hemisphere.²¹⁾ Shiraishi et al. also noted increased cerebral blood flow in the parietal cortex and around the pericallosal area of the non-affected hemisphere after PA.²²⁾ Of the 12 patients with right hemisphere damage in this study, 6 had left USN, which may have influenced the results of the right hemisphere damage. Conversely, right hemisphere damage without USN has also been reported to show PA.²³⁾ The right hemisphere damage in this study may have undergone visual and motor adaptation processes in the anterior left parieto-occipital sulcus and left parieto-occipital sulcus, which may have resulted in upward localization.²⁴⁾

The patients with right hemisphere damage in this study had no previous left hemisphere damage, and they might have adapted to the upward pointing task.

Regarding the lack of change in patients with left hemisphere damage, Ronchi et al. reported that patients with left hemisphere damage were less likely to show adaptation following the PA task than patients with right hemisphere damage.²⁵⁾ Our findings are similar to this previous study, and this may reflect the fact that the left hemisphere shows less adaptation than the right hemisphere.

In the line bisection test at the umbilical level (for the horizontal plane), no significant difference was observed in any of the groups. In patients with right hemisphere damage, the upward adaptation task had a significant effect on localization in the frontal plane (Z axis) but had a small effect in the horizontal plane (Y axis).

STS Movement

In patients with right hemisphere damage, the maximum pressure on the forefoot was increased after the intervention. In those with right hemisphere damage, the pointing task in the upward bias condition (Z axis) may have resulted in upward adaptation, and trunk movements were more likely to work in the direction of extension. If the left PA task can reconstruct spatial awareness to the left,²²⁾ then we can infer that the same upward learning occurs in the upward bias condition. The extension phase of the STS movement is a mixture of forward Y-axis movement²⁶⁾ and upward Z-axis movement.¹⁾ We hypothesized that during the extension phase of the STS movement, the upward movement of the sagittal plane (Z axis) was facilitated from the trunk extension activity, which may have affected the forward movement of the foot COP on the horizontal plane (Y axis).

Sato et al. reported that to achieve a standing position from sitting, it is necessary to move the foot COP forward and have the floor reaction force bring the center of gravity backward, which facilitates the STS movement.²⁶⁾ Furthermore, Cheng et al. reported that patients with cerebrovascular disease showed a large range of anterior–posterior sway in the extension phase of the STS task.²⁷⁾ Here, the range of anterior–posterior sway improved as the center of posture shifted forward in patients with right hemisphere damage, suggesting that it affects the extension phase of the STS movement. The upward bias condition may have facilitated the forward movement of the foot COP in the extension phase.

Balance Assessment

The range of anterior–posterior sway (horizontal plane, Y axis) during forward movement in the balance assessment was reduced after the intervention in patients with right hemisphere damage. Michel et al. indicated that the COP in the standing position deviates to the left in the right bias condition and to the right in the left bias condition of PA in healthy adults.²⁸⁾ Tilikete et al. reported that the foot COP moved from the right to the left after PA in patients with right hemisphere damage.¹⁵⁾ Rode et al. examined the plantar pressure while standing after temperature stimulation of the external auditory canal (Eustachian tube) in patients with right or left hemisphere damage.²⁹⁾ They reported that the COP deviated from the right to the midline in patients with right hemisphere damage.²⁹⁾ In the present study, adaptation between vision and motion in patients with right hemisphere damage resulted in the reorganization of higher-order spatial representation, which may have affected the postural control system during forward center of gravity movement.¹⁶⁾ In contrast, no effect of the intervention was observed in the balance assessment in patients with left hemisphere damage. Although improvements in the line bisection test after PA have been reported in patients with right USN,^30,31) it is possible that the intervention effect was not achieved because right USN was not targeted in this and previous studies.¹⁵⁾

Limitations

This study had some limitations. The long-term effects of the intervention were not examined because the duration of the intervention in this study was only 1 day. Given that we did not evaluate patients who were dependent on caregivers, it is unclear whether this treatment is useful for training for STS movement. In addition, the number of participants was small, and only patients in the subacute phase were included. Therefore, it will be necessary to conduct interventional studies of more patients, both in the acute and subacute phases.

In this study, we considered applying a two-way analysis of variance; however, given the small number of data and the fact that the data did not follow a normal distribution, we applied a nonparametric method. Therefore, this study used the Friedman test to examine the immediate effects of a single intervention.

CONCLUSION

After the intervention, patients with right hemisphere damage localized upward during vertical line bisection, increased forefoot pressure in the STS movement, and reduced the range of anterior–posterior sway during forward movement in the standing position. We hypothesized that an upward adaptation task would have an immediate effect on the line bisection test results, STS movement, and balance in patients with right hemisphere damage. The upward adaptation task is considered to encourage forefoot loading during the STS task and improves balance ability in patients with right hemisphere damage.

ACKNOWLEDGMENTS

The authors thank Mr. Takashi Baba, Manager of the Rehabilitation Department, Niiza Hospital, Japan, for providing the experimental site and staff.

CONFLICTS OF INTEREST

The authors have no conflicts of interest to declare.

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