Balance and gait disturbances and quality of life in patients with idiopathic parkinson's disease and progressive supranuclear palsy

Hatice Eraslan Boz; Aycem Öztürk Kiriş; Koray Koçoğlu; Berril Dönmez Çolakoğlu; Raif Çakmur; Gülden Akdal

doi:10.4103/nsn.nsn_148_20

ORIGINAL ARTICLE

Year : 2021 | Volume : 38 | Issue : 1 | Page : 45-49

Balance and gait disturbances and quality of life in patients with idiopathic parkinson's disease and progressive supranuclear palsy

Hatice Eraslan Boz¹, Aycem Öztürk Kiriş², Koray Koçoğlu², Berril Dönmez Çolakoğlu³, Raif Çakmur³, Gülden Akdal⁴
¹ Department of Neurology, Unit of Neuropsychology; Department of Neurosciences, Institute of Health Sciences, Izmir, Turkey
² Department of Neurosciences, Institute of Health Sciences, Izmir, Turkey
³ Department of Neurology, Unit of Neuropsychology; Department of Neurosciences, Institute of Health Sciences; Department of Neurology, Dokuz Eylul University, Izmir, Turkey
⁴ Department of Neurosciences, Institute of Health Sciences; Department of Neurology, Dokuz Eylul University, Izmir, Turkey

Date of Submission	23-Aug-2020
Date of Decision	11-Oct-2020
Date of Acceptance	24-Oct-2020
Date of Web Publication	26-Mar-2021

Correspondence Address:
Gülden Akdal
Department of Neurology, Dokuz Eylül University, Mithatpasa St, 1606, Narlıdere, Izmir
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/nsn.nsn_148_20

Abstract

Objective: The objective of this study is to compare the balance, gait, and quality of life of patients with idiopathic Parkinson's disease (PD), progressive supranuclear palsy (PSP), and healthy controls (HCs). Materials and Methods: The present study included 26 patients with PD, 14 patients with PSP, and 22 HCs. The Berg Balance Scale (BBS), Dynamic Gait Index (DGI), and the Turkish version of Mini-Mental State Examination (MMSE) were administered to all participants. The Parkinson 's disease questionnaire (PDQ-39) and Unified PD Rating Scale were evaluated only among patients with PD and PSP. Results: There was a significant difference between PD and PSP in terms of BBS, DGI, and all variables of PDQ-39 except “social support” (P < 0.05). Although a significant difference was found between patients with PSP and HCs in the BBS and DGI, there was no significant difference between patients with PD and HCs in the DGI and BBS. Further, the BBS and DGI were strongly correlated regarding the “mobility” and “activities of daily living” variables of the PDQ-39 and moderately correlated in terms of “total scores of PDQ-39,” “stigma,” and “communication” subscores. The MMSE was moderately associated with “total scores of PDQ-39” and the “mobility” subscore. Conclusion: This study demonstrated a significant deterioration in balance, gait, and the quality of life in patients with PSP compared with PD and HCs. However, there was no difference between patients with PD and HCs.

Keywords: Balance, gait, idiopathic Parkinson's disease, progressive supranuclear palsy, quality of life

How to cite this article:
Boz HE, Kiriş A&, Koçoğlu K, Çolakoğlu BD, Çakmur R, Akdal G. Balance and gait disturbances and quality of life in patients with idiopathic parkinson's disease and progressive supranuclear palsy. Neurol Sci Neurophysiol 2021;38:45-9

How to cite this URL:
Boz HE, Kiriş A&, Koçoğlu K, Çolakoğlu BD, Çakmur R, Akdal G. Balance and gait disturbances and quality of life in patients with idiopathic parkinson's disease and progressive supranuclear palsy. Neurol Sci Neurophysiol [serial online] 2021 [cited 2023 Mar 22];38:45-9. Available from: http://www.nsnjournal.org/text.asp?2021/38/1/45/311965

Introduction

As a clinical syndrome with symptoms such as rigidity, rest tremor, and gait problems, the most common subtype of parkinsonism is Parkinson's disease (PD), and progressive supranuclear palsy (PSP) is one of the secondary causes of less common parkinsonism.^[1] In PD, clinical features including gait disturbances, postural instability, and disease duration, and demographic factors such as age are reported to be significantly associated with loss of balance and falls.^[2] It is stated that there may be a fall risk of over 60% in patients with PD and over 80% in those with PSP.^[3],[4],[5] The abrupt and impetuous nature of gait in PSP is associated with impaired frontal functions.^[6] Detecting and monitoring gait and balance disorders in PD and PSP are very important in predicting the risk of falling, determining life changes, and guiding caregivers.

