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Impaired virtual space-tilting perception in Parkinson's disease with Pisa syndrome

  • Fuyuko Sasaki
    Affiliations
    Department of Neurology, Juntendo University School of Medicine, Tokyo, Japan
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  • Genko Oyama
    Correspondence
    Corresponding author. 2-1-1 Hongo, Bunkyo-Ku, Tokyo, 113-8421, Japan.
    Affiliations
    Department of Neurology, Juntendo University School of Medicine, Tokyo, Japan

    Department of Neurodegenerative and Demented Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Home Medical Care System Based on Information and Communication Technology, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Drug Development for Parkinson's Disease, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of PRO-Based Integrated Data Analysis in Neurological Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Research and Therapeutics for Movement Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan
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  • Yoshihiko Hirozane
    Affiliations
    Research, Takeda Pharmaceutical Company Limited, Japan
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  • Ryo Yamashita
    Affiliations
    Research, Takeda Pharmaceutical Company Limited, Japan
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  • Satoko Sekimoto
    Affiliations
    Department of Neurology, Juntendo University School of Medicine, Tokyo, Japan
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  • Nobutaka Hattori
    Affiliations
    Department of Neurology, Juntendo University School of Medicine, Tokyo, Japan

    Department of Neurodegenerative and Demented Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Home Medical Care System Based on Information and Communication Technology, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Drug Development for Parkinson's Disease, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of PRO-Based Integrated Data Analysis in Neurological Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan

    Department of Research and Therapeutics for Movement Disorders, Juntendo University Graduate School of Medicine, Tokyo, Japan
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Open AccessPublished:September 27, 2022DOI:https://doi.org/10.1016/j.parkreldis.2022.09.002

      Highlights

      • The virtual space-tilting perception was impaired in Parkinson's disease patients with the Pisa syndrome compared to patients without Pisa syndrome and controls.
      • Visual-spatial function and/or attentional in patients with Pisa syndrome impaired.

      Abstract

      Introduction

      The mechanism of Pisa syndrome in Parkinson's disease (PD) is unclear. We aimed to analyze the spatial perception of patients with PD with Pisa syndrome using virtual reality.

      Methods

      In total, 16 patients with Pisa syndrome, 16 age-matched patients without Pisa syndrome, and 16 age-matched controls were included. They viewed the virtual room gradually tilting to different 8 directions randomized across trials. The 75% discrimination threshold angle and the mean tilting discrimination angle for each direction were evaluated. Participants' lateral trunk deviation was measured using Kinect. Neuropsychological status was evaluated, using the Mini-Mental Status Examination (MMSE), the Japanese version of the Montreal-Cognitive Assessment, Frontal Assessment Battery, and the color-word interference task of the Stroop test. Visuospatial abilities were assessed using Benton Judgement of Line Orientation, and vestibular function was evaluated using Subjective Visual Vertical (SVV).

      Results

      The 75% discrimination threshold in the tilting discrimination angle was larger in all directions for those in the Pisa syndrome group compared to patients in the without Pisa syndrome group and those in the control group. There were significant differences between the three groups for Front-Right, Right, and Back. Patients with Pisa syndrome showed a significantly worse performance in these tests compared with controls and tended to have worse SVV performance compared with patients without Pisa syndrome.

      Conclusion

      The present findings support the hypothesis of visuo-spatial disability and/or attentional impairment in patients with Pisa syndrome.

