INTRODUCTION

Postural abnormalities affect 22.1% of patients with Parkinson’s disease (PwP), yet effective treatments remain an unmet need [1,2]. The Movement Disorders Society (MDS) Task Force has standardized diagnostic criteria, defining anterior trunk flexion subtypes and cutoff values [3]. In camptocormia, differences between the thoracic and lumbar types are recognized. For lateral trunk flexion (LTF), three categories exist: normal (0° to <5°), LTF (5°–10°), and Pisa syndrome (>10°), with no subtypes [4-7]. Although PwP often exhibit a pelvic lateral shift (PLS), its role in Parkinson’s disease (PD)-related LTF is unclear. This study explores PLS as a potential LTF subtype, examining its prevalence and relationship with the LTF angle.

MATERIALS & METHODS

Participants

Patients who attended an outpatient clinic and underwent an assessment at the rehabilitation department between March 2018 and March 2023 were included. The clinical evaluation data retrospectively obtained from medical records included basic patient information and periodic assessments recorded in the electronic medical records system. The selection criteria were as follows: 1) a definitive diagnosis of clinically established PD based on the Movement Disorder Society Clinical Diagnostic Criteria for Parkinson’s disease [8]; 2) informed consent obtained for the use of clinical evaluation data obtained during routine clinical practice; 3) no medical or surgical disease other than PD with spinal deformity; and 4) PD onset at 40 years or older.

Evaluation of the side and angle of the PLS

PLS angles were measured from still images taken with a digital camera (RICOH CX2) via NeuroPostureAPP [9], which is based on the method recommended by the MDS Task Force [3]. Reflective markers (Nobbyteck VNS-BL-MC-190) were attached to the spinous processes of the 7th cervical vertebra (C7) and the 5th lumbar vertebra (L5). The basic axis was a vertical line extending from L5 to the floor, and the PLS axis was a line connecting L5 and the center point between the two feet (Figure 1A). The PLS angle was considered positive when the pelvis shifted contralateral to the LTF and negative when it shifted ipsilateral to the LTF.

PLS was classified into three types: contralateral shift, ipsilateral shift, and no shift (angle 0°). The still images were captured at a distance of 3 meters and were centered on the center point of Jacoby’s line and the height of the iliac crest. Figure 1B shows representative examples measured according to the method shown in Figure 1A.

Evaluation of the LTF angle

The LTF angle was measured from still images via NeuroPostureAPP in the same way as the PLS angle was measured. For the LTF angle, the basic axis was the extension of the line connecting L5 and the center point between the two feet. The LTF axis was the line connecting C7 and L5, and the angle between these two axes was defined as the LTF angle [6]. The still images for LTF angle evaluation were taken with the patient facing forward and assuming their natural posture immediately after standing. Furthermore, as advocated by the MDS Task Force on Postural Abnormalities in Parkinsonism, we used the following diagnostic criterion: LTF angles ≥10° were defined as Pisa syndrome.

Clinical evaluation

The following attributes of the patients were captured: age, sex, diagnosis, comorbidities, duration of illness, and information on anti-PD medication. PD assessment was performed via the modified Hoehn and Yahr scale [10] and the Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDSUPDRS) [11] for PD assessment. The LTF angle and PLS angle were measured via still images.

Statistical analysis

Continuous variables are presented as the mean±standard deviation or median (min. to max.), and the Mann–Whitney U test was used for comparisons between two groups. Spearman’s rank correlation coefficient was determined for each type of PLS to determine the correlation between the PLS angle and the LTF angle. Univariate linear regression analysis adjusted for age and sex was performed to examine factors associated with the PLS angle, and multiple regression analysis was performed on any items with a p value <0.1 from the preceding analysis. Receiver operating characteristic curves were used to examine the sensitivity, specificity, and positivity rate of each clinical indicator of lateral flexion related to Pisa syndrome and LTF. The level of significance of each statistical endpoint was set at 5% or less.

Ethical standard

The study was approved by the Ethics Committee at St. Marianna University School of Medicine (approval no. 6281 B48) and was conducted in accordance with the STROBE guidelines to enhance quality and transparency. Informed consent was obtained using an opt-out form available at the clinic. The opt-out form included information on how the confidential information of the participant would not be used for purposes other than direct treatment and stated that refusal to participate in this study would not affect the participant’s medical care. The data collected were anonymised by removing personally identifiable information.

