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Quantitative assessment of posture in healthy controls and patients with Parkinson's disease
Journal Pre-proof Quantitative assessment of posture in healthy controls and patients with Parkinson's disease Christian Schlenstedt, Kathrin Boße, Olga Gavriliuc, Robin Wolke, Oliver Granert, Günther Deuschl, Nils G. Margraf PII:
S1353-8020(20)30022-5
DOI:
https://doi.org/10.1016/j.parkreldis.2020.01.012
Reference:
PRD 4257
To appear in:
Parkinsonism and Related Disorders
Received Date: 11 November 2019 Revised Date:
21 January 2020
Accepted Date: 23 January 2020
Please cite this article as: Schlenstedt C, Boße K, Gavriliuc O, Wolke R, Granert O, Deuschl Gü, Margraf NG, Quantitative assessment of posture in healthy controls and patients with Parkinson's disease, Parkinsonism and Related Disorders (2020), doi: https://doi.org/10.1016/ j.parkreldis.2020.01.012. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Quantitative assessment of posture in healthy controls and patients with Parkinson’s disease Christian Schlenstedt1*, Kathrin Boße1*, Olga Gavriliuc1, 2, Robin Wolke1, Oliver Granert1, Günther Deuschl1, Nils G. Margraf1
1 2
Department of Neurology, UKSH, Christian-Albrechts-University, Kiel, Germany Department of Neurology, State University of Medicine and Pharmacy “Nicolae Testemitanu”, Chisinau, Republic of Moldova
* These authors contributed equally.
Corresponding author: Prof. Dr. G. Deuschl, Department of Neurology, UKSH, Kiel Campus, Christian-Albrechts-University, Arnold-Heller-Str. 3, 24105 Kiel, Germany. E-mail address: [email protected].
Word count: 3109 Figures: 3 Tables: 1
Keywords: Parkinson’s disease, posture, angle measurement, camptocormia, forward bending, Pisa syndrome, axial symptoms, postural abnormalities.
Abstract Introduction A stooped posture is a main clinical feature of Parkinson’s disease (PD). The assessment of posture is important to measure treatment effects. The aim of this study was to investigate the reliability of a standardized postural rating tool, to calculate minimal detectable change scores and to assess the role of gender and age.
Methods Two independent raters assessed total camptocormia (TCC), upper camptocormia (UCC) and Pisa angles of 192 PD patients and 78 HC with the free NeuroPostureApp©(http://www.neuroimaging.uni-kiel.de/NeuroPostureApp). Reliabilities and linear models were calculated for different effects. Three subgroups were defined based on two thresholds (mean+2SD of HC and PD): A) normal, B) presumed stooped/lateral bended posture and C) postural disorder.
Results Intraclass correlation coefficients ranged between 0.71 and 0.95 for the interrater and testretest reliability of the three angles. The minimal detectable change values in the PD patients were 3.7°, 6.7° and 2.1° for the TCC, UCC and Pisa angle, respectively. Men had a more stooped posture than women (p<0.05). Patients with PD had a worse posture than HC (p<0.001) in all three angles. For the TCC angle, 39.1% of the patients had a normal posture (<17.4°), 47.9% a presumed stooped posture (>17.4°, <30.2°) and 6.3° had camptocormia (>30.2°).
Conclusions The NeuroPostureApp© is reliable. Our results confirmed gender differences and the progression of postural deviation in PD patients with age and empirically support the ≥30° TCC angle as a defining criterium for camptocormia. Diagnostic criteria for UCC and Pisa syndrome should be further explored in future studies.
Introduction A bent posture is a main clinical feature of Parkinson’s disease (PD). Postural impairments are independent risk factors for falls [1] and reduce the patients’ mobility and autonomy [2]. While dynamic postural control is increasingly being studied with neurophysiological methods and technical devices [3], postural alignment is traditionally measured with clinical scales such as the Unified Parkinson’s disease Rating Scale (UPDRS) item 28. The 4-point ordinal scaled UPDRS item 28 gives only a broad classification of posture but is not suited for a more detailed description of posture and may not be sensitive to change. Furthermore, a differentiation in the postural disorders camptocormia or Pisa syndrome is not intended. While a consensus was reached for the method of angle assessment in camptocormia [4], a further empirical substantiation of a threshold value for the angle criterion is still lacking for camptocormia and Pisa syndrome. Recently, studies have described postural alignment by rating postural angles from photographs. They found larger angles for dropped head, and anterior and lateral flexion in patients with PD than in healthy controls (HC) [5, 6]. Other studies with similar methodological approaches found an effect of age on postural alignment for patients with PD [7] and HC [8]. Another study, which used clinical rating criteria instead of postural angles, found an association between posture and disease severity [9]. Most of the existing studies that characterized posture by rating photographs assessed postural angles manually using different methods, and no information about the reliability or validity of these procedures was given. Therefore, simple objective and reliable angle measurement methods are needed. A recent study has validated a measurement of the forward bending angle using a free, software-supported tool [4]. This measurement proved to be valid for quantifying the anteroposterior (AP) angle and is applied here and extended by a frontal view to measure the lateral angle (Pisa-deviation). This study had the following aims: First, to investigate the reliability of a standardized, software-supported, postural rating assessment. The test-retest- as well as the interrater reliability and minimal detectable change scores will be evaluated, and the test instrument will be related to other clinical scales; second, to provide normative data of postural alignment for HC for this specific tool and to investigate the effect of gender and age, and third, to use the clinical rating instrument to compare the posture of patients with PD with HC and to study the progression of postural inclination with age for the two cohorts. Finally, the data of HC and PD will be used to discuss currently available criteria for the clinical
diagnosis of camptocormia, also taking upper camptocormia and Pisa syndrome in PD into consideration.
Methods Participants One hundred and ninety-two patients with idiopathic PD according to the UK Brain Bank PD criteria [10] were included in this study (Supplementary Table 1). We included 78 healthy controls between the 30 to 79 years old, with 10 to 20 from each decade. Exclusion criteria were neurological disease, other than PD, or injuries that could affect gait and posture. The HC were recruited from the patients’ relatives. The ethics committee of the medical faculty of Kiel University approved the study. Informed consent was obtained from all participants.
