Postural instability in the anterior-posterior plane is associated with impaired postural verticality perception and fall risk in Parkinsonian syndromes

Postural instability in the anterior-posterior plane is associated with impaired postural verticality perception and fall risk in Parkinsonian syndromes | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Postural instability in the anterior-posterior plane is associated with impaired postural verticality perception and fall risk in Parkinsonian syndromes Jeannine Bergmann, Carmen Krewer, Friedemann Müller, Klaus Jahn This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3857208/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Retropulsion is a postural behavior which seems frequent in Parkinsonian syndromes, hampering balance and functional tasks, as well as entailing an increase in the risk of falls. This study aimed to investigate different characteristics of retropulsion and their relation to functional disability, postural control and fall risk. Thirty subjects with Parkinsonian syndromes (75 ± 8 years, 13 female, 6 ± 5 years since diagnosis, median UPDRS III 33 (Q1-Q3 22–40), Hoehn and Yahr stage 3 ( 2 – 4 )) were assessed with the Scale for Retropulsion (SRP), the Berg Balance Scale, the subjective postural vertical, and diagnostic scales. The number of falls within the last 12 months and fall risk was determined. Results revealed signs of retropulsion in 87% of subjects. The SRP score correlated moderately to well with functional disability and disease severity, and strongly with the Berg Balance Scale. The severity of retropulsion was further associated with a backward shifted verticality perception. The SRP significantly differed between recurrent fallers and single or non-fallers and identified subjects at risk of falling. In summary, retropulsion is very frequent in Parkinsonian syndromes. Subjects with an SRP score ≥ 3 have an impaired reference of verticality with considerable balance impairments and an increased risk of falling. Health sciences/Neurology/Neurological disorders/Parkinsons disease Health sciences/Neurology/Neurological disorders/Neurodegenerative diseases Figures Figure 1 Figure 2 Introduction The Parkinsonian syndromes include idiopathic Parkinon’s disease (PD), progressive supranuclear palsy, multiple system atrophy, corticobasal degeneration, vascular Parkinsonism, and some other rare causes of parkinsonism. Besides bradykinesia, which is an essential sign that often leads to a diagnosis of parkinsonism, extrapyramidal rigidity, resting tremor and postural instability are cardinal signs of Parkinsonian syndromes and features of basal ganglia dysfunction. Postural instability is common in advanced PD but may also be an important early sign in other Parkinsonian syndromes. 1 In PD, postural instability becomes more prevalent and worsens with disease progression, but can also be present at an early stage. 2,3 In the advanced stages of the disease, postural instability is one of the most disabling symptoms and is associated with an increased risk of falls. 4,5 Falls and fear of falling are major determinants for poor quality of life, reduced mobility, and physical deconditioning. 6,7 One problem is the postural instability in the anterior-posterior plane, also described as retropulsion. As we understand it, retropulsion describes an active posterior displacement of the center of mass with a tendency to fall backwards, problems in shifting the center of mass actively forward, and resistance against passive correction. 8 This behavior may hamper sitting and standing and also the ability to perform functional tasks such as transferring and walking. In addition, it might be associated with an increased risk of falling. The retropulsion test (pull test) assesses the subject’s postural reaction to a rapid balance perturbation in the backward direction. It is a key component of the neurological examination and widely regarded as the gold standard to evaluate postural instability in subjects with PD. 9 However, this single-item test has only moderate reliability and correlates poorly with objective measures of balance and the number of falls. 10,11 One reason for the poor validity might be that the test captures only a fraction of the postural deficits in PD. Indeed, postural deficits in the sagittal plane can vary and include increased postural sway, reduced postural stability margins, impaired anticipatory postural adjustment, and deficient dynamic balance control. 5,12 Recently, the Scale for Retropulsion (SRP) was designed and evaluated for neurological disorders. 8,13 The scale covers different characteristics of retropulsion such as spontaneous posterior body tilt with the tendency of backward falling, insufficient reactive postural responses, an active backward pushing with resistance against passive correction, and the difficulty of shifting the center of mass actively forward. While subjects with Parkinsonian syndromes show abnormal postural control, the characteristics and the underlying pathology seem to be different. 14 The objective of this study was to investigate the different characteristics of retropulsion in individuals with Parkinsonian syndromes and their relation to measures of functional disability associated with parkinsonism, postural control and fall risk. Methods Participants Individuals included in the study met the following inclusion criteria: Parkinsonian syndrome according to the United Kingdom Parkinson’s Disease Society Brain Bank criteria, age 18 to 90 years, and postural instability. Subjects with orthopaedic hip problems, which limited hip flexion between 70° and 120°, were excluded from the study. Participants were tested when they were in a self-reported “on” state and felt mobile and comfortable. This study was approved by the Ethics Committee of the Ludwig-Maximilians-Universität München (number 405 − 11). All experiments were performed in accordance with relevant named guidelines and regulations. Informed written consent was obtained from the participants or their legal representatives. Outcome measures The SRP is a bedside test and comprises the following four subtests: static postural control, reactive postural control, resistance against correction, and dynamic postural control. 8 All subtests are tested in a sitting and a standing starting position resulting in eight items. Each item is rated on a fourpoint scale from 0 to 3. The total score ranges from 0 (no signs of retropulsion) to 24 (severe retropulsion). The SRP had excellent internal consistency, good to excellent test-retest and interrater reliabilities, and good content and construct validities for subjects with neurological disorders. The German version of the SRP was used. 13 The Berg Balance Scale determines balance function during a series of predetermined tasks on a five point scale from 0 to 4. 15 The total score ranges from 0 to 56 with higher scores representing higher balance function. Body sway and the limits of stability were assessed by using a Kistler force plate (Type 9260AA) and the Mars 3.0 software (Kistler, Winterthur, Switzerland). Body sway was recorded during 30 seconds of static standing with eyes open. The limits of stability were assessed in the anterior-posterior and the medio-lateral directions. The ratio of body sway to limits of stability was calculated as the ratio of the maximum sway amplitude in the anterior-posterior and the medio-lateral directions to the limits of stability in the respective planes. The subjective postural vertical (SPV) during standing was determined in the sagittal and frontal planes by using the Spacecurl. The apparatus and the experimental procedure used are described elsewhere. 16 The SPV error was calculated by averaging the six trials per plane. SPV measurements have good test-retest and interrater reliabilities 16 . The stages of the Parkinsonian syndromes were determined by the Hoehn and Yahr Staging Scale. 17 The categories described by Goetz et al. 18 were used to classify participants according to the severity of PD symptoms (stages 1 and 2, mild; stage 3, moderate; and stages 4 and 5, severe). The severity of PD was graded by the Unified Parkinson’s Disease Rating Scale III Motor part (UPDRS III). The UPDRS was obtained by the treating neurologist and extracted from the electronic patient file. The rate of falls was assessed by asking the participants for the number of falls within the last 12 months. Subjects who fell more than once within the last 12 months were classified as recurrent fallers. In addition, the Timed-Up and Go test was performed as an indicator of fall risk (cut-off ≥ 11.5 sec. indicating an increased risk). 