      Keywords

      1. Introduction

      Pisa syndrome (PS) is a postural deformity that complicates Parkinson's disease (PD) and is characterized by lateral deviation of the trunk while standing and can be reversed by passive mobilization or spine positioning [
      • Doherty K.M.
      • van de Warrenburg B.P.
      • Peralta M.C.
      • Silveira-Moriyama L.
      • Azulay J.P.
      • Gershanik O.S.
      • Bloem B.R.
      Postural deformities in Parkinson's disease.
      ]. The mechanism of PS in PD is still unclear. However, two main hypotheses have been postulated. One is a peripheral hypothesis related to musculoskeletal pathology with myopathic alterations in the paraspinal muscles. The other is a central hypothesis encompassing hyperactivation of axial muscles related to an imbalance of the basal ganglia network output or an altered sensory-motor integration [
      • Doherty K.M.
      • van de Warrenburg B.P.
      • Peralta M.C.
      • Silveira-Moriyama L.
      • Azulay J.P.
      • Gershanik O.S.
      • Bloem B.R.
      Postural deformities in Parkinson's disease.
      ]. In particular, the association between cognitive deficits such as verticality perception and altered visuospatial functions has been considered important in previous studies [
      • Scocco D.H.
      • Wagner J.N.
      • Racosta J.
      • Chade A.
      • Gershanik O.S.
      Subjective visual vertical in Pisa syndrome.
      ].
      In this pilot cross-sectional study, we aimed to analyze the relationship between PS and visual-spatial functions using a virtual three-dimensional tilt test in a virtual reality space. As a primary aim, we compared the virtual space-tilt perception using the tilting discrimination angle among PD patients with PS, PD patients without PS, and age-matched controls. We also analyzed the difference in neuropsychological scores between the three groups and evaluated the association between cognitive disability and tilting discrimination angle.

      2. Methods

      2.1 Participants

      Between January 2018 and October 2019, we recruited patients with PD at the Movement Disorders Clinic of the Juntendo University Hospital, Tokyo, Japan. The inclusion criteria were as follows: diagnosis of PD according to the criteria of UK PD Society Brain Bank, age 20–80 years, Yahr stage 1–3, and presence of PS with lateral deviation of the trunk while standing, which can be reversed by passive mobilization or spine positioning (PS+ group). We used 5° or more as the threshold angle for screening based on the minimal improvement angle [
      • Artusi C.A.
      • Bortolani S.
      • Merola A.
      • Zibetti M.
      • Busso M.
      • De Mercanti S.
      • Arnoffi P.
      • Martinetto S.
      • Gaidolfi E.
      • Veltri A.
      • Barbero P.
      • Lopiano L.
      Botulinum toxin for Pisa syndrome: an MRI-, ultrasound- and electromyography-guided pilot study.
      ]. The exclusion criteria were as follows: neurological (apart from PD) or orthopedic disease that can cause postural abnormalities, inability to stand independently, severe dyskinesias or prolonged OFF periods, having undergone treatment with device-aided therapy, poor corrected vision, dementia, or vestibular dysfunction. Age-matched patients with PD were recruited through the clinic as a PS- group. The age-matched healthy control group was recruited. We used the same cut-off of 5° or less for the PS- and control groups.

      2.2 Standard protocol approvals, registrations, and patient consents

      All participants provided written informed consent to participate in the study, which was approved by the Juntendo University Hospital Institutional Review Board (#17-200) and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

      2.3 Experimental protocols

      2.3.1 Demographic and clinical characteristics

      Demographic and clinical data analyzed included age, sex, disease duration, levodopa-equivalent daily dose, and dopamine agonist daily dose. All subjects underwent a comprehensive assessment of clinical, neurological, and neuropsychological assessments. In PD patients, the Movement Disorder Society-Unified Parkinson's Disease Rating Scale Part III (MDS-UPDRS III) was used to assess the severity of the motor disability. During the experiments, participants with PD took their regular dose of antiparkinsonian drugs, and all assessments were performed with medication the ON state.

      2.3.2 Neuropsychological assessment

      All participants underwent the following assessments: the global measure of cognitive function was assessed using the Mini-Mental Status Examination (MMSE) and the Japanese version of the Montreal-Cognitive Assessment (MoCA-J). Executive functions and attention were assessed using the Frontal Assessment Battery (FAB) and the color-word interference task of the Stroop test. Visuospatial abilities were assessed using Benton Judgement of Line Orientation (BJLOT). Vestibular function was evaluated using Subjective Visual Vertical (SVV).