Testing Postural alignment was assessed using photos captured from videos showing a standardized walking task, depicting the posture in the frontal and sagittal planes. Two photos of each participant were taken; a strictly lateral and a frontal view. The pictures were anonymized and blindly rated by two independent raters (KB, OG). All PD patients were rated in Med-OFF condition, after having withdrawn L-dopa for 12 h and dopamine-agonists for 72 h. The same raters reassessed photos of 50 randomly selected participants four weeks later to determine intra-subject test-retest reliability. The posture was rated with the NeuroPostureApp© (http://www.neuroimaging.unikiel.de/NeuroPostureApp) based on the following criteria (described in detail in a consensus study [4]): Total camptocormia (TCC) angle, defined as the angle between the line connecting the lateral malleolus to the L5 spinous process and the line connecting the L5 spinous process with the C7 spinous process [4], Upper camptocormia (UCC) angle, defined as the angle of the lines from the vertebral fulcrum to the spinous processes of L5 and C7, respectively [4], and lateral deviation (Pisa angle), defined as the angle between a line from the midpoint of the feet to the pubic symphysis and a line from the pubic symphysis to the jugular notch (Fig. 1).
PD symptom severity was evaluated with the Unified Parkinson’s Disease Rating Scale (UPDRS) [11], and an axial subscore [12] and the postural instability and gait difficulty (PIGD) score[13] were calculated.
Statistical analysis Mann-Whitney-U tests were performed for group comparisons. For the interrater and intrasubject test-retest reliability, intraclass correlation coefficients (ICCs) were calculated [14]. Minimal detectable change scores were computed for the TCC, UCC and Pisa angle for both cohorts separately according to [15]. Linear models for effects of disease, age and gender were calculated. Logarithmic transformation was used if the data did not fit linearity or if the data were not normally distributed. Post-hoc tests were conducted with Tukey correction for multiple comparisons. The level of significance was set at p<0.05. Statistical analysis were performed with R (version 1.0.136) [16].
Results Patients with PD and HC did not differ in age (PD: 59.0 (8.8); HC: 55.8 (14.2); p=0.054) or in the distribution of gender (f/m: PD: 62/130; HC: 32/43; p=0.146, Chi-square=2.1). Female and male PD patients did not differ in disease duration, disease severity (UPDRS total, UPDRS III), antiparkinsonian medication or the clinical assessment of posture (UPDRS item 28) (p>0.05). They did differ in age (p=0.003; women=61.8 (8.5); men=57.7 (8.7)). Please refer to Supplementary Table 1 for further details of the participant characteristics.
Figure 1 about here
Reliability and Minimal Detectable Change For the interrater reliability, intra-class coefficients (ICCs) were 0.95 (95% CI: 0.94-0.95), 0.83 (95% CI: 0.80-0.84) and 0.71 (95%CI: 0.67-0.74) for the TCC angle, UCC angle and Pisa angle assessment, respectively. This indicates excellent interrater reliability for the TCC angle, good reliability for the UCC angle and moderate reliability for the Pisa angle assessment [14]. For the intra-subject test-retest reliability, ICCs were 0.90 (95% CI: 0.88-0.92), 0.90 (95% CI:
0.88-0.92) and 0.88 (95% CI: 0.84-0.90) for TCC angle, UCC angle and Pisa angle, respectively, indicating excellent to good test-retest reliability. For HC the minimal detectable change (MDC) values were 2.2°, 5.1° and 1.2° for TCC angle, UCC angle and Pisa angle, respectively. For PD patients, the MDC values were 3.7°, 6.7° and 2.1° for the TCC angle, UCC angle and Pisa angle, respectively. Figure 1 shows the correlations between the measured angles and the clinical assessment (UPDRS, item 28). The correlation coefficients show a weak relationship between the two methods for all three angles. For TCC angle and Pisa angle the coefficients are slightly higher than for the UCC angle. Analyzing the slopes of the different correlations revealed significant differences between TCC versus UCC (p<0.001) and TCC versus Pisa (p=0.008) but not UCC versus Pisa (p=0.733). Expectedly, the clinical measurement covers a broad and overlapping range of angles demonstrating the greater subjectivity of the clinical score.
Postural alignment in healthy subjects Table 1 shows normative data for TCC angle, UCC angle and Pisa angle for the different age decades for HC as measured with the NeuroPostureApp©. Within the HC, the effect of age was not significant for the three angles (TCC angle: p=0.303, F=1.24; UCC angle: p=0.665, F=0.6; Pisa angle: p=0.457, F=0.92), indicating that neither the TCC-, UCC- nor the Pisa angle increased with age until 80 years. In contrast, the HC showed a significant difference between men and women , with a more pronounced bending in men on average by 1.6° for the TCC angle (p=0.03, F=4.9). Similar results were found for the UCC angle, with men having more stooped posture on average by 2.9° compared with women (p=0.011, F=6.7) (Supplementary Fig. 1). No significant effect of gender was found for the Pisa angle (p=0.81, F=0.06). No significant gender*age interaction was found (p>0.05), indicating that the development of postural abnormalities did not worsen differently between sexes over the different age groups.
Table 1 about here.
Patients with PD show impaired postural alignment that deteriorates with age compared with healthy controls A multivariate analysis of the role of diagnosis and age was performed. For the TCC angle a significant effect of group (p<0.001, F=183.6), age (p=0.001, F=4.7) and group*age interaction (p=0.046, F=2.5) was found. Post-hoc comparison revealed that for the group effect, PD showed larger TCC angles than HC for the age categories 40-49 (p=0.045), 50-59 (p<0.0001), 60-69 (p<0.0001) and 70-79 (p=0.004) years. For the effect of age, a significant difference was found in the PD patients when comparing the fifth and seventh decade (4049 and 60-69; p=0.005) (Fig. 2A). The significant group*age interaction indicates that the deterioration in postural alignment over time is greater for persons with PD compared with HC. For the UCC angle a significant group effect was found (p<0.001, F=57.7). Post-hoc testing showed significant differences between PD and HC for the sixth and seventh decades (50-59; p=0.003, and 60-69; p<0.001) (Fig. 2B). For the Pisa angle, a significant group effect was found (p<0.001, F=36.0). Post-hoc tests revealed a significant difference between PD and HC for persons aged 60-69 (p=0.026) (Fig. 2C).
Figure 2 about here.