19 Data analysis Descriptive statistics were applied to describe clinical characteristics of participants and the results from the SRP testing. Mann-Whitney-U tests were used to compare the SRP score of recurrent fallers with single and non-fallers, as well as to compare the SRP score of participants with an increased risk of falling according to the Timed-Up and Go test with participants with no increased fall risk. Spearman’s rank correlation (r Sp ) was used to determine construct validity of the SRP. The strength of the correlation was interpreted as: i) little or no correlation (r Sp r Sp ≤0.50), iii) moderate to good correlation (0.50 > r Sp ≤0.75) and good to excellent (r Sp >0.75). 20 Statistical analyses were performed using SPSS version 19. The level of significance was set at p < 0.05. Results Participants 30 individuals with Parkinsonian syndromes were included in the study (age: 75 ± 8 years, sex:13 female). The median UPDRS III score was 33 (Q1-Q3 22–40), the median Hoehn and Yahr stage 3 (Q1-Q3 2–4), and the average time since diagnosis was 6 ± 5 years. 24 of these individuals were diagnosed with PD (age: 74 ± 7 years, sex: 10 female, Hoehn and Yahr: 3 ( 2 – 4 ), years since diagnosis: 7 ± 6), 4 with progressive supranuclear palsy (age: 75 ± 10 years, sex: 3 female, Hoehn and Yahr: 3 (2.5–3.5), years since diagnosis: 5 ± 4) and 2 with vascular Parkinsonism (age: 82 ± 1 years, sex: 0 female, Hoehn and Yahr: 3.5 ( 2 – 5 ), years since diagnosis: 3 ± 1). Two patients were not able to perform the posturographic measurements and the SPV assessment due to their severe impairments. The UPDRS III was missing in eight individuals (no documentation in the patient file) and the fall rate was not provided in five participants. Scale for Retropulsion The median SRP score was 3 (Q1-Q3 1–5; minimum 0, maximum 17). Of the 30 individuals, 26 (86.7%) showed signs of retropulsion measured with the SRP. When looking at the SRP subtests, 11/30 (36.7%, median 0, Q1-Q3 0–1) showed signs of retropulsion at the subtest “static postural control”, 24/30 (80.0%, median 2, Q1-Q3 1–3) at the subtest “reactive postural control”, 15/30 (50.0%, median 1, Q1-Q3 0–1) at the subtest “resistance”, and 8/30 (26.7%, median 0, Q1-Q3 0–1) at the subtest “dynamic postural control”. Additionally, SRP scores were analyzed separately for individuals with PD, for individuals with progressive supranuclear palsy, and for individuals with vascular Parkinsonism, as shown in Table 1 . Table 1 Total SRP score and scores of the different SRP subtests for participants with Parkinson’s disease, progressive supranuclear palsy and vascular Parkinsonism Idiopathic Parkinson’s disease (n = 24) Progressive supranuclear palsy (n = 4) Vascular Parkinsonism (n = 2) Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion SRP total score 3 1–5 0–17 20 (83.3%) 3 3–6 3–9 4 (100%) 10 5–15 5–15 2 (100%) Subtest A Static postural control 0 0–1 0–4 8 (33.3%) 0 0–1 0–2 1 (25%) 3 1–4 1–4 2 (100%) Subtest B Reactive postural control) 2 1–2 0–4 18 (75.0%) 3 2–3 2–3 4 (100%) 2 1–3 1–3 2 (100%) Subtest C Resistance 0 0–1 0–4 10 (41.7%) 1 1–1 0–1 3 (75%) 3 3–3 3–3 2 (100%) Subtest D Dynamic postural control 0 0–1 0–5 6 (25.0%) 0 0–2 0–3 1 (25%) 3 0–5 0–5 1 (50%) When classifying the individuals according to the severity categories described by Goetz et al. 18 , the SRP scores significantly differed between these categories (Chi 2 = 10.379, p = 0.006): mild PD symptoms resulted in a median SRP score of 2 (Q1-Q3 0–3, n = 12), moderate symptoms in a median SPR score of 3 (3–5, n = 8), and severe symptoms in a median SRP score of 5 (4–10, n = 10). The results of the different subtests for these three categories can be found in Table 2 . Table 2 Total SRP score and scores of the different SRP subtests for subjects with mild, moderate and severe Parkinson’s disease symptoms according to Hoehn and Yahr staging. Mild Parkinson’s symptoms (n = 12) Moderate Parkinson’s symptoms (n = 8) Severe Parkinson’s symptoms (n = 10) Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion Median Q1-Q3 Min-Max Number of subjects with signs of retropulsion SRP total score 2 0–3 0–5 8 (66.7%) 3 3–5 1–8 8 (100%) 5 4–10 1–17 10 (100%) Subtest A Static postural control 0 0–0 0–1 2 (16.7%) 0 0–1 0–1 2 (25%) 1 0–2 0–4 7 (70%) Subtest B Reactive postural control 1 0–2 0–3 8 (66.7%) 2 2–3 1–3 8 (100%) 2 2–3 0–4 8 (80%) Subtest C Resistance 0 0–1 0–3 3 (25.0%) 0 0–1 0–2 3 (37.5%) 1 1–3 0–4 9 (90%) Subtest D Dynamic postural control 0 0–0 0–0 0 (0.0%) 0 0–1 0–5 2 (25%) 2 0–3 0–5 6 (60%) Correlation with measures for functional disability, postural control and falls The SRP score showed moderate to good correlations with Hoehn and Yahr staging (r Sp =0.668; p < 0.001) and the UPDRS III scoring (r Sp =0.582; p = 0.005). There was a strong correlation of the SRP with the Berg Balance Scale (r Sp =-0.823; p < 0.001) (Fig. 1 ). The SRP score moderately correlated with the sway area of the center of pressure during static standing (r Sp =0.571; p = 0.002). Correlations of the SRP with the limits of stability were fair in the anterior-posterior plane (r Sp =-0.490; p = 0.008) and not significant in the medio-lateral plane (p = 0.123). However, good correlations of the SRP score with the ratio body sway to limits of stability in the anterior-posterior plane (r Sp =0.714; p < 0.001) and in the medio-lateral plane (r Sp =0.637; p < 0.001) were found. The SRP score significantly correlated with the SPV error in the sagittal plane (r Sp =-0.499; p = 0.007), but not with the SPV in the frontal plane (p = 0.211). Figure 2 shows the SPV in the sagittal plane as a function of retropulsion measured with the SRP. The SRP score differed significantly between recurrent fallers and single or non-fallers (U = 28.500, Z=-2.619, p = 0.008). The median SRP score was 2 (Q1-Q3 0–3) for single or non-fallers and 4 ( 3 – 8 ) for recurrent fallers (> 1 fall within the last 12 months). The SRP also differed significantly for the risk of falling estimated with the Timed-Up and Go test (U = 37.500, Z=-2.916, p = 0.003). Participants with an increased risk of falling had a median SRP score of 4 (Q1-Q3 3–8) while patients with no increased risk of falling had a median score of 2 (0–3). Discussion Characteristics and severity of retropulsion Most of the individuals with Parkinsonian syndromes in our cohort showed retropulsion as measured with the SRP. While the severity of these signs varied widely, reactive postural control was impaired in almost all subjects. When looking at the severity of the PD symptoms, 67% of participants with mild symptoms and all participants with moderate symptoms showed deficient reactive postural control. Impaired reactive postural adjustments after external perturbation are well known in subjects with PD and can be tested with the retropulsion test. 9,21 It represents a key risk factor for frequent falls. 22 Resistance to passive movement in the sagittal plane, which was so far widely neglected in studies about Parkinsonian syndromes, was found in half of our participants. In subjects with severe PD symptoms, it was even present in 90% of cases. Static postural control was rarely affected in subjects with mild or moderate PD symptoms, but 70% of participants with severe symptoms showed signs of retropulsion during static sitting or standing. Similarly, retropulsion was not present in participants with mild symptoms during dynamic tasks, but in 60% of subjects with severe symptoms. Summing up, reactive postural control was affected in almost all subjects with Parkinsonian syndromes, even if PD symptoms were mild. In subjects with moderate PD symptoms, postural deficits additionally involved resistance to passive movement in 38% of cases and deficient static and/or dynamic postural control in 25% of cases. In subjects with severe PD symptoms, resistance and reactive postural control were the main issues, but impairments in static and dynamic postural control were also present in ≥ 60% of subjects. Correlation of retropulsion with functional disability, postural control and fall risk When looking at the correlations of the SRP with Parkinson-specific measures of functional disability, moderate to good correlations with the Hoehn and Yahr staging and the UPDRS III scoring were found. This indicates that more severe PD symptoms are associated with more pronounced retropulsion. Retropulsion not only correlated with functional disability, but also with balance measures. The strong correlation of the SRP score with the score of the Berg Balance Scale indicates that retropulsion is associated with more generic balance impairments. The sway area of the center of pressure during static standing and the limits of stability in the sagittal plane moderately correlated with the SRP score. Since these posturographic measures reflect only parts of the single subtests of the SRP, moderate correlations make sense. The SRP score correlated only in the sagittal plane with the limits of stability but not in the frontal plane, further underlining the construct validity of the SRP. The higher the retropulsion score, the more problems the participants had in shifting their center of gravity in the sagittal plane, while this was not the case in the frontal plane. Our findings support previous studies, which reported impaired ability to lean forwards and backwards in voluntary tasks in subjects with PD. These studies also showed that reduced limits of stability in the anterior-posterior plane occur already in the early stages of PD and further decline with disease progression and/or reduced response to levodopa medication. 