      2.3.3 Virtual space-tilting test

      The participants were provided with a virtual environment with immersive three-dimensional settings by wearing a virtual reality head-mount display (HTC Vive, HTC Corporation, Taipei) (Supplemental Figure 1). The virtual tilting program we developed showed that the participants gradually tilted in eight directions randomly. While performing the tasks, the participants were instructed to stand still with arms down, holding controllers on each side. Initially, the participants stood at the center of a room in the virtual environment, and then they performed twenty-four trials (8 conditions × 3 sessions). They viewed the room gradually tilting from different directions randomized across trials: Front, Front-Right, Right, Back-Right, Back, Back-Left, Left, and Front-Left (Fig. 1A). They were asked to click a button on the controller when they perceived room tilting. We calculated the 75% discrimination threshold angle, the point at which 75% of the participants noticed the space tilting, and the mean tilting discrimination angle for each direction.
      Fig. 1
      Fig. 1A. Virtual environment. A 3D room was provided to the participant with a head-mount display. The center is the view before each task started, and then the view tilted by 8° randomly.
      B. The 75% discrimination threshold angle in each direction. CO, controls; PS-, Parkinson's disease patients without Pisa syndrome; PS+, Parkinson's disease patients with Pisa syndrome.

      2.3.4 Lateral trunk deviation

      Lateral trunk deviation in the sagittal plane was measured using Kinect v2, which is an RGB depth camera used to measure the three-dimensional motion of the participant's skeletal structure by tracking 25 joints. Participants stood directly facing the Kinect sensor at a distance of 3 m. The mean frontal plane angle between the shoulder center and spine relative to the vertical was calculated over 40 s of still standing at a frequency of 30 Hz.

      2.3.5 Statistical analysis

      We tested between-group differences with the neuropsychological tests, lateral trunk deviation, and tilting discrimination angle using the Kruskal-Wallis test and Wilcoxon signed-rank test for post hoc analysis. We compared the clinical features between PS- and PS+ using the Mann-Whitney U test. All reported p-values were two-tailed and adjusted with Bonferroni correction for multiple comparisons. Data were analyzed using IBM SPSS Statistics version 24 software.