In addition to the main symptoms of the disease in patients with PD and PSP, features such as anxiety and cognitive impairment cause a decrease in the quality of life of patients.^{[1],[7],[8],[9],[10],[11],[12]} The diversity of symptoms in PD and PSP cause patients to be dependent on caregivers in their daily life activities and decrease their quality of life.^[11],[12]

It is very important to distinguish these two diseases from each other in terms of diagnosis, treatment, and rehabilitation because PD and PSP have similar clinical manifestations in the early stages.^[13] There are studies examining balance, gait disturbances,^[14] falls, and quality of life PD and PSP separately;^{[12],[15],[16]} however, as far as we know, no studies have examined these features together in both groups. In this study, we aimed to investigate the relation of quality of life with balance and gait disturbances in patients with PD and PSP.

Materials and Methods

Participants

The present study included 26 patients with idiopathic PD, 14 patients with PSP, and 22 healthy controls (HCs). The participants were recruited between September 2015 and January 2016 from the movement disorders outpatient clinic of Dokuz Eylul University Hospital, Department of Neurology. All participants had a complete physical and neurologic examination. The patients with probable PSP were selected according to the criteria of the National Institute of Neurological Disorders and Stroke and the Society for PSP,^[17] and the patients with PD were selected according to the United Kingdom PD Society Brain Bank clinical criteria for Idiopathic PD.^[18]

The HC group consisted of people with no neurologic and psychiatric disease. All participants were given the Berg Balance Scale (BBS), Dynamic Gait Index (DGI), and the Turkish version of Mini-Mental State Examination (MMSE);^[19] only patients with PSP and PD were administered the Unified Parkinson's Disease Rating Scale (UPDRS) and the Parkinson's Disease questionnaire-39 (PDQ-39).

The Ethics Committee of Dokuz Eylul University approved the study, and all participants were given informed consent.

Balance, gait, and quality of life assessments

The UPDRS assesses disease-specific impairment. In this study, the motor examination of UPDRS Part III, whose scores range from 0 to 92, was evaluated. High scores in this assessment indicate motor difficulties.^[20]

The PDQ-39 is a 5-point Likert-type scale that assesses disease-related changes in daily living activities. The highest score on this scale is 156, which indicates a better quality of life.^[21],[22]

The BBS evaluates static-dynamic balance ability with 14 items representing daily activities on a scale from 0 to 4. The maximum score is 56 points.^[23],[24]

The DGI evaluates gait instability and the risk of falling, the best possible score is 24.^[25]

Statistical analysis

All variables were analyzed using the IBM® SPSS® Statistics 22.0 program (Armonk, NY: IBM Corp., USA). The normality of data distribution was tested using the Kolmogorov–Smirnov test. The Mann–Whitney U-test was used to compare gait, balance, and quality of life scores of the PD and PSP groups. The Kruskal–Wallis test was performed to examine the differences between patient groups and controls. Kruskal–Wallis post hoc Dunn analysis for continuous variables and Chi-square post hoc analysis for categorical variables were used for the pairwise comparisons of groups. The relationship between quality of life and balance and gait scores in the patient groups was analyzed using the Spearman's correlation analysis. Significance level was set at P < 0.05 for all analyses.

Results

There was no significant difference between patients with PD and PSP and HCs in terms of age (P = 0.066), education (P = 0.058), sex (P = 0.691), and the MMSE (P = 0.066). In addition, there was no significant difference between patients with PD and PSP in the UPDRS (P = 0.824) and duration of disease (P = 0.416). These results are presented in [Table 1].