12,23 Interestingly, one of these studies revealed that subjects in Hoehn & Yahr stage 2 had a greater decline of their limits of stability in the backward direction than in the forward direction, suggesting that they maintained greater stability in the forward direction than in the backward direction, regardless of the asymmetry of motor signs. 23 When analyzing the ratio between body sway and limits of stability, strong correlations were found for the sagittal and the frontal planes. This implies that subjects with retropulsion have a reduced functional reserve in both planes during static standing. Since they approach their stability limits to a much greater extent they might be exposed to an increased fall risk. A previous study applied direction-specific surface translations to subjects with PD. PD patients had smaller stability margins in all directions compared to healthy controls, but especially for backward sway, suggesting that they are most vulnerable to falling in the backward direction. 24 Retropulsion further correlated moderately with postural verticality perception in the sagittal plane. This means that retropulsion was associated with a backward shifted internal reference of verticality. This is in line with previous studies that found impaired verticality perception in individuals with retropulsion. 25,26 A single case study with a severely affected PD patient reported a normalization of the backward shifted postural vertical after an intensive and specific rehabilitation program. 27 Confirming the construct of retropulsion measured with the SRP, retropulsion did not show a correlation to verticality perception in the frontal plane. Falls are frequent in parkinsonism, but falling rates vary substantially. 28 Our results revealed that recurrent fallers had significantly higher SRP scores than non- or single-fallers. Similarly, subjects with an increased risk of falls according to the Timed-Up and Go test showed severe retropulsion more frequently. An SRP score ≥ 3 seems to be associated with a history of falls in the previous year and with an increased fall risk. It was shown before that a history of falls is a short time predictor for the number of future falls. 4,29 In conclusion, the results of our study reveal that subjects with moderate PD symptoms showed SRP scores ≥ 3. A SRP score ≥ 3 was also associated with recurrent falls within the last twelve months and an increased risk of falling. Most of these subjects show a backward shifted SPV. Subjects with severe PD symptoms had SRP scores ≥ 5, mainly Berg Balance Scale scores lower than 45 and most of them were not able to perform the SPV assessment. In contrast, participants with no or mild retropulsion showed SRP scores ≤ 2, Berg Balance Scale scores above 45 and mainly normal verticality perception. Examination of the different Parkinsonian syndromes Due to the low number of subjects with atypical or secondary Parkinsonian syndromes, the main analyses in this study were done for all subjects together. Nonetheless, some interesting points need to be discussed. All subjects with progressive supranuclear palsy and vascular Parkinsonism included in this study showed signs of retropulsion, which was not the case in the group of PD subjects. Similarly, individuals with progressive supranuclear palsy or vascular Parkinsonism typically show axial signs as well as recurrent falls in early disease stages. 30 In PD by contrast, axial disturbances are not immediately evident, but become more visible in the middle-to-late stages. The overall severity of retropulsion was moderate in subjects with progressive supranuclear palsy and severe in subjects with vascular Parkinsonism. Subjects with progressive supranuclear palsy mainly showed impaired reactive postural control and resistance to passive movement in the sagittal plane. Subjects with vascular Parkinsonism additionally had deficient static postural control. This is in line with previous findings that a broad-based, unsteady stance is an early and sensitive (but non-specific) sign in vascular Parkinsonism. 30 Etiopathogenetic and pathophysiological factors might explain the different findings for the Parkinsonian syndromes. The present study implies that retropulsion is very frequent in subjects with Parkinsonian syndromes. A score ≥ 3 on the SRP may be a relevant cutoff. Individuals with a SRP score ≥ 3 seem to have an impaired reference of verticality with considerable balance impairments and an increased risk of falling. Systematic screening with the SRP might help to identify affected subjects and provide them with the most appropriate treatment and fall prevention. However, it is important to consider that subjects with Parkinsonian syndromes differ across the spectrum of disease severity in their postural motor learning ability and response to different fall prevention intervention 31 . Investigating the subscores of the SRP across the different syndromes and different disease stages might help to characterize postural control deficits of patients at risk of falls and add to the development of treatment approaches. Though the present study was open to all Parkinsonian syndromes, it involved only subjects with PD, progressive supranuclear palsy and vascular Parkinsonism. This and the small sample sizes of the progressive supranuclear palsy and vascular Parkinsonism groups limit the generalizability of the results for Parkinsonian syndromes. Further studies investigating retropulsion in large cohorts of the different syndromes are needed and might help to understand postural control mechanisms in these subjects. So far, there are few postural studies in atypical and secondary Parkinsonian syndromes. In addition, prospective fall assessment across different Parkinsonian syndromes and disease stages might improve the validity of the SRP to detect fall risk. As a new assessment method for postural control and falls in Parkinsonian syndromes, the SRP will be valuable for clinical work and clinical trials. Declarations Acknowledgment The authors thank Katie Göttlinger for language editing. Authors’ Contribution Conceptualization, J.B., C.K, F.M. and K.J.; Methodology, J.B., C.K. and K.J.; Validation, J.B.; Formal Analysis, J.B.; Investigation, J.B. and C.K.; Resources, J.B.; Data Curation, J.B.; Original Draft Preparation, J.B.; Review & Editing, C.K., K.J. and F.M. All authors have approved the final article. Data availability statement The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. Competing interests The authors have no competing interests to declare that are relevant to the content of this article Funding sources This work was supported by funds from the German Federal Ministry of Education and Research [BMBF IFB 01EO1401].The funding source was not involved in the collection, analysis and interpretation of data, in the writing of the report and in the decision to submit the article for publication. Ethical approval and consent This study was approved by the Ethics Committee of the Ludwig-Maximilians-Universität München (number 405-11). Informed written consent was obtained from the participants or their legal representatives. References Williams, D.R., Watt, H.C. & Lees, A.J. Predictors of falls and fractures in bradykinetic rigid syndromes: a retrospective study. J Neurol Neurosurg Psychiatry 77, 468–473 (2006). Lazarotto, L., et al. Static and dynamic postural control: Comparison between community old adults and people with Parkinson's disease. 