Submitted:
13 December 2023
Posted:
14 December 2023
You are already at the latest version
Abstract
Background: Parkinsons’s disease is characterized by progressive worsening of gait, posture and
balance with disability in daily life activities and to improvement in chronic musculoskeletal pain,
often in neck pain associated with worsening of balance. The aim of the study is to investigate the
correlation between scoliosis, balance and cervical pain in Parkinson’s disease.
Methods: Cross-sectional, pilot study. A total of 16 Parkinson’s patients were enrolled in the study.
The Pain Visual analogue scale and the short form McGill pain questionnaire measured neck cervical pain; static balance, Tinetti, Berg Balance and Short Physical Performance Battery scales(SPPB) were used to evaluate dynamic balance. Whole-spine standard X-ray assess spinal scoliosis with Cobb angles measurement .An observational statistical analysis was performed with the patients subdivided into a non-scoliosis (NS) group and a true scoliosis (TS) group based on whether they presented a Cobb’s angle below or ≥10°.
Results: Frequency of neck pain in the NS group was 37% compared to 50% in the TS group. A non-statistically significant
difference was found in terms of static, dynamic balance and cervical pain scores between NS and
TS groups.
Conclusions: Scoliosis, cervical pain and postural imbalance are significant yet often overlooked
complaints in PD.
Keywords:
Parkinson’s disease
; scoliosis
; postural imbalance
; pain
1. Introduction
Parkinsons’s disease (PD) is a chronic neurodegenerative disorder characterized by progressive worsening of gait, posture and balance. Abnormal postures and spinal misalignment tend to reduce dexterity, disrupt gait, and interfere with daily life activities also increasing the susceptibility to musculoskeletal pain or discomfort [1]. This becomes particularly evident in more advanced stages of the disease where striking sagittal or coronal plane spinal deviations occur (e.g., anterocollis, scoliosis, camptocormia and Pisa syndrome) and are further worsened by the process of aging [2]. Behind the origin of these clinical signs some authors suggest several peripheral (e.g., muscle rigidity, myopathy and soft tissue changes) and central causes (e.g., proprioceptive disintegration, dystonia and medication effects). However, the precise mechanism remains unclear [3]. Spinal scoliosis is a common disorder in PD with a reported prevalence between 43% and 90% [4]. Several experiments of artificially induced hemiparkinsonism on animal models have been showing to induce scoliosis, suggesting the possibility that this condition may have a neurologic background in some cases [1]. It is largely known that spinal regions are not independent of one another, and that the alteration of one segment can have repercussion on the other segments [5]. A study of Topalis and colleagues [6] found a higher prevalence of neck pain in adults with idiopathic scoliosis. Shin et al. [7] has shown that neck pain is associated with excessive cervical lordosis, upper thoracic kyphosis and altered shoulder and scapular kinematic in young women with forward head posture [7]. In addition to spinal deformities, individuals with chronic pain were shown to display balance impairment in multiple studies [8,9].
Despite the significant functional and quality of life impact of cervical pain and the vulnerability of these patients to develop spinal deformities and postural instability, so far, very little attention has been paid in the assessment of the relationship between these factors. Therefore, in this study, we aimed to investigate whether a correlation between scoliosis, poor static and dynamic balance, and cervical pain exists in a group of patients affected by PD. To our knowledge no previous study has been published that investigated this kind of relationship.
2. Materials and Methods
For this pilot, cross-sectional study, 16 consecutive patients with idiopathic PD that presented a scoliotic posture were recruited from the Physical and Rehabilitation outpatient clinic of the Agostino Gemelli University Hospital of Rome between May and October 2022. Part of these patients has been included in our previous study [10]. The present study complies with the STROBE guidelines.
2.1. Eligibility Criteria
The inclusion criteria were a diagnosis of PD according to the criteria of the Brain Bank of London; Hoehn and Yahr stage II-III; absence of cognitive impairment (MMSE> 24/30); effective pharmacological control of the pathology; acceptance and signature of informed consent.
The exclusion criteria comprised: a diagnosis of atypical Parkinsonism; presence of a clinically diagnosed Pisa syndrome, poor pharmacological compensation of the disease; diagnosis of other neurological, neuromuscular diseases or osteo-articular pathologies; visual impairment or vestibular disorders.