RESULTS

Participant characteristics

The demographics of the patients included in the study are shown in Supplementary Table 1 (in the online-only Data Supplement). In total, 158 patients (70 men and 88 women) met the selection criteria.

Distribution and characteristics of the PLS angles

Supplementary Figure 1 (in the online-only Data Supplement) shows the distribution of the PLS angles. Three types were identified: patients in whom the PLS was ipsilateral to lateral flexion (ipsilateral shift type, ≥0.1° ipsilaterally), patients in whom the PLS was contralateral to lateral flexion (contralateral shift type, ≥0.1° contralaterally), and patients with no lateral shift (no shift type, angle=0°). There were 43 patients (27.2%) with the ipsilateral shift type, 80 patients (50.6%) with the contralateral shift type, and 35 patients (22.2%) with the no shift type. The median shift was 1.0° (0.1°–6°) for the ipsilateral shift type and 1.5° (0.1°–7°) for the contralateral shift type. Factor items determining PLS angles in the contralateral shift type included the LTF angle (95% confidence interval [CI]: 0.099–0.158, p<0.001). Multiple regression analysis adjusted for age and sex revealed that the LTF angle was the only significant factor (95% CI: 0.077–0.138, p<0.001) (Supplementary Table 2 in the online-only Data Supplement).

A scatter plot of the PLS and LTF angles is shown in Figure 2A. There was a significant positive correlation in the contralateral shift type, indicating a relationship between the magnitude of the LTF angle and the PLS angle in this type (r=0.48, p<0.001). However, there was no significant correlation with the ipsilateral shift type, indicating that there was no relationship between the LTF angle and the PLS angle. The LTF angle of 8.5°±9.6° for the contralateral shift type was significantly greater than that of 2.8°±4.2° for the ipsilateral shift type (p<0.001) (Figure 2B). Supplementary Figure 2 (in the online-only Data Supplement) shows the ipsilateral and contralateral PLS angles for each score on the MDS-UPDRS Part 3.13. For a score of 2 (mild), the contralateral shift type was more likely than the ipsilateral shift type was, and the contralateral shift type had a larger PLS angle than the ipsilateral shift type did (p=0.017). There were no differences between the two types for the other scores.

PLS angles and cutoff values for clinical indices in the contralateral type

For the contralateral shift type, the PLS angle had an area under the curve (AUC) of 0.698 (95% CI: 0.584–0.812, p=0.002) for LTF (5° to <10°), with a cutoff of 2.35° (sensitivity 0.381, specificity 0.947, positivity 89.5%). For Pisa syndrome (≥10°), the AUC was 0.854 (95% CI: 0.755–0.953, p<0.001), with a cutoff of 2.2° (sensitivity 0.706, specificity 0.857, positivity 57.1%) (Supplementary Figure 3 in the online-only Data Supplement).

DISCUSSION

This study investigated the relationship between PLS and LTF in PwP. PLS was classified into three types: contralateral shift, ipsilateral shift, and no shift. The contralateral shift type exhibited greater LTF angles, and a positive correlation was observed between the LTF angle and the PLS angle. These findings suggest that PLS contralateral to the LTF is an important factor related to the LTF and a critical clinical sign for evaluation. The PLS contralateral to the LTF may compensate for the lateral shift in the center of gravity caused by the LTF, contributing to the maintenance of balance. In contrast, the ipsilateral shift was unrelated to the LTF angle and may exacerbate lateral imbalance. In patients with Pisa syndrome (LTF angle ≥10°), the PLS contralateral to the LTF was found to be ≥2.2°. To the best of our knowledge, this may be the first report on PLS in Pisa syndrome.

The present study has several limitations. Owing to the retrospective, cross-sectional nature of this study, whether ipsilateral to contralateral shift of the pelvis occurs over time is subject to conjecture. Furthermore, the definition of PLS has not been established, which is a necessary step to obtain uniform evidence in future studies of PLS. This study was conducted at a single institution, so selection bias may be present. Although this study revealed a relationship between the PLS angle and LTF, it remains unresolved whether PLS functions as a compensatory mechanism for LTF or affects the progression of LTF. Future work will be needed to clarify the relationship between the balance function and the PLS angle, as one example.

In this study, three types of PLS were found in the PwP. PLS was related to the LTF angle in patients with contralateral shift, and a PLS of more than 2.2° was found to occur in patients with Pisa syndrome. Therefore, during follow-up observation, an evaluation that includes lateral displacement of the pelvis is important.

Supplementary Materials

Notes

Conflicts of Interest

The authors have no financial conflicts of interest.