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Can J Public Health 83 Suppl 2, S7-11 (1992). Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3857208","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":267145324,"identity":"fe8cdb06-2980-4c2f-a7b0-c237ae3c44ac","order_by":0,"name":"Jeannine Bergmann","email":"data:image/png;base64,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","orcid":"","institution":"Schön Klinik Bad Aibling","correspondingAuthor":true,"prefix":"","firstName":"Jeannine","middleName":"","lastName":"Bergmann","suffix":""},{"id":267145326,"identity":"288e1519-f196-4b3d-bd13-c807c6dd5ea2","order_by":1,"name":"Carmen Krewer","email":"","orcid":"","institution":"Schön Klinik Bad Aibling","correspondingAuthor":false,"prefix":"","firstName":"Carmen","middleName":"","lastName":"Krewer","suffix":""},{"id":267145327,"identity":"a32dac24-1f5c-49a5-86cd-a1b5a6ea7eed","order_by":2,"name":"Friedemann Müller","email":"","orcid":"","institution":"Schön Klinik Bad Aibling","correspondingAuthor":false,"prefix":"","firstName":"Friedemann","middleName":"","lastName":"Müller","suffix":""},{"id":267145329,"identity":"6455a646-9397-41a1-b447-0109ebbcab88","order_by":3,"name":"Klaus Jahn","email":"","orcid":"","institution":"Schön Klinik Bad Aibling","correspondingAuthor":false,"prefix":"","firstName":"Klaus","middleName":"","lastName":"Jahn","suffix":""}],"badges":[],"createdAt":"2024-01-12 14:14:11","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3857208/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3857208/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":49776468,"identity":"4271a1ac-8677-4039-853b-470dfb0ada4c","added_by":"auto","created_at":"2024-01-17 21:11:01","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":28715,"visible":true,"origin":"","legend":"\u003cp\u003eScatterplot of the correlation between the Berg Balance Scale and the Scale for Retropulsion. The dotted line represents a Berg Balance Scale score of 45, which implies an increased risk of falling.\u003csup\u003e32\u003c/sup\u003e\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-3857208/v1/2eaeb2012f9624f803fa03c0.png"},{"id":49777132,"identity":"b46eb004-56b2-4890-8291-d065e8b546bb","added_by":"auto","created_at":"2024-01-17 21:19:01","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":29981,"visible":true,"origin":"","legend":"\u003cp\u003eScatterplot of the correlation between the subjective postural vertical in the sagittal plane and the Scale for Retropulsion. The dotted lines represent the ranges of normality of the subjective postural vertical in the sagittal plane.\u003csup\u003e16\u003c/sup\u003e\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-3857208/v1/2fa3686e0a689effd256929f.png"},{"id":51576975,"identity":"fefec4a4-2af1-4eb2-896d-8816f1d5ed79","added_by":"auto","created_at":"2024-02-24 05:45:28","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":345868,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3857208/v1/2cb1943c-bafd-4aab-a104-74c0e28fee9a.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Postural instability in the anterior-posterior plane is associated with impaired postural verticality perception and fall risk in Parkinsonian syndromes","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe Parkinsonian syndromes include idiopathic Parkinon\u0026rsquo;s disease (PD), progressive supranuclear palsy, multiple system atrophy, corticobasal degeneration, vascular Parkinsonism, and some other rare causes of parkinsonism. Besides bradykinesia, which is an essential sign that often leads to a diagnosis of parkinsonism, extrapyramidal rigidity, resting tremor and postural instability are cardinal signs of Parkinsonian syndromes and features of basal ganglia dysfunction. Postural instability is common in advanced PD but may also be an important early sign in other Parkinsonian syndromes.\u003csup\u003e1\u003c/sup\u003e In PD, postural instability becomes more prevalent and worsens with disease progression, but can also be present at an early stage.\u003csup\u003e2,3\u003c/sup\u003e In the advanced stages of the disease, postural instability is one of the most disabling symptoms and is associated with an increased risk of falls.\u003csup\u003e4,5\u003c/sup\u003e Falls and fear of falling are major determinants for poor quality of life, reduced mobility, and physical deconditioning.\u003csup\u003e6,7\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eOne problem is the postural instability in the anterior-posterior plane, also described as retropulsion. As we understand it, retropulsion describes an active posterior displacement of the center of mass with a tendency to fall backwards, problems in shifting the center of mass actively forward, and resistance against passive correction.\u003csup\u003e8\u003c/sup\u003e This behavior may hamper sitting and standing and also the ability to perform functional tasks such as transferring and walking. In addition, it might be associated with an increased risk of falling.\u003c/p\u003e \u003cp\u003eThe retropulsion test (pull test) assesses the subject\u0026rsquo;s postural reaction to a rapid balance perturbation in the backward direction. It is a key component of the neurological examination and widely regarded as the gold standard to evaluate postural instability in subjects with PD.\u003csup\u003e9\u003c/sup\u003e However, this single-item test has only moderate reliability and correlates poorly with objective measures of balance and the number of falls.\u003csup\u003e10,11\u003c/sup\u003e One reason for the poor validity might be that the test captures only a fraction of the postural deficits in PD. Indeed, postural deficits in the sagittal plane can vary and include increased postural sway, reduced postural stability margins, impaired anticipatory postural adjustment, and deficient dynamic balance control.\u003csup\u003e5,12\u003c/sup\u003e Recently, the Scale for Retropulsion (SRP) was designed and evaluated for neurological disorders.\u003csup\u003e8,13\u003c/sup\u003e The scale covers different characteristics of retropulsion such as spontaneous posterior body tilt with the tendency of backward falling, insufficient reactive postural responses, an active backward pushing with resistance against passive correction, and the difficulty of shifting the center of mass actively forward.\u003c/p\u003e \u003cp\u003eWhile subjects with Parkinsonian syndromes show abnormal postural control, the characteristics and the underlying pathology seem to be different.\u003csup\u003e14\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eThe objective of this study was to investigate the different characteristics of retropulsion in individuals with Parkinsonian syndromes and their relation to measures of functional disability associated with parkinsonism, postural control and fall risk.\u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eParticipants\u003c/h2\u003e \u003cp\u003eIndividuals included in the study met the following inclusion criteria: Parkinsonian syndrome according to the United Kingdom Parkinson\u0026rsquo;s Disease Society Brain Bank criteria, age 18 to 90 years, and postural instability. Subjects with orthopaedic hip problems, which limited hip flexion between 70\u0026deg; and 120\u0026deg;, were excluded from the study. Participants were tested when they were in a self-reported \u0026ldquo;on\u0026rdquo; state and felt mobile and comfortable.\u003c/p\u003e \u003cp\u003e This study was approved by the Ethics Committee of the Ludwig-Maximilians-Universit\u0026auml;t M\u0026uuml;nchen (number 405\u0026thinsp;\u0026minus;\u0026thinsp;11). All experiments were performed in accordance with relevant named guidelines and regulations. Informed written consent was obtained from the participants or their legal representatives.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eOutcome measures\u003c/h2\u003e \u003cp\u003eThe SRP is a bedside test and comprises the following four subtests: static postural control, reactive postural control, resistance against correction, and dynamic postural control.\u003csup\u003e8\u003c/sup\u003e All subtests are tested in a sitting and a standing starting position resulting in eight items. Each item is rated on a fourpoint scale from 0 to 3. The total score ranges from 0 (no signs of retropulsion) to 24 (severe retropulsion). The SRP had excellent internal consistency, good to excellent test-retest and interrater reliabilities, and good content and construct validities for subjects with neurological disorders. The German version of the SRP was used.