      3. Results

      A total of 18 PS+ patients, 16 age-matched PS- patients, and 16 age-matched controls were enrolled. Two patients from the PS+ group were excluded because they could not complete the tests. Therefore, 16 PS+ patients, 16 age-matched PS- patients, and 16 age-matched controls were analyzed. The demographic and clinical features of all groups are summarized in Table 1. There were no participants who had co-occurrence of other postural abnormality such as head drop and camptocormia. No significant differences were found for age and sex among the three groups. No significant difference was found for disease duration and MDS-UPDRS Part III score between the PS+ and PS- groups. Total levodopa equivalent dose (LED) and levodopa dose were significantly higher in the PS- group, although there was no significant difference for dopamine agonist LED (total LED, p = 0.017; levodopa LED, p = 0.004; dopamine agonist LED, p = 0.752). In the PS+ group, nine patients leaned to the right side and seven to the left side. There were significant differences between the three groups (χ2 = 30.659, p < 0.0001, df = 2). In pairwise group comparisons, PS+ had significantly larger lateral trunk deviation than control (adjusted p < 0.0001) and PS- (adjusted p < 0.0001). There were no significant differences between control and PS- (adjusted p = 1).
      Table 1The demographic and clinical features of participants.
      CO (n = 16)PS-(n = 16)PS+ (n = 16)P-valueadjusted P-value
      CO vs PS-CO vs PS+PS- vs PS+
      Age (years)66.0 ± 8.266.1 ± 7.565.8 ± 7.30.993
      Sex (% male)6938440.18
      Disease duration (years)NA6.8 ± 2.87.4 ± 5.20.094
      MDS-UPDRS Part ⅢNA17.0 ± 8.221.3 ± 7.70.102
      Total LED (mg)NA625.6 ± 382.3863.6 ± 289.30.017*
      Levodopa dose (mg)NA442.4 ± 284.6706.1 ± 231.00.004**
      Dopamine agonist LED (mg)NA183.3 ± 162.0157.5 ± 114.00.752
      Lateral trunk deviation (degree)***1.3 ± 0.71.3 ± 1.06.4 ± 2.5<0.0001**1<0.0001**<0.0001**
      Pisa to rightNANA9
      MoCA-J25.5 ± 2.526.2 ± 2.825.6 ± 3.10.632
      MMSE29.1 ± 1.429.2 ± 1.229.1 ± 1.10.834
      FAB14.3 ± 2.315.8 ± 2.415.4 ± 2.30.892
      Stroop test46.4 ± 3.342.6 ± 11.442.6 ± 7.30.012*0.1680.009**1
      BJLOT26.5 ± 3.723.1 ± 5.420.9 ± 5.30.012*0.1410.012*0.717
      SVV1.2 ± 0.91.7 ± 0.95.5 ± 4.70.008**0.2250.002**0.061
      Tilting discrimination angle
      Front6.9 ± 5.49.4 ± 5.010.5 ± 4.50.054
      Front Right5.3 ± 3.87.3 ± 3.49.5 ± 4.90.015*0.2130.013*0.884
      Right5.5 ± 3.96.4 ± 2.99.2 ± 4.40.026*0.8160.021*0.335
      Back Right6.0 ± 3.97.6 ± 4.38.8 ± 3.70.176
      Back7.3 ± 5.78.5 ± 3.910.2 ± 4.00.046*0.2040.013*0.225
      Back Left7.2 ± 5.15.9 ± 2.58.9 ± 5.00.205
      Left6.0 ± 5.16.7 ± 3.98.7 ± 5.70.087
      Front Left6.7 ± 5.27.0 ± 4.27.8 ± 4.90.557
      Data are reported as mean ± standard deviation. CO, controls; PS-, Parkinson's disease patients without Pisa syndrome; PS+, Parkinson's disease patients with Pisa syndrome; MDS-UPDRS Part III, Movement Disorders Society-Unified Parkinson's Disease Rating Scale Part III; MoCA-J, the Japanese version of Montreal-Cognitive Assessment; MMSE, the Mini-Mental Status Examination; FAB, Frontal Assessment Battery; Stroop test, the color-word interference task of Stroop test; BJLOT, Benton's judgement of line orientation test; SVV, subjective visual vertical.; LED, levodopa equivalent dose; NA, not applicable. *Statistically significant (p < 0.05), ** Statistically significant (p < 0.01), ***Measured with Kinect during evaluation day.

      3.1 Neuropsychological assessment

      The Kruskal-Wallis test showed no significant differences among the three groups in the results of global cognitive evaluation tests: MoCA-J (χ2 = 0.918, p = 0.632, df = 2), MMSE (χ2 = 0.362, p = 0.834, df = 2), and FAB (χ2 = 0.230, p = 0.892, df = 2). There were significant differences between the three groups in the Stroop test (χ2 = 8.819, p = 0.012, df = 2), BJLOT (χ2 = 8.896, p = 0.012, df = 2), and SVV (χ2 = 9.681, p = 0.008, df = 2). In pairwise group comparisons, PS+ showed significantly worse performance compared with control group: adjusted p = 0.009 for Stroop test, adjusted p = 0.012 for BJLOT, and adjusted p = 0.002 for SVV. Furthermore, PS+ tended to have worse SVV performance compared to PS- (adjusted p = 0.061) (Table 1).

      3.2 Virtual space-tilting perception

      Fig. 1B shows the 75% discrimination threshold angle in each direction. The graph indicates higher discrimination thresholds for the PS+ group compared to that of the other two groups in all directions. Therefore, we conducted an exploratory analysis of the tilting discrimination angles in each direction in the three groups. Kruskal-Wallis test showed significant differences between the three groups for Front-Right (χ2 = 8.335, p = 0.015, df = 2), Right (χ2 = 7.315, p = 0.026, df = 2), and Back (χ2 = 6.158, p = 0.046, df = 2), and a statistical tendency for Front (χ2 = 5.828, p = 0.054, df = 2). Pairwise comparisons showed that the PS+ group had significantly poor perception compared to control group in Front-Right (p = 0.013), Right (p = 0.021), and Back (p = 0.013) (Table 1). There was no significant correlation between the laterality of Pisa syndrome.