Table 1: Clinical and demographical features

Click here to view

According to post hoc tests, there were significant differences between patients with PD and PSP in the BBS (adjusted P = 0.002) and DGI (adjusted P = 0.004) and between patients with PSP and HCs in the BBS (P < 0.001) and DGI (P < 0.001). No significant difference was found between patients with PD and HCs in terms of the BBS and DGI. However, the mean DGI score of patients with PSP (13.9 ± 7.2) showed a risk of falling [Table 2].

Table 2: Balance and gait scores

Click here to view

There were significant differences between patients with PD and PSP in the total score of PDQ-39 (P < 0.001) and mobility (P < 0.001), activities of daily living (P < 0.001), emotional well-being (P = 0.008), stigma (P < 0.001), cognitive impairment (P = 0.012), communication (P = 0.001), and bodily discomfort (P = 0.002) subscores of the PDQ-39. No significant difference was found between the groups in the social support (P = 0.076) subscore of the PDQ-39. The mean and standard deviations of PDQ-39 in the patient groups are presented in [Table 3].

Table 3: The scores of the Parkinsonfs disease questionnaire-39 scale

Click here to view

There were negative strong correlations between the BBS and mobility subscores of PDQ-39 (r = −0.635, P < 0.001), and activities of daily living subscores of PDQ-39 (r = −0.655, P < 0.001), and between the DGI and mobility subscores of PDQ-39 (r = −0.647, P < 0.001), and activities of daily living subscores of PDQ-39 (r = −0.640, P < 0.001). In addition, there were negative moderate correlations between the DGI and total scores of PDQ-39 (r = −0.573, P < 0.001), stigma (r = −0.431, P = 0.006), and communication (r = −0.545, P < 0.001). Further, there were negative moderate correlations between the BBS and total scores of PDQ-39 (r = −0.545, P < 0.001), stigma (r = −0.413, P = 0.009), and communication (r = −0.414, P = 0.009). Moreover, there were negative moderate correlations between the MMSE and the total score of PDQ-39 (r = −0.481, P < 0.001) and mobility (r = −0.549, P < 0.001). The correlation results are presented in [Table 4].

Table 4: Correlations between Parkinsonfs Disease Questionnaire-39 and scores of balance and gait on Parkinsonfs disease and progressive supranuclear palsy

Click here to view

Discussion

Our study demonstrated that patients with PSP had more difficulties in balance and gait compared with patients with PD and HCs. In addition, the risk of falling according to the DGI in patients with PSP was significantly higher than in those with PD and HCs (P < 0.001). Moreover, quality of life in patients with PSP was significantly affected compared with PD. Balance and gait changes were significantly associated with quality of life in patients with PD and PSP (P < 0.05). Although balance and gait disturbances are known in the later stage of PSP in the literature,^[1],[14] the patients with PSP in this study were in relatively early stages.

Many scales are used in clinical settings that evaluate balance and gait dysfunctions. DGI is suggested for use as a reliable objective scale in clinical practice.^[25] In this study, patients with PSP reported that they experienced falls more compared with those with PD and HCs in terms of the DGI. Patients with PD and HCs were similar in terms of balance, gait, and risk of falling [Table 2]. It is emphasized that the same clinical symptoms will not be seen together in every patient, and nonmotor symptoms may be seen earlier than others in PD.^[26],[27] In this study, because PD subtypes were not determined, patients with PD may not be differentiated in terms of balance, gait, and falling from HCs.

In our study, there was no difference in terms of duration of disease in patients with PD and PSP; there may be more balance and gait disturbances in the later stages because PSP has a faster progression.^[6] Motor causes such as weakness, plasticity, axial rigidity, and nonmotor symptoms such as abnormal vertical eye movement, convergence difficulties, and cognitive impairment in PSP are reported to contribute to gait abnormalities.^[28],[29] Our findings are consistent with the fact that balance, gait disturbances, and falls may occur in both PSP and PD.