\u003csup\u003e13\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eThe Berg Balance Scale determines balance function during a series of predetermined tasks on a five point scale from 0 to 4.\u003csup\u003e15\u003c/sup\u003e The total score ranges from 0 to 56 with higher scores representing higher balance function.\u003c/p\u003e \u003cp\u003eBody sway and the limits of stability were assessed by using a Kistler force plate (Type 9260AA) and the Mars 3.0 software (Kistler, Winterthur, Switzerland). Body sway was recorded during 30 seconds of static standing with eyes open. The limits of stability were assessed in the anterior-posterior and the medio-lateral directions. The ratio of body sway to limits of stability was calculated as the ratio of the maximum sway amplitude in the anterior-posterior and the medio-lateral directions to the limits of stability in the respective planes.\u003c/p\u003e \u003cp\u003eThe subjective postural vertical (SPV) during standing was determined in the sagittal and frontal planes by using the Spacecurl. The apparatus and the experimental procedure used are described elsewhere.\u003csup\u003e16\u003c/sup\u003e The SPV error was calculated by averaging the six trials per plane. SPV measurements have good test-retest and interrater reliabilities \u003csup\u003e16\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe stages of the Parkinsonian syndromes were determined by the Hoehn and Yahr Staging Scale.\u003csup\u003e17\u003c/sup\u003e The categories described by Goetz et al.\u003csup\u003e18\u003c/sup\u003e were used to classify participants according to the severity of PD symptoms (stages 1 and 2, mild; stage 3, moderate; and stages 4 and 5, severe). The severity of PD was graded by the Unified Parkinson\u0026rsquo;s Disease Rating Scale III Motor part (UPDRS III). The UPDRS was obtained by the treating neurologist and extracted from the electronic patient file.\u003c/p\u003e \u003cp\u003eThe rate of falls was assessed by asking the participants for the number of falls within the last 12 months. Subjects who fell more than once within the last 12 months were classified as recurrent fallers. In addition, the Timed-Up and Go test was performed as an indicator of fall risk (cut-off \u0026ge;\u0026thinsp;11.5 sec. indicating an increased risk).\u003csup\u003e19\u003c/sup\u003e\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eDescriptive statistics were applied to describe clinical characteristics of participants and the results from the SRP testing. Mann-Whitney-U tests were used to compare the SRP score of recurrent fallers with single and non-fallers, as well as to compare the SRP score of participants with an increased risk of falling according to the Timed-Up and Go test with participants with no increased fall risk.\u003c/p\u003e \u003cp\u003eSpearman\u0026rsquo;s rank correlation (r\u003csub\u003eSp\u003c/sub\u003e) was used to determine construct validity of the SRP. The strength of the correlation was interpreted as: i) little or no correlation (r\u003csub\u003eSp\u003c/sub\u003e \u0026lt;0.25), ii) fair correlation (0.25\u0026thinsp;\u0026gt;\u0026thinsp;r\u003csub\u003eSp\u003c/sub\u003e \u0026le;0.50), iii) moderate to good correlation (0.50\u0026thinsp;\u0026gt;\u0026thinsp;r\u003csub\u003eSp\u003c/sub\u003e \u0026le;0.75) and good to excellent (r\u003csub\u003eSp\u003c/sub\u003e \u0026gt;0.75).\u003csup\u003e20\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eStatistical analyses were performed using SPSS version 19. The level of significance was set at p\u0026thinsp;\u0026lt;\u0026thinsp;0.05.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eParticipants\u003c/h2\u003e \u003cp\u003e30 individuals with Parkinsonian syndromes were included in the study (age: 75\u0026thinsp;\u0026plusmn;\u0026thinsp;8 years, sex:13 female). The median UPDRS III score was 33 (Q1-Q3 22\u0026ndash;40), the median Hoehn and Yahr stage 3 (Q1-Q3 2\u0026ndash;4), and the average time since diagnosis was 6\u0026thinsp;\u0026plusmn;\u0026thinsp;5 years. 24 of these individuals were diagnosed with PD (age: 74\u0026thinsp;\u0026plusmn;\u0026thinsp;7 years, sex: 10 female, Hoehn and Yahr: 3 (\u003cspan additionalcitationids=\"CR3\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e), years since diagnosis: 7\u0026thinsp;\u0026plusmn;\u0026thinsp;6), 4 with progressive supranuclear palsy (age: 75\u0026thinsp;\u0026plusmn;\u0026thinsp;10 years, sex: 3 female, Hoehn and Yahr: 3 (2.5\u0026ndash;3.5), years since diagnosis: 5\u0026thinsp;\u0026plusmn;\u0026thinsp;4) and 2 with vascular Parkinsonism (age: 82\u0026thinsp;\u0026plusmn;\u0026thinsp;1 years, sex: 0 female, Hoehn and Yahr: 3.5 (\u003cspan additionalcitationids=\"CR3 CR4\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e), years since diagnosis: 3\u0026thinsp;\u0026plusmn;\u0026thinsp;1). Two patients were not able to perform the posturographic measurements and the SPV assessment due to their severe impairments. The UPDRS III was missing in eight individuals (no documentation in the patient file) and the fall rate was not provided in five participants.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eScale for Retropulsion\u003c/h2\u003e \u003cp\u003eThe median SRP score was 3 (Q1-Q3 1\u0026ndash;5; minimum 0, maximum 17). Of the 30 individuals, 26 (86.7%) showed signs of retropulsion measured with the SRP. When looking at the SRP subtests, 11/30 (36.7%, median 0, Q1-Q3 0\u0026ndash;1) showed signs of retropulsion at the subtest \u0026ldquo;static postural control\u0026rdquo;, 24/30 (80.0%, median 2, Q1-Q3 1\u0026ndash;3) at the subtest \u0026ldquo;reactive postural control\u0026rdquo;, 15/30 (50.0%, median 1, Q1-Q3 0\u0026ndash;1) at the subtest \u0026ldquo;resistance\u0026rdquo;, and 8/30 (26.7%, median 0, Q1-Q3 0\u0026ndash;1) at the subtest \u0026ldquo;dynamic postural control\u0026rdquo;.\u003c/p\u003e \u003cp\u003eAdditionally, SRP scores were analyzed separately for individuals with PD, for individuals with progressive supranuclear palsy, and for individuals with vascular Parkinsonism, as shown in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eTotal SRP score and scores of the different SRP subtests for participants with Parkinson\u0026rsquo;s disease, progressive supranuclear palsy and vascular Parkinsonism\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"13\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c12\" colnum=\"12\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c13\" colnum=\"13\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c5\" namest=\"c2\"\u003e \u003cp\u003eIdiopathic Parkinson\u0026rsquo;s disease (n\u0026thinsp;=\u0026thinsp;24)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c9\" namest=\"c6\"\u003e \u003cp\u003eProgressive supranuclear palsy (n\u0026thinsp;=\u0026thinsp;4)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c13\" namest=\"c10\"\u003e \u003cp\u003eVascular Parkinsonism (n\u0026thinsp;=\u0026thinsp;2)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSRP total score\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e20 (83.3%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u0026ndash;6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e3\u0026ndash;9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e4 (100%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e10\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e5\u0026ndash;15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e5\u0026ndash;15\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e2 (100%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest A\u003c/p\u003e \u003cp\u003eStatic postural control\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e8 (33.3%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e1 (25%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e1\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e1\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e2 (100%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest B\u003c/p\u003e \u003cp\u003eReactive postural control)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e18 (75.0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e2\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e2\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e4 (100%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e1\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e1\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e2 (100%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest C\u003c/p\u003e \u003cp\u003eResistance\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e10 (41.