      4. Discussion

      We found that the 75% discrimination threshold in the tilting discrimination angle was larger in all directions for the PS+ group than for the PS- and control groups. This suggests that PD patients, especially those with PS, have poor visual tilting perception in the virtual space provided by headset display. The PS+ group showed significantly worse performance than the control group and tended to have worse performance compared with the PS- group in SVV, which is in line with previous studies showing that vestibular perception [
      • Scocco D.H.
      • Wagner J.N.
      • Racosta J.
      • Chade A.
      • Gershanik O.S.
      Subjective visual vertical in Pisa syndrome.
      ] and/or cognitive deficits such as altered visual-spatial functions have been considered to play an important role in the mechanism of PS [
      • Huh Y.E.
      • Kim K.
      • Chung W.H.
      • Youn J.
      • Kim S.
      • Cho J.W.
      Pisa syndrome in Parkinson's disease: pathogenic roles of verticality perception deficits.
      ].
      The mechanism of PS has not been fully explained, but there is accumulating evidence showing that the central mechanism plays an important role. The Stroop color-word interference task is a test to examine age-related decline in inhibitory control, mainly by the frontal cortex, which contributes to postural control [
      • Borel L.
      • Alescio-Lautier B.
      Posture and cognition in the elderly: interaction and contribution to the rehabilitation strategies.
      ]. It has been reported that patients with PS have more difficulty shifting attention and adapting to changing demands than controls. BJLOT is considered to be a measure of visuospatial judgement mediated by the inferior-parietal, occipito-parietal, and occipito-temporal regions of the right hemisphere [
      • Tranel D.
      • Vianna E.
      • Manzel K.
      • Damasio H.
      • Grabowski T.
      Neuroanatomical correlates of the Benton facial recognition test and judgment of line orientation test.
      ]. Vitale et al. reported that reduced performance on BJLOT was independently associated with PS occurrence [
      • Vitale C.
      • Falco F.
      • Trojano L.
      • Erro R.
      • Moccia M.
      • Allocca R.
      • Agosti V.
      • Santangelo F.
      • Barone P.
      • Santangelo G.
      Neuropsychological correlates of Pisa syndrome in patients with Parkinson's disease.
      ]. SVV deviation is indicative of vestibular imbalance [
      • Dieterich M.
      • Brandt T.
      Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs.
      ]. Recent data suggest that vestibular defects can be found in PD patients and are at least partially associated with postural abnormalities in patients with PD [
      • Scocco D.H.
      • Wagner J.N.
      • Racosta J.
      • Chade A.
      • Gershanik O.S.
      Subjective visual vertical in Pisa syndrome.
      ]. As in previous studies, our data showed that PS is associated with attention disorders, executive dysfunction, and vestibular imbalance in PD patients with PS.
      The visual tilting perception assessed in our study is a visual domain task, and our study revealed that PS+ patients displayed impaired visuospatial cognition in addition to vestibular function, which is usually severely impaired with PD. Beylergil et al. reported that PD affects motion perception in the visual and vestibular domains in a severity-dependent manner [
      • Beylergil S.B.
      • Petersen M.
      • Gupta P.
      • Elkasaby M.
      • Kilbane C.
      • Shaikh A.G.
      Severity-dependent effects of Parkinson's disease on perception of visual and vestibular heading.
      ]. It is still unclear whether these dysfunctions cause postural abnormalities or occur as a result of postural abnormalities in PD. In addition, the pathological mechanism of PS in PD might be due to multiple factors. It is possible that visual field dependence indicates an inability to properly integrate vestibular, proprioceptive, and visual information [
      • Yu Y.
      • Lauer R.T.
      • Tucker C.A.
      • Thompson E.D.
      • Keshner E.A.
      Visual dependence affects postural sway responses to continuous visual field motion in individuals with cerebral palsy.
      ]. Overreliance on visual information is exhibited as an inability to respond appropriately to self-motion feedback [
      • Dokka K.
      • Kenyon R.V.
      • Keshner E.A.
      • Kording K.P.
      Self versus environment motion in postural control.
      ]. For PD patients with impaired vestibular function and increased dependence on visual information, visually focused rehabilitation strategies may be effective for posture correction.
      Virtual space tilting might be used for rehabilitation to improve and prevent PS in patients with PD. Indeed, Omura et al. reported that the tilted view provided by the headset displays a deviated posture to the ipsilateral side in healthy males [
      • Ohmura Y.
      • Yano S.
      • Katsuhira J.
      • Migita M.
      • Yozu A.
      • Kondo T.
      Inclination of standing posture due to the presentation of tilted view through an immersive head-mounted display.
      ]. It may enable posture-correcting rehabilitation by providing a view tilted to the opposite side of the patient's deviated side.
      This study has several limitations. First, this was a pilot study with small sample size. Second, although we used a lightweight device, the weight of the headset might affect somatosensory perception. Additionally, immersion and presence quality of the virtual environment may also have influenced the experiment. Third, medications may affect the results. Indeed, levodopa dose was different among the groups in this study.
      In conclusion, we found that PD patients, especially those with PS, had impaired virtual space-tilting perception, which reflects visuospatial function. Rehabilitation focused on visuospatial function in a virtual environment where the inclination of the space can be adjusted freely may be beneficial for PD patients with lateral trunk deviation to correct posture. To develop a new rehabilitation strategy with virtual reality, further research is needed to find optimal virtual-spatial conditions for posture correction programs in PD patients.