It was observed that the quality of life of patients with PSP was significantly affected in total score and all subscores except for social support of the PDQ-39 compared with patients with PD [Table 3]. It has been stated that the duration and severity of the disease and severe cognitive impairment contribute negatively to the quality of life in PSP.^[10],[12] Similarly, similar determinants affect the quality of life in PD.^[15] These results seem consistent with our findings. Barone et al.^[30] suggested that the PDQ-39 was one of the best tools for assessing the quality of life in patients with PD, with strong features such as retest reliability, internal consistency, and content validity.^[31] A significant decrease in the health-related quality of life scale (HRQoL) was shown in patients with PSP compared with HCs. In the HRQoL, it was reported that the physical composite scores were affected more than the mental composite scores in patients with PSP.^[12] Moreover, in a 1-year follow-up study of patients with PSP, a significant reduction in quality of life was reported, particularly in physical functionality, social functionality, and vitality subscores.^[32] Considering that physical symptoms significantly reduce the quality of life in patients with PSP, it may decrease the burden of patients and caregivers if physicians address these symptoms with priority.

In the current study, all variables of the PDQ-39 except for the cognitive impairment subscore were found to be significantly associated with gait and balance scores and global cognitive status in patients with PD and PSP. In addition, the cognitive impairment subscore of the PDQ-39 was significantly correlated with the severity of disease in patients with PD and PSP in the current study [Table 4]. As shown in many studies, it is known that factors such as gait and balance difficulties, disease severity, depression, and dementia are related to quality of life in patients with PD and PSP.^{[10],[11],[12],[16]} Therefore, our results are consistent with these findings. Although it is stated in the literature that the duration and severity of the disease is one of the determinants of quality of life,^[15] no relationship was found between disease severity and quality of life in the current study. This may be related to the similarity of the PD and PSP groups in the duration and severity of the disease. Similar to the literature,^[33] a significant relationship was found between the MMSE and quality of life in our study.

Some unexplored factors that may affect the quality of life of patients prevent the generalization of the results of the study. Furthermore, the frequency of falls was recorded, but the characteristics of the falls were not considered.