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e1\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e3 (75%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e3\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e3\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e2 (100%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest D\u003c/p\u003e \u003cp\u003eDynamic postural control\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e6 (25.0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e1 (25%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e1 (50%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eWhen classifying the individuals according to the severity categories described by Goetz et al. \u003csup\u003e18\u003c/sup\u003e, the SRP scores significantly differed between these categories (Chi\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;10.379, p\u0026thinsp;=\u0026thinsp;0.006): mild PD symptoms resulted in a median SRP score of 2 (Q1-Q3 0\u0026ndash;3, n\u0026thinsp;=\u0026thinsp;12), moderate symptoms in a median SPR score of 3 (3\u0026ndash;5, n\u0026thinsp;=\u0026thinsp;8), and severe symptoms in a median SRP score of 5 (4\u0026ndash;10, n\u0026thinsp;=\u0026thinsp;10). The results of the different subtests for these three categories can be found in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eTotal SRP score and scores of the different SRP subtests for subjects with mild, moderate and severe Parkinson\u0026rsquo;s disease symptoms according to Hoehn and Yahr staging.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"13\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c10\" colnum=\"10\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c11\" colnum=\"11\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c12\" colnum=\"12\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c13\" colnum=\"13\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c5\" namest=\"c2\"\u003e \u003cp\u003eMild Parkinson\u0026rsquo;s symptoms (n\u0026thinsp;=\u0026thinsp;12)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c9\" namest=\"c6\"\u003e \u003cp\u003eModerate Parkinson\u0026rsquo;s symptoms (n\u0026thinsp;=\u0026thinsp;8)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"4\" nameend=\"c13\" namest=\"c10\"\u003e \u003cp\u003eSevere Parkinson\u0026rsquo;s symptoms (n\u0026thinsp;=\u0026thinsp;10)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003eMedian\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003eQ1-Q3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003eMin-Max\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003eNumber of subjects with signs of retropulsion\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSRP total score\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e8 (66.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e3\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e1\u0026ndash;8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e8 (100%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e4\u0026ndash;10\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e1\u0026ndash;17\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e10 (100%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest A\u003c/p\u003e \u003cp\u003eStatic postural control\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e2 (16.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e2 (25%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e0\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e7 (70%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest B\u003c/p\u003e \u003cp\u003eReactive postural control\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e8 (66.7%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e2\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e1\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e8 (100%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e2\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e8 (80%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest C\u003c/p\u003e \u003cp\u003eResistance\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e3 (25.0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e3 (37.5%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e1\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e0\u0026ndash;4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e9 (90%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSubtest D\u003c/p\u003e \u003cp\u003eDynamic postural control\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0\u0026ndash;0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e0\u0026ndash;0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0 (0.0%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e0\u0026ndash;1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c8\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c9\"\u003e \u003cp\u003e2 (25%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c10\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c11\"\u003e \u003cp\u003e0\u0026ndash;3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c12\"\u003e \u003cp\u003e0\u0026ndash;5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c13\"\u003e \u003cp\u003e6 (60%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eCorrelation with measures for functional disability, postural control and falls\u003c/h2\u003e \u003cp\u003eThe SRP score showed moderate to good correlations with Hoehn and Yahr staging (r\u003csub\u003eSp\u003c/sub\u003e=0.668; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and the UPDRS III scoring (r\u003csub\u003eSp\u003c/sub\u003e=0.582; p\u0026thinsp;=\u0026thinsp;0.005).\u003c/p\u003e \u003cp\u003eThere was a strong correlation of the SRP with the Berg Balance Scale (r\u003csub\u003eSp\u003c/sub\u003e=-0.823; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The SRP score moderately correlated with the sway area of the center of pressure during static standing (r\u003csub\u003eSp\u003c/sub\u003e=0.571; p\u0026thinsp;=\u0026thinsp;0.002). Correlations of the SRP with the limits of stability were fair in the anterior-posterior plane (r\u003csub\u003eSp\u003c/sub\u003e=-0.490; p\u0026thinsp;=\u0026thinsp;0.008) and not significant in the medio-lateral plane (p\u0026thinsp;=\u0026thinsp;0.123). However, good correlations of the SRP score with the ratio body sway to limits of stability in the anterior-posterior plane (r\u003csub\u003eSp\u003c/sub\u003e=0.714; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and in the medio-lateral plane (r\u003csub\u003eSp\u003c/sub\u003e=0.637; p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) were found.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe SRP score significantly correlated with the SPV error in the sagittal plane (r\u003csub\u003eSp\u003c/sub\u003e=-0.499; p\u0026thinsp;=\u0026thinsp;0.007), but not with the SPV in the frontal plane (p\u0026thinsp;=\u0026thinsp;0.211). Figure\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e shows the SPV in the sagittal plane as a function of retropulsion measured with the SRP.\u003c/p\u003e \u003cp\u003eThe SRP score differed significantly between recurrent fallers and single or non-fallers (U\u0026thinsp;=\u0026thinsp;28.500, Z=-2.619, p\u0026thinsp;=\u0026thinsp;0.008). The median SRP score was 2 (Q1-Q3 0\u0026ndash;3) for single or non-fallers and 4 (\u003cspan additionalcitationids=\"CR4 CR5 CR6 CR7\" citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e) for recurrent fallers (\u0026gt;\u0026thinsp;1 fall within the last 12 months).\u003c/p\u003e \u003cp\u003eThe SRP also differed significantly for the risk of falling estimated with the Timed-Up and Go test (U\u0026thinsp;=\u0026thinsp;37.500, Z=-2.916, p\u0026thinsp;=\u0026thinsp;0.003). Participants with an increased risk of falling had a median SRP score of 4 (Q1-Q3 3\u0026ndash;8) while patients with no increased risk of falling had a median score of 2 (0\u0026ndash;3).\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eCharacteristics and severity of retropulsion\u003c/h2\u003e \u003cp\u003eMost of the individuals with Parkinsonian syndromes in our cohort showed retropulsion as measured with the SRP. While the severity of these signs varied widely, reactive postural control was impaired in almost all subjects. When looking at the severity of the PD symptoms, 67% of participants with mild symptoms and all participants with moderate symptoms showed deficient reactive postural control. Impaired reactive postural adjustments after external perturbation are well known in subjects with PD and can be tested with the retropulsion test.