Stratification of the cohort according to the severity of the postural angles The Spearman correlation of the three angles showed a weak positive relationship between TCC and Pisa angle (PD: p<0.001, R=0.27; HC: p=0.16, R=0.16), between TCC and UCC (PD: p=0.037, R=0.16; HC: p=0.46, R=0.087), and between UCC and Pisa (PD: p=0.001, R=0.24; HC: p=0.11, R=-0.19) for patients with PD (Fig. 3). We calculated a cut-off between HC and PD patients (blue lines in Fig. 3) based on the data of this study as the mean + 2 SD of the values in HC (TCC angle: 17.4°, UCC angle: 43.4°, Pisa angle: 2.6°) and a cut-off criterion between stooped posture and postural disorders (red lines in Fig. 3) based on data of this study as the mean + 2 SD of the values in PD (TCC angle: 30.2°, UCC angle: 50.9°, Pisa angle: 4.7°). According to these cut-off criteria we classified the PD patients into three subgroups: patients with a posture within normal limits (TCC angle: 39.1%, UCC angle: 67.7%, Pisa angle: 70.8%), patients with a presumed stooped or lateral
bended posture (TCC angle: 47.9%, UCC angle: 22.4%, Pisa angle: 17.7%), and patients with a postural disorder (TCC angle: 6.3%, UCC angle: 4.2%, Pisa angle: 6.8%). However, using the commonly employed, published criteria to describe postural disorders changed the stratification of the cohort: while twelve of 192 patients with PD had camptocormia (6.3 %), as clinically defined by TCC ≥30° [17], forty patients (20.8%) were diagnosed with upper camptocormia defined by an UCC angle >=45° [18]. Only two patients (1.0%) had a Pisa syndrome with an angle of lateral deviation ≥10° [19]. Interestingly, in our cohort there was no overlap of patients with camptocormia (TCC ≥30°) or Pisa syndrome with a lateral bending ≥10°. Only one patient suffered from both Pisa syndrome and upper camptocormia (UCC ≥45°). There was a more frequent overlap (n = 7) in the patients with TCC ≥30° and UCC ≥45°.
Figure 3 about here.
Discussion In this study, reliability of a standardized, objective and freely available web application to rate postural alignment was investigated, and posture was compared between healthy controls and people with PD. We found good to excellent interrater and test-retest reliability in assessing the TCC angle and UCC angle with the NeuroPostureApp©. However, interrater reliability was only moderate when rating the Pisa angle [4]. The degree of reliability is similar to that of an earlier paper [4], especially with regard to the TCC angle. Our data show that the used postural rating instrument is more sensitive to differences than the traditionally used UPDRS item 28. There is a profound overlap in angles for the different categories of this item. Although UPDRS has been used in many studies, our results show that UPDRS item 28 does not allow the reliable identification of patients with a postural disorder (such as camptocormia or Pisa syndrome). In addition, posture assessment with the NeuroPostureApp© does not require any other technical equipment, since photographs can be easily analyzed with the WebApp to measure postural angles. Minimal detectable change values were calculated for each of the three angles taking into account the reliability of the different angles [15]. This parameter depends on the precision of the measurement and indicates a threshold for a true difference between two angles that
is not likely to be due to chance variation in measurement and outside the range of statistical error [15]. The magnitude of the minimal detectable change values as set forth in this study may be useful in the interpretation of treatment effects. We provided normative data for the postural alignment of healthy controls in the AP and mediolateral (ML) directions for different age groups, and investigated the effect of gender. Our results confirm the results of previous studies [8, 20], which showed that men have a more stooped posture than women for the TCC angle and UCC angle. Interestingly, effects were strongest for the UCC angle, which reflects the bending of the upper body without involving the hip-angle. Possible reasons might be differences in postural control or in the biomechanics of the two sexes. We did not find any significant age-related differences in postural angles in the healthy controls. Another study [8] did find an effect of age on postural angles. A larger sample size, a greater age spread and a different method to measure postural angles in that study might explain this different finding. Our results showed that compared with HC, patients with PD have a more severe postural deviation in the AP and ML directions, as expected, and that the differences are particularly pronounced in the age range from 50 to 80 years. Furthermore, in contrast to HC, postural inclination progressed with aging for PD patients. Other studies showed similar findings and neuronal loss due to disease progression or aging-related temporal gradients were proposed as possible reasons [5, 7, 21]. On the basis of angle measurements in the HC cohort we defined cut-off criteria that differentiated PD patients with a normal posture from those with a pathologically stooped or lateral deviated posture. Notably, for the TCC angle 39.1%, for the UCC angle 67.7% and for the Pisa angle 70.8% of this cohort of advanced PD patients had postural angles within the range of HC. The defined cut-off criteria might help to objectively distinguish between normal and stooped posture of PD patients. We further defined cut-off criteria based on the data of our PD cohort, to differentiate between PD patients with a stooped/lateral-deviated posture and patients with a postural disorder such as camptocormia or Pisa syndrome. Of note, our calculated and empirically defined cut-off value of 30.2° for the TCC angle is a confirmation of the currently established value of ≥30° for the diagnosis of total camptocormia [4, 22]. Furthermore, it empirically confirms the criterion of ≥30° for the diagnosis of camptocormia as proposed in an earlier study in PD patients [17]. In addition,
we found a prevalence of 6.3% for patients with total camptocormia, which is in line with the frequently published prevalence rates [23, 24]. For upper camptocormia our calculated cut-off criterion of 50.9° was close to the published criterion of 45° [18]. However, the rather small difference of 6° between the two cut-off values was associated with a major difference of 16.6% (n = 32) in the patients identified as possibly affected with UCC. There is to date no empirical substantiation of the criterion for UCC, and this should be the target for future studies. Furthermore, while the TCC angle differed significantly between HC and PD patients in all age groups from 40 years onwards, differences between PD and HC in the UCC angle were only found for the age range from 50 to 70 years (Fig. 2). The correlation of TCC and UCC was weak. At present, we primarily recommend to use the TCC angle as a well studied overall measure in camptocormia. Further studies are necessary to gain empirical data for the concept of upper camptocormia. At present, one should avoid equating total camptocormia with lower camptocormia since this has not yet been investigated. With regard to the Pisa syndrome our empirically defined cut-off of 4.7° clearly differed from the criterion of 10° currently discussed in the literature [19]. Applying this criterion to our cohort resulted in only two patients being identified as having a Pisa syndrome. Another study found a similar low incidence of Pisa syndrome [25]. An overlap with camptocormia is not a possible explanation. Although we were not able to define clear diagnostic criteria due to further lacking clinical information, our data further confirm the 30° criterion in total camptocormia and underline the need of a further empirical assessment of the criteria for upper camptocormia and Pisa syndrome. It should be mentioned that the present study used a validated method for measuring the angles. There are other studies [5, 6] with larger cohorts of subjects and patients, but the landmarks they used do not correspond with those of the present method, and they did not provide interrater and test-retest reliability of their measures. They used the trochanter major and the acromion as representative landmarks for the core measurements of the vertebral column angles. This is most likely to have a systematically larger variation due to the variation between acromion and processus spinosus of C7, or to the uncertainties of the position of the trochanter major. Therefore, the angles found in their assessments cannot be directly compared with ours.