2.2. Clinical Evaluation
2.2.1. Medical Examination
Patients that met the inclusion criteria underwent a medical examination during which anamnestic data were collected regarding the age, weight, height, Body Mass Index (BMI), disease duration and current PD treatment including daily dose of Levodopa. All the patients were examined in the morning during the “ON” pharmacological phase.
2.2.2. Radiographic Evaluation
Each patient underwent a standard whole-spine X-ray in two planes (antero-posterior and lateral) in orthostatism. A senior radiologist evaluated the radiological images for the presence of spinal scoliosis and other deformities. To avoid misinterpretation with Pisa syndrome, which is a reversible lateral bending of the trunk, scoliosis was defined as the presence of a radiographic Cobb’s angle of at least 10° on the coronal plane, with or without vertebral rotation, that is not corrected by passive movement or supine position [3]. The curve was classified according to the location of its apex (most lateral vertebra) and its extremities (most peripheral upper and lower vertebrae), the direction of the convexity (right or left) and the curvature range (broad or narrow). The presence of other pathological findings in the coronal (e.g., compensation curve) or sagittal plane (e.g., kyphosis, lordosis, listhesis, etc.) was also reported when present.
2.2.3. Stabilometric Evaluation
Static balance was assessed through a standardized stabilometric exam performed on a 'Prokin PK 254 P' device produced by TecnoBody Srl. (Dalmine, BG, Italy). The device consists of a static platform (47 cm in circumference) with four piezoelectric sensors positioned at the extremities of the four cardinal points. The temporal resolution was 0.01 seconds, and the sampling frequency was set at 20 Hz. The patients were asked to stand on the platform for 60 seconds in a neutral position with the feet forming a 30-degree angle. The test was carried out 30 seconds with the eyes open and 30 seconds with the eyes closed. All data were analysed using ProKin 36 software to calculate the centre of pressure (CoP) sway on the X (anterior-posterior) and Y (medio-lateral) axes (mm), the CoP velocity on the X (anterior-posterior) and Y (medio-lateral) axes (mm/s), the sway path perimeter (mm), and the area of the ellipse (mm2). Lower values reflect greater control in maintaining static balance. We considered as primary outcome the reduction of the length of adaptive movements of the following variables:
- -
- SwayAP and SwayML (mm): standard deviation of CoP time series along the anterior-posterior and medio-lateral axes;
- -
- VelocityAP and VelocityML (mm/s): velocity of oscillations along the anterior-posterior and medio-lateral axes;
- -
- Perimeter (mm): total length of CoP trajectory;
- -
- Area (mm2): area of the 95 % confidence ellipse [11].
- -
- RombergArea: ratio between the value of the area with the eyes closed and with the eyes open.
2.3. Dynamic Balance
Dynamic balance was evaluated using the Tinetti, the Berg Balance scale (BBS) and the Short Physical Performance Battery (SPPB).
- -
- The Tinetti scale is a 16-item standardized screening modality for gait and balance disorders in elderly patients and patients with PD. The scoring system ranges from 0 to 28. The higher the score, the lower the risk of falls [12].
- -
- The BBS is a 14-item scale used to test patients with balance problems, validated in PD. The score ranges from 0 to 56 and does not include gait assessment. The lower the score, the greater the risk of falling [13].
- -
- The SPPB is used to assess functional mobility in elderly patients or individuals affected by neurological diseases. It includes 3 subsets (walking, sit-to-stand and balance). The score ranges from 0 to 12; the lower the score, the lower the functional ability [14].
The study was carried out according to the Declaration of Helsinki and the protocol was approved by the Ethics Committee of the Policlinico Gemelli Foundation (UCSC prot. N 5492/14, 05.03.2014). All patients provided their informed consent prior to inclusion in the study.