Conclusion

The present study revealed that balance, gait disturbances, and marked quality of life were significantly affected in patients with PSP compared with those with PD. These results may contribute to the planning of treatment and rehabilitation and monitoring of PSP.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1.	Keener AM, Bordelon YM. Parkinsonism. Semin Neurol 2016;36:330-4.
2.	Sveinbjornsdottir S. The clinical symptoms of Parkinson's disease. J Neurochem 2016;139 Suppl 1:318-24.
3.	Wood BH, Bilclough JA, Bowron A, Walker RW. Incidence and prediction of falls in Parkinson's disease: A prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 2002;72:721-5.
4.	Stolze H, Klebe S, Zechlin C, Baecker C, Friege L, Deushl G. Falls infrequent neurological diseases: Prevalence, risk factors and aetiology. J Neurol 2004;251:79-84.
5.	Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L, et al. Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson's syndrome and PSP-parkinsonism. Brain 2005;128:1247-58.
6.	Golbe LI. Progressive supranuclear palsy. Semin Neurol 2014;34:151-9.
7.	Chen H, Burton EA, Webster RG, Huang X, Savica R, Abbott RD, et al. Research on the premotor symptoms of Parkinson's disease: Clinical and etiological implications. A review. Environ Health Perspect 2016;121:11-2.
8.	Pont-Sunyer C, Hotter A, Gaig C, Seppi K, Compta Y, Katzenschlager R, et al. The onset of nonmotor symptoms in Parkinson's disease (the ONSET PD study). Mov Disord 2015;30:229-37.
9.	Schrag A, Sheikh S, Quinn NP, Lees AJ, Selai C, Mathias C, et al. A comparison of depression, anxiety, and health status in patients with progressive supranuclear palsy and multiple system atrophy. Mov Disord 2010;25:1077-81.
10.	Winter Y, Spottke AE, Stamelou M, Cabanel N, Eggert K, Höglinger GU, et al. Health-related quality of life in multiple system atrophy and progressive supranuclear palsy. Neurodegener Dis 2011;8:438-46.
11.	Rahman S, Griffin HJ, Quinn NP, Jahanshahi M. Quality of life in Parkinson's disease: The relative importance of the symptoms. Mov Disord 2008;23:1428-34.
12.	Schrag A, Selai C, Davis J, Lees AJ, Jahanshahi M, Quinn N. Health-related quality of life in patients with progressive supranuclear palsy. Mov Disord 2003;18:1464-9.
13.	Olanow CW, Stern MB, Sethi K. The scientific and clinical basis for the treatment of Parkinson's disease. J Neurol 2009;72:1-136.
14.	Egerton T, Williams DR, Iansek R. Comparison of gait in progressive supranuclear palsy, Parkinson's disease and healthy older adults. BMC Neurol 2012;12:116.
15.	Soh SE, Morris ME, McGinley JL. Determinants of health-related quality of life in Parkinson's disease: A systematic review. Parkinsonism Relat Disord 2011;17:1-9.
16.	Rajiah K, Maharajan MK, Yeen SJ, Lew S. Quality of life and caregivers' burden of Parkinson's disease. Neuroepidemiology 2017;48:131-7.
17.	Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): Report of the NINDS-SPSP international workshop. Neurology 1996;47:1-9.
18.	Gibb WR, Lees AJ. The relevance of the Lewy body to the pathogenesis of idiopathic Parkison's disease. J Neurol Neurosurg Psychiatry 1988;51:745-52.
19.	Keskinoglu P, Ucku R, Yener G, Yaka E, Kurt P, Tunca Z. Reliability and validity of revised Turkish version of Mini Mental State Examination (rMMSE-T) in community-dwelling educated and uneducated elderly. Int J Geriatr Psychiatry 2009;24:1242-50.
20.	Fahn S, Elton RL. Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale. In: Fahn S, Marsden CD, Calne D, Holstein N, editors. Recent Developments in Parkinson's Disease. New Jersey: Macmillian Healthcare Information; 1987. p. 153-63.
21.	Peto V, Jenkinson C, Fitzpatrick R, Greenhall R. The development and validation of a short measure of functioning and well being for individuals with Parkinson's disease. Qual Life Res 1995;4:241-8.
22.	Dereli EE, Yaliman A, Kuru Çolaka T, Çakmak A, Razak Özdinçler A, Badilli Demirbaş Ş. Turkish version study of “Parkinson's disease quality of life questionnaire” (PDQL). Noro Psikiyatr Ars 2015;52:128-32.
23.	Berg K. Measuring balance in the elderly: Preliminary development of an instrument. Physiother Can 1989;41:304-11.
24.	Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: Validation of an instrument. Can J Public Health 1992;83 Suppl 2:S7-11.
25.	Shumway-Cook A, Woollacott M. Motor Control: Theory and Practical Applications. Baltimore: Williams & Wilkins Press; 1995.
26.	Lawton M, Baig F, Rolinski M, Ruffman C, Nithi K, May MT, et al. Parkinson's Disease subtypes in the oxford Parkinson Disease Centre (OPDC) discovery cohort. J Parkinsons Dis 2015;5:269-79.
27.	van Rooden SM, Colas F, Martínez-Martín P, Visser M, Verbaan D, Marinus J, et al. Clinical subtypes of Parkinson's disease. Mov Disord 2011;26:51-8.
28.	Lubarsky M, Juncos JL. Progressive supranuclear palsy: A current review. Neurologist 2008;14:79-88.
29.	Di Fabio RP, Zampieri C, Tuite P. Gaze control and foot kinematics during stair climbing: Characteristics leading to fall risk in progressive supranuclear palsy. Phys Ther 2008;88:240-50.
30.	Barone P, Erro R, Picillo M. Quality of life and nonmotor symptoms in Parkinson's disease. Int Rev Neurobiol 2017;133:499-516.
31.	Bloem BR, Marinus J, Almeida Q, Dibble L, Nieuwboer A, Post B, et al. Measurement instruments to assess posture, gait, and balance in Parkinson's disease: Critique and recommendations. Mov Disord 2016;31:1342-55.
32.	Pekmezović T, JeĐmenica-Lukić M, Petrović I, Špica V, Tomić A, Kostić VS. Quality of life in patients with progressive supranuclear palsy: One-year follow-up. J Neurol 2015;262:2042-8.
33.	Duncan GW, Khoo TK, Yarnall AJ, O'Brien JT, Coleman SY, Brooks DJ, et al. Health-related quality of life in early Parkinson's disease: The impact of nonmotor symptoms. Mov Disord 2014;29:195-202.