Conclusion The non-commercial NeuroPosturApp© assessed in this paper is a reliable and easy to handle tool for measuring postural alignment in healthy subjects and people with PD. The App proved to be capable of describing the total and upper camptocormia angles, and the Pisa angle. The App is freely accessible on http://www.neuroimaging.unikiel.de/NeuroPostureApp. The age-related changes in normal subjects are only mild but do differ between the sexes. The results of this study confirm the progression with age of the postural deviation in PD patients. This study empirically supports the TCC criterion of ≥30° described in the literature and emphasizes its use as a suitable overall measurement for camptocormia. Diagnostic criteria for upper camptocormia and Pisa syndrome should be further explored in future studies, taking into account detailed clinical information and other aspects such as patient reported outcomes. In addition, the presented rating tool needs to be assessed in interventional studies to determine its usefulness in detecting treatment effects.
Funding: This project was funded by the Deutsche Forschungsgemeinschaft (DFG, SFB 1261, TP B5) and the Franz & Ursula Coppenrath-Stiftung.
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Figures Fig. 1: Methods of angle assessment using the NeuroPostureApp (A, C, E), and Spearman correlation between angle assessment and the UPDRS item 28 (posture) for the TCC, UCC and Pisa angle (B, D, F).
Fig. 2: Posture of PD patients compared to healthy controls (HC) with respect to different age decades for A) TCC (total camptocormia) angle, B) UCC (upper camptocormia) angle and C) Pisa angle. The bars above figures A, B and C represent significant (p < 0.05) differences. Post-hoc comparisons were made with Tukey correction for multiple comparisons.
Fig. 3: Scatter plots of the combinations of the three angles (TCC, UCC and Pisa angle) with each other; Blue lines represent the mean +2 SD for HC; Red lines represent mean +2 SD for PD. HC: healthy controls; TCC: total camptocormia; UCC: upper camptocormia.
Table 1. Postural alignment in HC and PD patients for the different age groups. PD (n=192)
HC (n=75)
n
Mean (SD)
Median [Range]
95% CI
n
Mean (SD)
Median [Range]
Patients outside HC 95%CI (n (%))
30-39 40-49
12 13
9.92 (3.55) 11.14 (4.35) a
10 [5-17] 10 [6-15]
7.7 - 12.2 8.5 - 11.9
5 24
14.2 (4.8) 15.81 (5.82) a,e
11.5 [10-21] 16.5 [5-28]
2 (40) 17 (70)
50-59
19
9.16 (2.81) b
8 [5-15]
7.8 - 10.5
63
17.95 (6.51) b
Variable
Age group
TCC
60-69 UCC
Pisa
16
10 (4.08)
c
10.5 [2-17] d
7.8 - 12.2
83
21.38 (7.19)
16 [9-42]
56 (89)
c,e
20.5 [9.5-47]
75 (90)
d
70-79 30-39 40-49 50-59
15 12 13 19
11.53 (2.95) 34.25 (4.22) 33.43 (3.61) 33.95 (5.82) f
10 [8-16] 34 [27-41] 35 [23-37] 33 [21-46]
9.9 - 13.2 31.6 - 36.9 31.0 - 35.5 31.1 - 36.8
17 5 24 63
21.43 (5.79) 34.1 (5.27) 38.4 (6.05) 39.75 (6.48) f
20.5 [7.5-37] 32.5 [27.5-39.5] 38 [28-49] 40.5 [24.5-56]
16 (94) 4 (80) 18 (75) 48 (76)
60-69 70-79 30-39 40-49 50-59 60-69 70-79
16 15 12 13 19 16 15
34.38 (3.79) g 35.87 (5.15) 1.33 (0.78) 1 (0.88) 1 (0.82) 1.12 (0.72) h 0.8 (0.68)
33.5 [29-41] 36 [27-44] 1.5 [0-2] 1 [0-2] 1 [0-3] 1 [0-2] 1 [0-2]
32.4 - 36.4 33.0 - 38.7 0.8 - 1.8 0.4 - 1.4 0.6 - 1.4 0.7 - 1.5 0.4 - 1.2
83 17 5 24 63 83 17
41.54 (5.71) g 41.55 (6.05) 0.8 (0.45) 1.64 (0.82) 1.73 (1.27) 2.52 (2.12) h 2.55 (2.54)
41.75 [31-55] 39.75 [33-49] 0.5 [0.5-1.5] 1.5 [0-3] 1.5 [0.7] 2 [0-12.5] 1.5 [0-11.5]
65 (78) 12 (70) 3 (60) 17( 71) 45 (71) 51 (61) 11 (65)
Note. CI: confidence interval; HC: healthy controls; n: number of participants; PD: Parkinson’s disease; SD: standard deviation; TCC: total camptocormia; UCC: upper camptocormia. Values represent degrees (°); a, b, c, d, e, f, g, h significantly different (p<0.05).
A
TCC − Pisa
TCC (°)
40
Group
30
HC 20
PD
10
0 0
4
8
12
Pisa (°)
B
TCC − UCC
TCC (°)
40
Group
30
HC 20
PD
10
0 20
30
40
50
UCC (°)
C
UCC − Pisa
Pisa (°)
12
8
Group HC PD
4
0 20
30
40
UCC (°)
50
Highlights •
The free NeuroPostureApp proved reliable for precisely assessing posture.
•
Men had a more stooped posture than women.