2.4. Statistical Analysis
Per-protocol analysis was carried on. Statistical analyses were performed using Statistic Package for Social Sciences (SPSS) version 25.0. Data for categorial variables were expressed as absolute numbers and percentage and the Fisher exact or Pearson's chi-square tests were used to compare them. Continuous variables were expressed as mean, standard deviation (SD) and minimum and maximum value, due to the small sample size. These data were compared using the Mann-Whitney U test. The Pearson correlation coefficient was used to explore the associations between continuous variables. Linear and logistic regression model analysis were performed to provide an adjusted assessment of factors potentially associated with the presence of scoliosis in patients with PD.
3. Results
A total of 16 patients affected by PD were assessed for presence of scoliosis (8 males and 8 females). Half of them met the criteria for scoliosis [3] and were classified as the “true scoliosis” group (TS); the other half presented a Cobb’s angle of less than 10° and were defined as the “non-scoliosis” group (NS). Table 1 summarizes the clinical and demographic characteristics of the patients. Besides the proportion of males and females, there was no statistically significant difference between groups in all the examined variables.
The NS group presented a thoracic spinal deviation below the cutoff angle for diagnosing scoliosis. In one case we found a significant dorsal kyphosis (55°) and in another case a grade I retrolisthesis of T2 over L2.
In the TS group, except for one patient who presented a severe scoliosis (50.15°), all the other patients presented a mild form scoliosis with a Cobb’s angle ≤ 20°. In most cases the curvature was lumbar and broad range. Other spinal abnormalities observed included one case of listhesis and two cases of vertebral fracture. Details about the radiological characteristics of the patients are displayed.
Static balance evaluation did not show a statistically significant difference between the TS group and the NS group, in all the stabilometric parameters examined. Likewise, dynamic balance evaluation did not show a statistically significant difference in both the SPPB, Tinetti and the Berg Balance scales between groups (Table 2).
The study of the Pearson coefficient and linear regression models did not show any association between the Cobb’s angle and the Tinetti scale, SPPB, BBS or other stabilometric parameters (Table 3).
Patients with scoliosis showed a lower variability of the perimeter but a higher variability of the area at the Romberg index compared to the SA group.
Frequency of neck pain revealed a prevalence of 37% in the NS group compared to 50% in the TS group. However, a non-statistically significant difference in cervical pain severity was observed between groups in both the VAS and in the McGill scores (Table 1). Subgroup analysis showed that subjects with a disease duration less than 48 months had a higher prevalence of neck pain compared to those with a disease duration longer than 48 months (n=6; 75.0% vs n= 1; 12.5%; P-value >0.05).
The study of the Pearson coefficient and linear regression models showed no association between cervical pain and the Tinetti, SPPB and BBS or other stabilometric parameters (Table 1).
Furthermore, patients with neck pain showed a lower variability of the Romberg index (both area and perimeter) than patients without neck pain.
4. Discussion
Postural deformities including scoliosis tend to occur more often in PD than in the general elderly population [2,15]. Scoliosis and abnormal posture can produce any type of joint pain and exacerbate the overall sensory impairment and the risk of falls in PD [15]. Static and dynamic balance normally rely on the sound integration of visual, vestibular, and proprioceptive sensory information within the basal ganglia and on a coordinated reflex and motor activity [16]. Many studies have demonstrated that patients with PD have subnormal integration of peripheral sensory stimuli with greater reliance on the visual input during static and dynamic motor tasks [3,16]. Furthermore, the development of balance problems and falls is typically indicative of disease progression and worse prognosis [17]. In our study, static and dynamic balance evaluation did not reveal significant differences between the TS and the NS group.
The regression models highlighted that the demographic and clinical characteristics of the patients can significantly influence the dynamic balance assessment questionnaires, but this evidence does not translate into worse stabilometric data in those who had a greater Cobb angle. This could indicate that scoliosis, neck pain and postural imbalance do not have a linear association between them. The severity of PD and the severity of scoliosis are able to influence dynamic imbalance and risk of falling, but this association still needs to be further studied to identify whether the two conditions together determine an increased risk compared to these two risk factors considered individually.