\u003csup\u003e9,21\u003c/sup\u003e It represents a key risk factor for frequent falls.\u003csup\u003e22\u003c/sup\u003e Resistance to passive movement in the sagittal plane, which was so far widely neglected in studies about Parkinsonian syndromes, was found in half of our participants. In subjects with severe PD symptoms, it was even present in 90% of cases. Static postural control was rarely affected in subjects with mild or moderate PD symptoms, but 70% of participants with severe symptoms showed signs of retropulsion during static sitting or standing. Similarly, retropulsion was not present in participants with mild symptoms during dynamic tasks, but in 60% of subjects with severe symptoms. Summing up, reactive postural control was affected in almost all subjects with Parkinsonian syndromes, even if PD symptoms were mild. In subjects with moderate PD symptoms, postural deficits additionally involved resistance to passive movement in 38% of cases and deficient static and/or dynamic postural control in 25% of cases. In subjects with severe PD symptoms, resistance and reactive postural control were the main issues, but impairments in static and dynamic postural control were also present in \u0026ge;\u0026thinsp;60% of subjects.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eCorrelation of retropulsion with functional disability, postural control and fall risk\u003c/h2\u003e \u003cp\u003eWhen looking at the correlations of the SRP with Parkinson-specific measures of functional disability, moderate to good correlations with the Hoehn and Yahr staging and the UPDRS III scoring were found. This indicates that more severe PD symptoms are associated with more pronounced retropulsion. Retropulsion not only correlated with functional disability, but also with balance measures. The strong correlation of the SRP score with the score of the Berg Balance Scale indicates that retropulsion is associated with more generic balance impairments. The sway area of the center of pressure during static standing and the limits of stability in the sagittal plane moderately correlated with the SRP score. Since these posturographic measures reflect only parts of the single subtests of the SRP, moderate correlations make sense. The SRP score correlated only in the sagittal plane with the limits of stability but not in the frontal plane, further underlining the construct validity of the SRP. The higher the retropulsion score, the more problems the participants had in shifting their center of gravity in the sagittal plane, while this was not the case in the frontal plane. Our findings support previous studies, which reported impaired ability to lean forwards and backwards in voluntary tasks in subjects with PD. These studies also showed that reduced limits of stability in the anterior-posterior plane occur already in the early stages of PD and further decline with disease progression and/or reduced response to levodopa medication.\u003csup\u003e12,23\u003c/sup\u003e Interestingly, one of these studies revealed that subjects in Hoehn \u0026amp; Yahr stage 2 had a greater decline of their limits of stability in the backward direction than in the forward direction, suggesting that they maintained greater stability in the forward direction than in the backward direction, regardless of the asymmetry of motor signs.\u003csup\u003e23\u003c/sup\u003e When analyzing the ratio between body sway and limits of stability, strong correlations were found for the sagittal and the frontal planes. This implies that subjects with retropulsion have a reduced functional reserve in both planes during static standing. Since they approach their stability limits to a much greater extent they might be exposed to an increased fall risk. A previous study applied direction-specific surface translations to subjects with PD. PD patients had smaller stability margins in all directions compared to healthy controls, but especially for backward sway, suggesting that they are most vulnerable to falling in the backward direction.\u003csup\u003e24\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eRetropulsion further correlated moderately with postural verticality perception in the sagittal plane. This means that retropulsion was associated with a backward shifted internal reference of verticality. This is in line with previous studies that found impaired verticality perception in individuals with retropulsion.\u003csup\u003e25,26\u003c/sup\u003e A single case study with a severely affected PD patient reported a normalization of the backward shifted postural vertical after an intensive and specific rehabilitation program.\u003csup\u003e27\u003c/sup\u003e Confirming the construct of retropulsion measured with the SRP, retropulsion did not show a correlation to verticality perception in the frontal plane.\u003c/p\u003e \u003cp\u003eFalls are frequent in parkinsonism, but falling rates vary substantially.\u003csup\u003e28\u003c/sup\u003e Our results revealed that recurrent fallers had significantly higher SRP scores than non- or single-fallers. Similarly, subjects with an increased risk of falls according to the Timed-Up and Go test showed severe retropulsion more frequently. An SRP score\u0026thinsp;\u0026ge;\u0026thinsp;3 seems to be associated with a history of falls in the previous year and with an increased fall risk. It was shown before that a history of falls is a short time predictor for the number of future falls.\u003csup\u003e4,29\u003c/sup\u003e\u003c/p\u003e \u003cp\u003eIn conclusion, the results of our study reveal that subjects with moderate PD symptoms showed SRP scores\u0026thinsp;\u0026ge;\u0026thinsp;3. A SRP score\u0026thinsp;\u0026ge;\u0026thinsp;3 was also associated with recurrent falls within the last twelve months and an increased risk of falling. Most of these subjects show a backward shifted SPV. Subjects with severe PD symptoms had SRP scores\u0026thinsp;\u0026ge;\u0026thinsp;5, mainly Berg Balance Scale scores lower than 45 and most of them were not able to perform the SPV assessment. In contrast, participants with no or mild retropulsion showed SRP scores\u0026thinsp;\u0026le;\u0026thinsp;2, Berg Balance Scale scores above 45 and mainly normal verticality perception.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eExamination of the different Parkinsonian syndromes\u003c/h2\u003e \u003cp\u003eDue to the low number of subjects with atypical or secondary Parkinsonian syndromes, the main analyses in this study were done for all subjects together. Nonetheless, some interesting points need to be discussed. All subjects with progressive supranuclear palsy and vascular Parkinsonism included in this study showed signs of retropulsion, which was not the case in the group of PD subjects. Similarly, individuals with progressive supranuclear palsy or vascular Parkinsonism typically show axial signs as well as recurrent falls in early disease stages.\u003csup\u003e30\u003c/sup\u003e In PD by contrast, axial disturbances are not immediately evident, but become more visible in the middle-to-late stages. The overall severity of retropulsion was moderate in subjects with progressive supranuclear palsy and severe in subjects with vascular Parkinsonism. Subjects with progressive supranuclear palsy mainly showed impaired reactive postural control and resistance to passive movement in the sagittal plane. Subjects with vascular Parkinsonism additionally had deficient static postural control. This is in line with previous findings that a broad-based, unsteady stance is an early and sensitive (but non-specific) sign in vascular Parkinsonism.\u003csup\u003e30\u003c/sup\u003e Etiopathogenetic and pathophysiological factors might explain the different findings for the Parkinsonian syndromes.