•
In contrast to healthy controls (up to an age of 79 years) the posture of PD patients worsened with age.
•
The data empirically confirmed the diagnostic criterion ≥30° for total camptocormia.
S1353-8020(20)30022-5
DOI:
https://doi.org/10.1016/j.parkreldis.2020.01.012
Reference:
PRD 4257
To appear in:
Parkinsonism and Related Disorders
Received Date: 11 November 2019 Revised Date:
21 January 2020
Accepted Date: 23 January 2020
Please cite this article as: Schlenstedt C, Boße K, Gavriliuc O, Wolke R, Granert O, Deuschl Gü, Margraf NG, Quantitative assessment of posture in healthy controls and patients with Parkinson's disease, Parkinsonism and Related Disorders (2020), doi: https://doi.org/10.1016/ j.parkreldis.2020.01.012. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Quantitative assessment of posture in healthy controls and patients with Parkinson’s disease Christian Schlenstedt1*, Kathrin Boße1*, Olga Gavriliuc1, 2, Robin Wolke1, Oliver Granert1, Günther Deuschl1, Nils G. Margraf1
1 2
Department of Neurology, UKSH, Christian-Albrechts-University, Kiel, Germany Department of Neurology, State University of Medicine and Pharmacy “Nicolae Testemitanu”, Chisinau, Republic of Moldova
* These authors contributed equally.
Corresponding author: Prof. Dr. G. Deuschl, Department of Neurology, UKSH, Kiel Campus, Christian-Albrechts-University, Arnold-Heller-Str. 3, 24105 Kiel, Germany. E-mail address: [email protected].
Word count: 3109 Figures: 3 Tables: 1
Keywords: Parkinson’s disease, posture, angle measurement, camptocormia, forward bending, Pisa syndrome, axial symptoms, postural abnormalities.
Abstract Introduction A stooped posture is a main clinical feature of Parkinson’s disease (PD). The assessment of posture is important to measure treatment effects. The aim of this study was to investigate the reliability of a standardized postural rating tool, to calculate minimal detectable change scores and to assess the role of gender and age.
Methods Two independent raters assessed total camptocormia (TCC), upper camptocormia (UCC) and Pisa angles of 192 PD patients and 78 HC with the free NeuroPostureApp©(http://www.neuroimaging.uni-kiel.de/NeuroPostureApp). Reliabilities and linear models were calculated for different effects. Three subgroups were defined based on two thresholds (mean+2SD of HC and PD): A) normal, B) presumed stooped/lateral bended posture and C) postural disorder.
Results Intraclass correlation coefficients ranged between 0.71 and 0.95 for the interrater and testretest reliability of the three angles. The minimal detectable change values in the PD patients were 3.7°, 6.7° and 2.1° for the TCC, UCC and Pisa angle, respectively. Men had a more stooped posture than women (p<0.05). Patients with PD had a worse posture than HC (p<0.001) in all three angles. For the TCC angle, 39.1% of the patients had a normal posture (<17.4°), 47.9% a presumed stooped posture (>17.4°, <30.2°) and 6.3° had camptocormia (>30.2°).
Conclusions The NeuroPostureApp© is reliable. Our results confirmed gender differences and the progression of postural deviation in PD patients with age and empirically support the ≥30° TCC angle as a defining criterium for camptocormia. Diagnostic criteria for UCC and Pisa syndrome should be further explored in future studies.
Introduction A bent posture is a main clinical feature of Parkinson’s disease (PD). Postural impairments are independent risk factors for falls [1] and reduce the patients’ mobility and autonomy [2]. While dynamic postural control is increasingly being studied with neurophysiological methods and technical devices [3], postural alignment is traditionally measured with clinical scales such as the Unified Parkinson’s disease Rating Scale (UPDRS) item 28. The 4-point ordinal scaled UPDRS item 28 gives only a broad classification of posture but is not suited for a more detailed description of posture and may not be sensitive to change. Furthermore, a differentiation in the postural disorders camptocormia or Pisa syndrome is not intended. While a consensus was reached for the method of angle assessment in camptocormia [4], a further empirical substantiation of a threshold value for the angle criterion is still lacking for camptocormia and Pisa syndrome. Recently, studies have described postural alignment by rating postural angles from photographs. They found larger angles for dropped head, and anterior and lateral flexion in patients with PD than in healthy controls (HC) [5, 6]. Other studies with similar methodological approaches found an effect of age on postural alignment for patients with PD [7] and HC [8]. Another study, which used clinical rating criteria instead of postural angles, found an association between posture and disease severity [9]. Most of the existing studies that characterized posture by rating photographs assessed postural angles manually using different methods, and no information about the reliability or validity of these procedures was given. Therefore, simple objective and reliable angle measurement methods are needed. A recent study has validated a measurement of the forward bending angle using a free, software-supported tool [4]. This measurement proved to be valid for quantifying the anteroposterior (AP) angle and is applied here and extended by a frontal view to measure the lateral angle (Pisa-deviation). This study had the following aims: First, to investigate the reliability of a standardized, software-supported, postural rating assessment. The test-retest- as well as the interrater reliability and minimal detectable change scores will be evaluated, and the test instrument will be related to other clinical scales; second, to provide normative data of postural alignment for HC for this specific tool and to investigate the effect of gender and age, and third, to use the clinical rating instrument to compare the posture of patients with PD with HC and to study the progression of postural inclination with age for the two cohorts. Finally, the data of HC and PD will be used to discuss currently available criteria for the clinical
diagnosis of camptocormia, also taking upper camptocormia and Pisa syndrome in PD into consideration.
Methods Participants One hundred and ninety-two patients with idiopathic PD according to the UK Brain Bank PD criteria [10] were included in this study (Supplementary Table 1). We included 78 healthy controls between the 30 to 79 years old, with 10 to 20 from each decade. Exclusion criteria were neurological disease, other than PD, or injuries that could affect gait and posture. The HC were recruited from the patients’ relatives. The ethics committee of the medical faculty of Kiel University approved the study. Informed consent was obtained from all participants.