The literature does not provide any data regarding a possible correlation between scoliosis and balance problems in PD so that the only comparison can be done with individuals with idiopathic scoliosis and no PD. In this regard, previous studies have shown a significant correlation between scoliosis and static imbalance in adolescents with moderate idiopathic scoliosis compared to the healthy controls [18,19]. Furthermore, patients with high major curves had a better postural stability than those with low major curves [20]. Regarding the correlation between scoliosis and dynamic imbalance, compared to healthy controls, Shirado et al. [21] found a significant lower weight’s shift in the patients with idiopathic scoliosis during both slow and fast side-shifts. Furthermore, weight’s shift was less on the concave side than on the convex one. Another study by Haber et al. [22] suggests that scoliotic subjects have a slower speed of gait due to a shorter stride length and a longer stride time. Moreover, they display variations in the timing of muscle activation. Also in this case, to the best of our knowledge, no study investigated the correlation between scoliosis and walking problems in PD. This correlation should be further explored in future studies.
Literature data on neck pain prevalence are currently insufficient both in PD patients and in individuals with idiopathic scoliosis. The study of Kim et al. [23] is the only one reporting a prevalence of neck pain of 5.5% in a cohort of 400 patients with PD, while the study of Topalis et al. [6] is the only one reporting a prevalence of cervical pain of 42% in adults with idiopathic scoliosis. In our study the prevalence of cervical pain was of 50% in PD patients with scoliosis and 37% in those without scoliosis. Regarding the severity of cervical pain, the average VAS and McGill score was tendentially higher in the TS group compared to the NS group. However, this data did not reach a statistical significance. In contrast, subgroup analysis stratified by disease duration showed that individuals with a disease duration >48 months seem to experience less cervical pain compared to patients with more recent onset of the disease. This data is in contrast with the study of Silverdale et al. [24] in which disease duration was not found to influence pain severity in a cohort of 1957 participants with early/moderate PD. Regarding the correlation between neck pain and balance problems, subjects with neck pain did not reveal any difference in dynamic and static balance parameters compared to those without it. Like for scoliosis and neck pain, also in this case we did not find any literature data that investigated this kind of relationship in PD patients. However, if we look at the general population, a study of Ruhe et al. [8] suggests that individuals with neck pain display diminished proprioception and impaired postural control.
Limitations of the Study
This study has a few limitations that should be noted. First, the small sample size and the lack of a control group without PD limit the power of our observation. Second, we performed the clinical assessment at the “ON” phase which could have masked the real level of functional disability and pain of the patients. Third, we did not assess the duration of cervical pain in the group of patients who reported it which could have been useful to make further correlations with balance impairment.
5. Conclusions
Scoliosis, cervical pain and postural imbalance are significant yet often overlooked complaints of PD. Early detection and accurate screening could minimize potential pain and suffering and increase the quality of life. Our results did not show a clear correlation between scoliosis, cervical pain, and static and dynamic imbalance in PD. However, disease duration <48 months seems to be a risk factor for cervical pain. Given the limitations of our study and the paucity of the literature on this subject, further studies are needed to clarify these preliminary findings.
Funding
This study was supported and funded by the Italian Ministry of Health-Ricerca corrente. The founders had no role in study design, data collection and analysis, publication decision, or manuscript preparation.
Institutional Review Board Statement
The study was carried out according to the Declaration of Helsinki and the protocol was approved by the Ethics Committee of the Policlinico Gemelli Foundation (UCSC prot. N 5492/14, 05.03.2014).
Informed Consent Statement
All patients provided written informed consent prior to inclusion in the study.
Data Availability Statement
Not applicable.
Conflicts of Interest
The authors declare no conflict of interest.
Consent for publication
All patients provided written informed consent for publication prior to inclusion in the study.
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Table 1.
Clinical and demographic characteristics of the patients and evaluation of cervical pain.