      Study funding

      This study was partially supported by grant from the Japan Society for the Promotion of Science , Grant-in-Aid for Scientific Research (C) ( #21K12711 s) and Grants-in-Aid from the Research Committee of CNS Degenerative Diseases, Research on Policy Planning and Evaluation for Rare and Intractable Diseases, Health, Labour and Welfare Sciences Research Grants, the Ministry of Health, Labour and Welfare, Japan ( 20FC1049 ).

      Declaration of competing interest

      Department of Neurodegenerative and Demented Disorders is a joint-research course supported by GLORY LTD, Kirin Company LTD, Mitsubishi UFJ Lease & Finance Company LTD. Department of Home Medical Care System based on Information and Communication Technology is a joint-research course supported by Sunwels Co., Ltd. Department of Drug Development for Parkinson's Disease, Juntendo University Faculty of Medicine is a supported course supported by Ohara Pharmaceutical Co.,Ltd. and PARKINSON Laboratories Co., Ltd. Dr. Oyama received speaker honoraria from Medtronic, Boston Scientific, Otsuka Pharmaceutical Co. Ltd., Sumitomo Dainippon Pharma Co. Ltd., Eisai Co., Ltd., Takeda Pharmaceutical Company LTD., Kyowa Hakko Kirin Co. Ltd., and AbbVie, Inc. NH received speaker honoraria from AbbVie GK, EA Pharma, Eisai Co., Ltd., Otsuka Pharmaceutical Co., Ltd., Ono Pharmaceutical Co., Ltd., OHARA Pharmaceutical Co., Ltd, Kyowa Kirin Co., Ltd., Senju Pharmaceutical Co., Ltd., Sumitomo Dainippon Pharma Co., Ltd., Takeda Pharmaceutical Co., Ltd., Medtronic, Inc., Novartis Pharma K·K.

      Acknowledgement

      The authors thank Drs. Yutaka Oji, Taiji Tsunemi, Taku Hatano and Yasushi Shimo for assisting with patient identification and recruitment. The authors thank Shoichi Nakao, Toshiyuki Ohnishi, and Yasunori Fukuda, the VR team members from Research, Takeda Pharmaceutical Company Limited, for sharing the idea to develop the VR program.

      Appendix A. Supplementary data

      Multimedia component 1

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