Testing Postural alignment was assessed using photos captured from videos showing a standardized walking task, depicting the posture in the frontal and sagittal planes. Two photos of each participant were taken; a strictly lateral and a frontal view. The pictures were anonymized and blindly rated by two independent raters (KB, OG). All PD patients were rated in Med-OFF condition, after having withdrawn L-dopa for 12 h and dopamine-agonists for 72 h. The same raters reassessed photos of 50 randomly selected participants four weeks later to determine intra-subject test-retest reliability. The posture was rated with the NeuroPostureApp© (http://www.neuroimaging.unikiel.de/NeuroPostureApp) based on the following criteria (described in detail in a consensus study [4]): Total camptocormia (TCC) angle, defined as the angle between the line connecting the lateral malleolus to the L5 spinous process and the line connecting the L5 spinous process with the C7 spinous process [4], Upper camptocormia (UCC) angle, defined as the angle of the lines from the vertebral fulcrum to the spinous processes of L5 and C7, respectively [4], and lateral deviation (Pisa angle), defined as the angle between a line from the midpoint of the feet to the pubic symphysis and a line from the pubic symphysis to the jugular notch (Fig. 1).
PD symptom severity was evaluated with the Unified Parkinson’s Disease Rating Scale (UPDRS) [11], and an axial subscore [12] and the postural instability and gait difficulty (PIGD) score[13] were calculated.
Statistical analysis Mann-Whitney-U tests were performed for group comparisons. For the interrater and intrasubject test-retest reliability, intraclass correlation coefficients (ICCs) were calculated [14]. Minimal detectable change scores were computed for the TCC, UCC and Pisa angle for both cohorts separately according to [15]. Linear models for effects of disease, age and gender were calculated. Logarithmic transformation was used if the data did not fit linearity or if the data were not normally distributed. Post-hoc tests were conducted with Tukey correction for multiple comparisons. The level of significance was set at p<0.05. Statistical analysis were performed with R (version 1.0.136) [16].
Results Patients with PD and HC did not differ in age (PD: 59.0 (8.8); HC: 55.8 (14.2); p=0.054) or in the distribution of gender (f/m: PD: 62/130; HC: 32/43; p=0.146, Chi-square=2.1). Female and male PD patients did not differ in disease duration, disease severity (UPDRS total, UPDRS III), antiparkinsonian medication or the clinical assessment of posture (UPDRS item 28) (p>0.05). They did differ in age (p=0.003; women=61.8 (8.5); men=57.7 (8.7)). Please refer to Supplementary Table 1 for further details of the participant characteristics.
Figure 1 about here
Reliability and Minimal Detectable Change For the interrater reliability, intra-class coefficients (ICCs) were 0.95 (95% CI: 0.94-0.95), 0.83 (95% CI: 0.80-0.84) and 0.71 (95%CI: 0.67-0.74) for the TCC angle, UCC angle and Pisa angle assessment, respectively. This indicates excellent interrater reliability for the TCC angle, good reliability for the UCC angle and moderate reliability for the Pisa angle assessment [14]. For the intra-subject test-retest reliability, ICCs were 0.90 (95% CI: 0.88-0.92), 0.90 (95% CI:
0.88-0.92) and 0.88 (95% CI: 0.84-0.90) for TCC angle, UCC angle and Pisa angle, respectively, indicating excellent to good test-retest reliability. For HC the minimal detectable change (MDC) values were 2.2°, 5.1° and 1.2° for TCC angle, UCC angle and Pisa angle, respectively. For PD patients, the MDC values were 3.7°, 6.7° and 2.1° for the TCC angle, UCC angle and Pisa angle, respectively. Figure 1 shows the correlations between the measured angles and the clinical assessment (UPDRS, item 28). The correlation coefficients show a weak relationship between the two methods for all three angles. For TCC angle and Pisa angle the coefficients are slightly higher than for the UCC angle. Analyzing the slopes of the different correlations revealed significant differences between TCC versus UCC (p<0.001) and TCC versus Pisa (p=0.008) but not UCC versus Pisa (p=0.733). Expectedly, the clinical measurement covers a broad and overlapping range of angles demonstrating the greater subjectivity of the clinical score.
Postural alignment in healthy subjects Table 1 shows normative data for TCC angle, UCC angle and Pisa angle for the different age decades for HC as measured with the NeuroPostureApp©. Within the HC, the effect of age was not significant for the three angles (TCC angle: p=0.303, F=1.24; UCC angle: p=0.665, F=0.6; Pisa angle: p=0.457, F=0.92), indicating that neither the TCC-, UCC- nor the Pisa angle increased with age until 80 years. In contrast, the HC showed a significant difference between men and women , with a more pronounced bending in men on average by 1.6° for the TCC angle (p=0.03, F=4.9). Similar results were found for the UCC angle, with men having more stooped posture on average by 2.9° compared with women (p=0.011, F=6.7) (Supplementary Fig. 1). No significant effect of gender was found for the Pisa angle (p=0.81, F=0.06). No significant gender*age interaction was found (p>0.05), indicating that the development of postural abnormalities did not worsen differently between sexes over the different age groups.
Table 1 about here.
Patients with PD show impaired postural alignment that deteriorates with age compared with healthy controls A multivariate analysis of the role of diagnosis and age was performed. For the TCC angle a significant effect of group (p<0.001, F=183.6), age (p=0.001, F=4.7) and group*age interaction (p=0.046, F=2.5) was found. Post-hoc comparison revealed that for the group effect, PD showed larger TCC angles than HC for the age categories 40-49 (p=0.045), 50-59 (p<0.0001), 60-69 (p<0.0001) and 70-79 (p=0.004) years. For the effect of age, a significant difference was found in the PD patients when comparing the fifth and seventh decade (4049 and 60-69; p=0.005) (Fig. 2A). The significant group*age interaction indicates that the deterioration in postural alignment over time is greater for persons with PD compared with HC. For the UCC angle a significant group effect was found (p<0.001, F=57.7). Post-hoc testing showed significant differences between PD and HC for the sixth and seventh decades (50-59; p=0.003, and 60-69; p<0.001) (Fig. 2B). For the Pisa angle, a significant group effect was found (p<0.001, F=36.0). Post-hoc tests revealed a significant difference between PD and HC for persons aged 60-69 (p=0.026) (Fig. 2C).
Figure 2 about here.