| Non-Scoliosis (N = 8; 50%) Mean ± SD (min–max) |
True Scoliosis (N = 8; 50%) Mean ± SD (min–max) |
P Value | |
|---|---|---|---|
| Sex (male/female) | 6/2 | 2/6 | 0.13 a |
| Age (years) | 70.63 ± 10.20 (55 – 82) |
70.25 ± 10.87 (53 – 81) |
0.94 b |
| BMI (kg/m2) | 26.00 ± 2.90 (23 – 31) |
25.16 ± 3.75 (21 – 32) |
0.62 b |
| Length of disease (months) | 66.00 ± 32.14 (20 – 112) |
76.00 ± 75.26 (28 – 232) |
0.75 b |
| UPDRS score | 20.25 ± 6.20 (9 – 28) | 24.43 ± 13.39 (9 – 44) |
0.47 b |
| H & Y classification | 1.69 ± 0.26 (1.50 – 2.00) |
1.929 ± 0.70 (1.50 – 3.00) |
0.36 b |
| LEDD (mg/day) | 456.25 ± 247.04 (100 – 800) |
450.00 ± 386.22 (0 – 1000) |
0.97 b |
| Number of drugs | 2.38 ± 1.06 (1 – 4) |
2.14 ± 1.06 (1 – 4) |
0.68 b |
| VAS cervical | 2.50 ± 3.50 (0 – 8) |
3.75 ± 4.02 (0 – 8) |
0.52b |
| McGill cervical | 6.88 ± 9.70 (0 – 21) |
8.88 ± 10.43 (0 – 26) |
0.69b |
Abbreviations: BMI – Body Mass Index; UPDRS – Unified Parkinson’s Disease Rating Scale; MMS – Mini Mental Status; UPDRS- Unified Parkinson’s Disease Rating Scale; LEDD – Levodopa Equivalent Daily Dose. a Fischer Test; b T-student Test.
Table 2.
Clinical evaluation of static and dynamic balance.
| Non-Scoliosis (N = 8) Mean ± SD (min - max) |
True Scoliosis (N = 8) Mean ± SD (min - max) |
P Value | |
|---|---|---|---|
| SPPB Equilibrium | 3.13 ± 0.64 (2 – 4) |
3.00 ± 1.00 (2 – 4) |
0.78b |
| SPPB Gait | 4.00 ± 0.00 (4 – 4) |
3.43 ± 0.78 (2 – 4) |
0.10b |
| SPPB Sit-to-stand | 3.13 ± 0.64 (2 – 4) |
2.43 ± 1.51 (0 – 4) |
0.29b |
| SPPB Total | 10.25 ± 1.03 (9 – 12) |
8.86 ± 3.02 (5 – 12) |
0.28b |
| Tinetti | 24.13 ± 1.12 (22 – 26) |
21.14 ± 4.18 (12 – 24) |
0.11b |
| BBS | 47.00 ± 1.60 (45 – 50) |
45.29 ± 5.09 (37 – 52) |
0.42b |
| Eyes Open | |||
| Sway AP (mm) | 3.13 ± 1.24 (1 – 4) |
3.50 ± 1.60 (2 – 6) |
0.61b |
| Sway ML (mm) | 2.38 ± 1.50 (1 – 6) |
3.00 ± 1.77 (1 – 7) |
0.46b |
| Velocity AP (mm/s) | 9.25 ± 5.82 (3 – 18) |
7.38 ± 2.82 (4 – 13) |
0.43b |
| Velocity ML (mm/s) | 5.25 ± 1.75 (3 – 7) |
4.87 ± 1.53 (3 – 7) |
0.65b |
| Perimeter (mm) | 279.88 ± 143.61 (114 – 496) |
237.50 ± 74.91 (158 – 387) |
0.45b |
| Area (mm2) | 145.75 ± 108.42 (32 – 383) |
183.25 ± 150.85 (59 – 490) |
0.58b |
| Eyes Closed | |||
| Sway AP (mm) | 5.25 ± 2.60 (1 – 10) |
5.50 ± 1.69 (4 – 8) |
0.82b |
| Sway ML (mm) | 3.25 ± 1.83 (2 – 7) |
3.38 ± 1.68 (1 – 6) |
0.89b |
| Velocity AP (mm/s) | 26.25 ± 28.68 (5 – 94) |
17.38 ± 10.48 (7 – 37) |
0.43b |
| Velocity ML (mm/s) | 9.62 ± 7.02 (4 – 26) |
9.13 ± 4.97 (4 – 20) |
0.87b |
| Perimeter (mm) | 705.38 ± 723.49 (153 – 2411) |
509.50 ± 287.25 (196 – 963) |
0.49b |
| Area (mm2) | 393.88 ± 433.23 (44 – 1400) |
334.75 ± 194.49 (81 – 580) |
0.73b |
| Romberg (EC/EO) | |||
| Perimeter (mm) | 2.25 ± 1.24 (1.34 – 4.97) |
2.05 ± 0.83 (1.21 – 3.93) |
0.73 b |
| Area (mm2) | 2.75 ± 2.75 (1.34 – 9.52) |
2.24 ± 1.44 (1.01 – 5.34) |
0.65 b |
b T-student Test.