Funding Statement

This study was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Nos. JP21K11321, JP22H00547, JP24K14361).

Acknowledgments

The authors thank Ryoma Aoki and Takuya Iwamoto, Ken Kumai, Keisuke Shiraishi, Natsumi Takahashi, Kazuki Yoshida, rehabilitation therapists of the Department of Rehabilitation, Noborito Neurology Clinic, for their assistance in data collection. The authors also thank Tina Tajima, Professor of the Research Institute of Medical Education, St. Marianna University School of Medicine, for meticulous English editing.

Author Contributions

Conceptualization: Kyohei Mikami. Data curation: Kyohei Mikami. Formal analysis: Kyohei Mikami. Funding acquisition: Makoto Shiraishi. Investigation: Kyohei Mikami, Akika Yoshimoto. Methodology: Kyohei Mikami, Makoto Shiraishi. Project administration: Tsutomu Kamo. Resources: Kyohei Mikami. Software: Kyohei Mikami. Supervision: Tsutomu Kamo. Validation: Makoto Shiraishi. Visualization: Kyohei Mikami. Writing—original draft: Kyohei Mikami. Writing—review & editing: Makoto Shiraishi.

Figure 1.

PLS and shift angle measurements with representative examples. A: Definitions of the PLS and shift angle. PLS is defined as the lateral displacement of the trunk to either the ipsilateral or contralateral side relative to a center point between the feet. The bold arrow indicates the direction of the PLS. B: Representative examples of contralateral (left panel) and ipsilateral (right panel) PLS. LTF, lateral trunk flexion; L5, fifth lumbar vertebra; PLS, pelvic lateral shift.

Figure 2.

Scatter plot of the PLS and LTF angles and comparison of the LTF and PLS angles among different shift types. A: The PLS angle is positive when the pelvis shifts contralateral to the LTF and negative when it shifts ipsilateral to the LTF. B: LTF angles for the contralateral and ipsilateral shift types. PLS, pelvic lateral shift; LTF, lateral trunk flexion.

REFERENCES

• 1. Cao S, Cui Y, Jin J, Li F, Liu X, Feng T. Prevalence of axial postural abnormalities and their subtypes in Parkinson’s disease: a systematic review and meta-analysis. J Neurol 2023;270:139–151.ArticlePubMedPDF
• 2. LeWitt PA, Chaudhuri KR. Unmet needs in Parkinson disease: motor and non-motor. Parkinsonism Relat Disord 2020;80(Suppl 1):S7–S12.ArticlePubMed
• 3. Tinazzi M, Geroin C, Bhidayasiri R, Bloem BR, Capato T, Djaldetti R, et al. Task force consensus on nosology and cut-off values for axial postural abnormalities in parkinsonism. Mov Disord Clin Pract 2022;9:594–603.ArticlePubMedPMCPDF
• 4. Artusi CA, Montanaro E, Tuttobene S, Romagnolo A, Zibetti M, Lopiano L. Pisa syndrome in Parkinson’s disease is associated with specific cognitive alterations. Front Neurol 2019;10:577.ArticlePubMedPMC
• 5. Mikami K, Shiraishi M, Kamo T. Effect of subjective vertical perception on lateral flexion posture of patients with Parkinson’s disease. Sci Rep 2022;12:1532.ArticlePubMedPMCPDF
• 6. Artusi CA, Geroin C, Imbalzano G, Camozzi S, Aldegheri S, Lopiano L, et al. Assessment of axial postural abnormalities in parkinsonism: automatic picture analysis software. Mov Disord Clin Pract 2023;10:636–645.ArticlePubMedPMCPDF
• 7. Aldegheri S, Artusi CA, Camozzi S, Di Marco R, Geroin C, Imbalzano G, et al. Camera- and viewpoint-agnostic evaluation of axial postural abnormalities in people with Parkinson’s disease through augmented human pose estimation. Sensors (Basel) 2023;23:3193.ArticlePubMedPMC
• 8. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 2015;30:1591–1601.ArticlePubMed
• 9. Margraf NG, Wolke R, Granert O, Berardelli A, Bloem BR, Djaldetti R, et al. Consensus for the measurement of the camptocormia angle in the standing patient. Parkinsonism Relat Disord 2018;52:1–5.ArticlePubMed
• 10. Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C, et al. Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 2004;19:1020–1028.PubMed
• 11. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008;23:2129–2170.PubMed

Figure & Data

References

Citations

Citations to this article as recorded by  

Comments on this article