Stratification of the cohort according to the severity of the postural angles The Spearman correlation of the three angles showed a weak positive relationship between TCC and Pisa angle (PD: p<0.001, R=0.27; HC: p=0.16, R=0.16), between TCC and UCC (PD: p=0.037, R=0.16; HC: p=0.46, R=0.087), and between UCC and Pisa (PD: p=0.001, R=0.24; HC: p=0.11, R=-0.19) for patients with PD (Fig. 3). We calculated a cut-off between HC and PD patients (blue lines in Fig. 3) based on the data of this study as the mean + 2 SD of the values in HC (TCC angle: 17.4°, UCC angle: 43.4°, Pisa angle: 2.6°) and a cut-off criterion between stooped posture and postural disorders (red lines in Fig. 3) based on data of this study as the mean + 2 SD of the values in PD (TCC angle: 30.2°, UCC angle: 50.9°, Pisa angle: 4.7°). According to these cut-off criteria we classified the PD patients into three subgroups: patients with a posture within normal limits (TCC angle: 39.1%, UCC angle: 67.7%, Pisa angle: 70.8%), patients with a presumed stooped or lateral
bended posture (TCC angle: 47.9%, UCC angle: 22.4%, Pisa angle: 17.7%), and patients with a postural disorder (TCC angle: 6.3%, UCC angle: 4.2%, Pisa angle: 6.8%). However, using the commonly employed, published criteria to describe postural disorders changed the stratification of the cohort: while twelve of 192 patients with PD had camptocormia (6.3 %), as clinically defined by TCC ≥30° [17], forty patients (20.8%) were diagnosed with upper camptocormia defined by an UCC angle >=45° [18]. Only two patients (1.0%) had a Pisa syndrome with an angle of lateral deviation ≥10° [19]. Interestingly, in our cohort there was no overlap of patients with camptocormia (TCC ≥30°) or Pisa syndrome with a lateral bending ≥10°. Only one patient suffered from both Pisa syndrome and upper camptocormia (UCC ≥45°). There was a more frequent overlap (n = 7) in the patients with TCC ≥30° and UCC ≥45°.
Figure 3 about here.
Discussion In this study, reliability of a standardized, objective and freely available web application to rate postural alignment was investigated, and posture was compared between healthy controls and people with PD. We found good to excellent interrater and test-retest reliability in assessing the TCC angle and UCC angle with the NeuroPostureApp©. However, interrater reliability was only moderate when rating the Pisa angle [4]. The degree of reliability is similar to that of an earlier paper [4], especially with regard to the TCC angle. Our data show that the used postural rating instrument is more sensitive to differences than the traditionally used UPDRS item 28. There is a profound overlap in angles for the different categories of this item. Although UPDRS has been used in many studies, our results show that UPDRS item 28 does not allow the reliable identification of patients with a postural disorder (such as camptocormia or Pisa syndrome). In addition, posture assessment with the NeuroPostureApp© does not require any other technical equipment, since photographs can be easily analyzed with the WebApp to measure postural angles. Minimal detectable change values were calculated for each of the three angles taking into account the reliability of the different angles [15]. This parameter depends on the precision of the measurement and indicates a threshold for a true difference between two angles that
is not likely to be due to chance variation in measurement and outside the range of statistical error [15]. The magnitude of the minimal detectable change values as set forth in this study may be useful in the interpretation of treatment effects. We provided normative data for the postural alignment of healthy controls in the AP and mediolateral (ML) directions for different age groups, and investigated the effect of gender. Our results confirm the results of previous studies [8, 20], which showed that men have a more stooped posture than women for the TCC angle and UCC angle. Interestingly, effects were strongest for the UCC angle, which reflects the bending of the upper body without involving the hip-angle. Possible reasons might be differences in postural control or in the biomechanics of the two sexes. We did not find any significant age-related differences in postural angles in the healthy controls. Another study [8] did find an effect of age on postural angles. A larger sample size, a greater age spread and a different method to measure postural angles in that study might explain this different finding. Our results showed that compared with HC, patients with PD have a more severe postural deviation in the AP and ML directions, as expected, and that the differences are particularly pronounced in the age range from 50 to 80 years. Furthermore, in contrast to HC, postural inclination progressed with aging for PD patients. Other studies showed similar findings and neuronal loss due to disease progression or aging-related temporal gradients were proposed as possible reasons [5, 7, 21]. On the basis of angle measurements in the HC cohort we defined cut-off criteria that differentiated PD patients with a normal posture from those with a pathologically stooped or lateral deviated posture. Notably, for the TCC angle 39.1%, for the UCC angle 67.7% and for the Pisa angle 70.8% of this cohort of advanced PD patients had postural angles within the range of HC. The defined cut-off criteria might help to objectively distinguish between normal and stooped posture of PD patients. We further defined cut-off criteria based on the data of our PD cohort, to differentiate between PD patients with a stooped/lateral-deviated posture and patients with a postural disorder such as camptocormia or Pisa syndrome. Of note, our calculated and empirically defined cut-off value of 30.2° for the TCC angle is a confirmation of the currently established value of ≥30° for the diagnosis of total camptocormia [4, 22]. Furthermore, it empirically confirms the criterion of ≥30° for the diagnosis of camptocormia as proposed in an earlier study in PD patients [17]. In addition,
we found a prevalence of 6.3% for patients with total camptocormia, which is in line with the frequently published prevalence rates [23, 24]. For upper camptocormia our calculated cut-off criterion of 50.9° was close to the published criterion of 45° [18]. However, the rather small difference of 6° between the two cut-off values was associated with a major difference of 16.6% (n = 32) in the patients identified as possibly affected with UCC. There is to date no empirical substantiation of the criterion for UCC, and this should be the target for future studies. Furthermore, while the TCC angle differed significantly between HC and PD patients in all age groups from 40 years onwards, differences between PD and HC in the UCC angle were only found for the age range from 50 to 70 years (Fig. 2). The correlation of TCC and UCC was weak. At present, we primarily recommend to use the TCC angle as a well studied overall measure in camptocormia. Further studies are necessary to gain empirical data for the concept of upper camptocormia. At present, one should avoid equating total camptocormia with lower camptocormia since this has not yet been investigated. With regard to the Pisa syndrome our empirically defined cut-off of 4.7° clearly differed from the criterion of 10° currently discussed in the literature [19]. Applying this criterion to our cohort resulted in only two patients being identified as having a Pisa syndrome. Another study found a similar low incidence of Pisa syndrome [25]. An overlap with camptocormia is not a possible explanation. Although we were not able to define clear diagnostic criteria due to further lacking clinical information, our data further confirm the 30° criterion in total camptocormia and underline the need of a further empirical assessment of the criteria for upper camptocormia and Pisa syndrome. It should be mentioned that the present study used a validated method for measuring the angles. There are other studies [5, 6] with larger cohorts of subjects and patients, but the landmarks they used do not correspond with those of the present method, and they did not provide interrater and test-retest reliability of their measures. They used the trochanter major and the acromion as representative landmarks for the core measurements of the vertebral column angles. This is most likely to have a systematically larger variation due to the variation between acromion and processus spinosus of C7, or to the uncertainties of the position of the trochanter major. Therefore, the angles found in their assessments cannot be directly compared with ours.