Table 3.
Association between Cobb’s angle and the Tinetti scale, SPPB, BBS or other stabilometric parameters.
Table 3.
Association between Cobb’s angle and the Tinetti scale, SPPB, BBS or other stabilometric parameters.
| Cobb’s Angle | Univariate Models 1 |
Multivariate Models 2 |
||||
|---|---|---|---|---|---|---|
| UnstandardizedB Coefficients | P-Value | R Squarea | UnstandardizedB Coefficients | P-Value | R Square b | |
| SPPB Total | -0.39 ± 1.69 | 0.82 | 0.01 | -0.51 ± 2.21 | 0.82 | 0.56 |
| Tinetti | -0.49 ± 1.16 | 0.68 | 0.02 | 0.17 ± 3.15 | 0.96 | 0.52 |
| BBS | -0.79 ± 0.94 | 0.42 | 0.05 | -0.03 ± 1.10 | 0.98 | 0.55 |
| Perimeter (EC/EO) | 4.68 ± 2.93 | 0.13 | 0.15 | 4.84 ± 2.97 | 0.15 | 0.69 |
| Area (EC/EO) | 1.55 ± 1.47 | 0.31 | 0.07 | 1.27 ± 1.68 | 0.48 | 0.59 |
1 Unadjusted model; 2 Adjusted model for age, sex, disease duration, BMI; LEDD (mg/day) and VAS score; a R Square for univariate models; b R Square for multivariate models.
Table 4.
Association between cervical pain and the Tinetti scale, SPPB, Berg balance or other stabilometric parameters.
Table 4.
Association between cervical pain and the Tinetti scale, SPPB, Berg balance or other stabilometric parameters.
| VAS score | Univariate Models 1 |
Multivariate Models 2 |
||||
|---|---|---|---|---|---|---|
| Unstandardized B Coefficients |
P-Value | R Square a | Unstandardized B Coefficients |
P-Value | R Square b | |
| SPPB Total | 0.36 ± 0.43 | 0.43 | 0.05 | 0.25 ± 0.70 | 0.73 | 0.40 |
| Tinetti | 0.25 ± 0.29 | 0.41 | 0.05 | 0.94 ± 0.83 | 0.30 | 0.50 |
| Berg Balance | 0.15 ± 0.27 | 0.59 | 0.02 | 0.19 ± 0.33 | 0.60 | 0.42 |
| Perimeter (EC/EO) | -1.08 ± 0.92 | 0.26 | 0.09 | -0.71 ± 1.30 | 0.60 | 0.42 |
| Area (EC/EO) | -0.49 ± 0.44 | 0.28 | 0.08 | -0.39 ± 0.54 | 0.50 | 0.44 |
| Mc Gill score |
Univariate Models 1 |
Multivariate Models 2 |
||||
| Unstandardized B Coefficients |
P-Value | R Square a | Unstandardized B Coefficients |
P-Value | R Square b | |
| SPPBTotal | 1.11 ± 1.22 | 0.38 | 0.06 | 0.49 ± 2.01 | 0.81 | 0.42 |
| Tinetti | 0.72 ± 0.84 | 0.41 | 0.05 | 2.34 ± 2.44 | 0.37 | 0.49 |
| Berg Balance | 0.48 ± 0.76 | 0.54 | 0.03 | 0.45 ± 0.96 | 0.66 | 0.43 |
| Perimeter (EC/EO) | -2.78 ± 2.43 | 0.27 | 0.09 | -2.62 ± 3.68 | 0.50 | 0.46 |
| Area (EC/EO) | -1.31 ± 1.17 | 0.28 | 0.08 | -1.26 ± 1.53 | 0.44 | 0.47 |
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