\u003c/p\u003e \u003cp\u003eThe present study implies that retropulsion is very frequent in subjects with Parkinsonian syndromes. A score\u0026thinsp;\u0026ge;\u0026thinsp;3 on the SRP may be a relevant cutoff. Individuals with a SRP score\u0026thinsp;\u0026ge;\u0026thinsp;3 seem to have an impaired reference of verticality with considerable balance impairments and an increased risk of falling. Systematic screening with the SRP might help to identify affected subjects and provide them with the most appropriate treatment and fall prevention. However, it is important to consider that subjects with Parkinsonian syndromes differ across the spectrum of disease severity in their postural motor learning ability and response to different fall prevention intervention \u003csup\u003e31\u003c/sup\u003e. Investigating the subscores of the SRP across the different syndromes and different disease stages might help to characterize postural control deficits of patients at risk of falls and add to the development of treatment approaches.\u003c/p\u003e \u003cp\u003eThough the present study was open to all Parkinsonian syndromes, it involved only subjects with PD, progressive supranuclear palsy and vascular Parkinsonism. This and the small sample sizes of the progressive supranuclear palsy and vascular Parkinsonism groups limit the generalizability of the results for Parkinsonian syndromes. Further studies investigating retropulsion in large cohorts of the different syndromes are needed and might help to understand postural control mechanisms in these subjects. So far, there are few postural studies in atypical and secondary Parkinsonian syndromes. In addition, prospective fall assessment across different Parkinsonian syndromes and disease stages might improve the validity of the SRP to detect fall risk. As a new assessment method for postural control and falls in Parkinsonian syndromes, the SRP will be valuable for clinical work and clinical trials.\u003c/p\u003e \u003c/div\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cem\u003eAcknowledgment\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe authors thank Katie G\u0026ouml;ttlinger for language editing.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eAuthors\u0026rsquo; Contribution\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eConceptualization, J.B., C.K, F.M. and K.J.; Methodology, J.B., C.K. and K.J.; Validation, J.B.; Formal Analysis, J.B.; Investigation, J.B. and C.K.; Resources, J.B.; Data Curation, J.B.; Original Draft Preparation, J.B.; Review \u0026amp; Editing, C.K., K.J. and F.M. All authors have approved the final article.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eData availability statement\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eCompeting interests\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no competing interests to declare that are relevant to the content of this article\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eFunding sources\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by funds from the German Federal Ministry of Education and Research [BMBF IFB 01EO1401].The funding source was not involved in the collection, analysis and interpretation of data, in the writing of the report and in the decision to submit the article for publication.\u003c/p\u003e\n\u003cp\u003e\u003cem\u003eEthical approval and consent\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eThis study was approved by the Ethics Committee of the Ludwig-Maximilians-Universit\u0026auml;t M\u0026uuml;nchen (number 405-11). Informed written consent was obtained from the participants or their legal representatives.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eWilliams, D.R., Watt, H.C. \u0026amp; Lees, A.J. Predictors of falls and fractures in bradykinetic rigid syndromes: a retrospective study. J Neurol Neurosurg Psychiatry 77, 468\u0026ndash;473 (2006).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLazarotto, L., \u003cem\u003eet al.\u003c/em\u003e Static and dynamic postural control: Comparison between community old adults and people with Parkinson's disease. Physiother Res Int 25, e1844 (2020).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVoss, T.S., \u003cem\u003eet al.\u003c/em\u003e Fall frequency and risk assessment in early Parkinson's disease. Parkinsonism Relat Disord 18, 837\u0026ndash;841 (2012).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePickering, R.M., \u003cem\u003eet al.\u003c/em\u003e A meta-analysis of six prospective studies of falling in Parkinson's disease. Mov Disord 22, 1892\u0026ndash;1900 (2007).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePark, J.H., Kang, Y.J. \u0026amp; Horak, F.B. What Is Wrong with Balance in Parkinson's Disease? J Mov Disord 8, 109\u0026ndash;114 (2015).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGrimbergen, Y.A., Schrag, A., Mazibrada, G., Borm, G.F. \u0026amp; Bloem, B.R. Impact of falls and fear of falling on health-related quality of life in patients with Parkinson's disease. J Parkinsons Dis 3, 409\u0026ndash;413 (2013).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLanders, M.R. \u0026amp; Nilsson, M.H. A theoretical framework for addressing fear of falling avoidance behavior in Parkinson's disease. Physiother Theory Pract, 1\u0026ndash;17 (2022).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBergmann, J., Krewer, C., Koenig, E., M\u0026uuml;ller, F. \u0026amp; Jahn, K. Devlopment of a clinical scale to assess retropulsion in neurological disorders. Neurol Rehabil 25, 7\u0026ndash;17 (2019).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNonnekes, J., Goselink, R., Weerdesteyn, V. \u0026amp; Bloem, B.R. The retropulsion test: a good evaluation of postural instability in Parkinson's disease? J Parkinsons Dis 5, 43\u0026ndash;47 (2015).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBloem, B.R., Beckley, D.J., van Hilten, B.J. \u0026amp; Roos, R.A. Clinimetrics of postural instability in Parkinson's disease. J Neurol 245, 669\u0026ndash;673 (1998).\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJohnson, L., \u003cem\u003eet al.\u003c/em\u003e Clinical and posturographic correlates of falling in Parkinson's disease. 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Can J Public Health 83 Suppl 2, S7-11 (1992).\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3857208/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3857208/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eRetropulsion is a postural behavior which seems frequent in Parkinsonian syndromes, hampering balance and functional tasks, as well as entailing an increase in the risk of falls. This study aimed to investigate different characteristics of retropulsion and their relation to functional disability, postural control and fall risk.\u003c/p\u003e \u003cp\u003eThirty subjects with Parkinsonian syndromes (75\u0026thinsp;\u0026plusmn;\u0026thinsp;8 years, 13 female, 6\u0026thinsp;\u0026plusmn;\u0026thinsp;5 years since diagnosis, median UPDRS III 33 (Q1-Q3 22\u0026ndash;40), Hoehn and Yahr stage 3 (\u003cspan additionalcitationids=\"CR3\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e)) were assessed with the Scale for Retropulsion (SRP), the Berg Balance Scale, the subjective postural vertical, and diagnostic scales. The number of falls within the last 12 months and fall risk was determined. Results revealed signs of retropulsion in 87% of subjects. The SRP score correlated moderately to well with functional disability and disease severity, and strongly with the Berg Balance Scale. The severity of retropulsion was further associated with a backward shifted verticality perception. The SRP significantly differed between recurrent fallers and single or non-fallers and identified subjects at risk of falling. In summary, retropulsion is very frequent in Parkinsonian syndromes. Subjects with an SRP score\u0026thinsp;\u0026ge;\u0026thinsp;3 have an impaired reference of verticality with considerable balance impairments and an increased risk of falling.\u003c/p\u003e","manuscriptTitle":"Postural instability in the anterior-posterior plane is associated with impaired postural verticality perception and fall risk in Parkinsonian syndromes","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-17 21:10:56","doi":"10.21203/rs.3.rs-3857208/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"9b9178a5-390e-4993-a196-96883475ca4a","owner":[],"postedDate":"January 17th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":28140082,"name":"Health sciences/Neurology/Neurological disorders/Parkinsons disease"},{"id":28140083,"name":"Health sciences/Neurology/Neurological disorders/Neurodegenerative diseases"}],"tags":[],"updatedAt":"2024-02-24T05:45:13+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-17 21:10:56","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3857208","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3857208","identity":"rs-3857208","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}