Conclusion The non-commercial NeuroPosturApp© assessed in this paper is a reliable and easy to handle tool for measuring postural alignment in healthy subjects and people with PD. The App proved to be capable of describing the total and upper camptocormia angles, and the Pisa angle. The App is freely accessible on http://www.neuroimaging.unikiel.de/NeuroPostureApp. The age-related changes in normal subjects are only mild but do differ between the sexes. The results of this study confirm the progression with age of the postural deviation in PD patients. This study empirically supports the TCC criterion of ≥30° described in the literature and emphasizes its use as a suitable overall measurement for camptocormia. Diagnostic criteria for upper camptocormia and Pisa syndrome should be further explored in future studies, taking into account detailed clinical information and other aspects such as patient reported outcomes. In addition, the presented rating tool needs to be assessed in interventional studies to determine its usefulness in detecting treatment effects.
Funding: This project was funded by the Deutsche Forschungsgemeinschaft (DFG, SFB 1261, TP B5) and the Franz & Ursula Coppenrath-Stiftung.
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Figures Fig. 1: Methods of angle assessment using the NeuroPostureApp (A, C, E), and Spearman correlation between angle assessment and the UPDRS item 28 (posture) for the TCC, UCC and Pisa angle (B, D, F).
Fig. 2: Posture of PD patients compared to healthy controls (HC) with respect to different age decades for A) TCC (total camptocormia) angle, B) UCC (upper camptocormia) angle and C) Pisa angle. The bars above figures A, B and C represent significant (p < 0.05) differences. Post-hoc comparisons were made with Tukey correction for multiple comparisons.
Fig. 3: Scatter plots of the combinations of the three angles (TCC, UCC and Pisa angle) with each other; Blue lines represent the mean +2 SD for HC; Red lines represent mean +2 SD for PD. HC: healthy controls; TCC: total camptocormia; UCC: upper camptocormia.
Table 1. Postural alignment in HC and PD patients for the different age groups. PD (n=192)
HC (n=75)
n
Mean (SD)
Median [Range]
95% CI
n
Mean (SD)
Median [Range]
Patients outside HC 95%CI (n (%))
30-39 40-49
12 13
9.92 (3.55) 11.14 (4.35) a
10 [5-17] 10 [6-15]
7.7 - 12.2 8.5 - 11.9
5 24
14.2 (4.8) 15.81 (5.82) a,e
11.5 [10-21] 16.5 [5-28]
2 (40) 17 (70)
50-59
19
9.16 (2.81) b
8 [5-15]
7.8 - 10.5
63
17.95 (6.51) b
Variable
Age group
TCC
60-69 UCC
Pisa
16
10 (4.08)
c
10.5 [2-17] d
7.8 - 12.2
83
21.38 (7.19)
16 [9-42]
56 (89)
c,e
20.5 [9.5-47]
75 (90)
d
70-79 30-39 40-49 50-59
15 12 13 19
11.53 (2.95) 34.25 (4.22) 33.43 (3.61) 33.95 (5.82) f
10 [8-16] 34 [27-41] 35 [23-37] 33 [21-46]
9.9 - 13.2 31.6 - 36.9 31.0 - 35.5 31.1 - 36.8
17 5 24 63
21.43 (5.79) 34.1 (5.27) 38.4 (6.05) 39.75 (6.48) f
20.5 [7.5-37] 32.5 [27.5-39.5] 38 [28-49] 40.5 [24.5-56]
16 (94) 4 (80) 18 (75) 48 (76)
60-69 70-79 30-39 40-49 50-59 60-69 70-79
16 15 12 13 19 16 15
34.38 (3.79) g 35.87 (5.15) 1.33 (0.78) 1 (0.88) 1 (0.82) 1.12 (0.72) h 0.8 (0.68)
33.5 [29-41] 36 [27-44] 1.5 [0-2] 1 [0-2] 1 [0-3] 1 [0-2] 1 [0-2]
32.4 - 36.4 33.0 - 38.7 0.8 - 1.8 0.4 - 1.4 0.6 - 1.4 0.7 - 1.5 0.4 - 1.2
83 17 5 24 63 83 17
41.54 (5.71) g 41.55 (6.05) 0.8 (0.45) 1.64 (0.82) 1.73 (1.27) 2.52 (2.12) h 2.55 (2.54)
41.75 [31-55] 39.75 [33-49] 0.5 [0.5-1.5] 1.5 [0-3] 1.5 [0.7] 2 [0-12.5] 1.5 [0-11.5]
65 (78) 12 (70) 3 (60) 17( 71) 45 (71) 51 (61) 11 (65)
Note. CI: confidence interval; HC: healthy controls; n: number of participants; PD: Parkinson’s disease; SD: standard deviation; TCC: total camptocormia; UCC: upper camptocormia. Values represent degrees (°); a, b, c, d, e, f, g, h significantly different (p<0.05).
A
TCC − Pisa
TCC (°)
40
Group
30
HC 20
PD
10
0 0
4
8
12
Pisa (°)
B
TCC − UCC
TCC (°)
40
Group
30
HC 20
PD
10
0 20
30
40
50
UCC (°)
C
UCC − Pisa
Pisa (°)
12
8
Group HC PD
4
0 20
30
40
UCC (°)
50
Highlights •
The free NeuroPostureApp proved reliable for precisely assessing posture.
•
Men had a more stooped posture than women.
•
In contrast to healthy controls (up to an age of 79 years) the posture of PD patients worsened with age.
•
The data empirically confirmed the diagnostic criterion ≥30° for total camptocormia.