Abstract
Background
MDS‐UPDRS Severity Levels (SLs), derived from clinician‐ and patient‐rated scales, remain underused to evaluate response to subthalamic deep brain stimulation (STN‐DBS) in patients with Parkinson's disease (PD).
Objectives
To evaluate MDS‐UPDRS SL as markers of STN‐DBS response.
Methods
SLs were categorized as mild, moderate, or severe using established cut‐off points for Parts II, III Off, and IV. Improvement was defined as a decrease in at least one SL. Part III Off improvement was correlated to quality‐of‐life scales and used to predict SL improvement using ROC Curve analysis.
Results
A total of 51 patients (34.1% female, aged 58.9 ± 10.2 years, disease duration 12.3 ± 4.1 years) were evaluated 12 months after surgery. MDS‐UPDRS III Off changes over 30% predicted SL improvements in MDS‐UPDRS II (AUC = 0.83, p = 0.015) and IV (AUC = 0.89, p = 0.001).
Conclusion
Our findings suggest that improvement in MDS‐UPDRS SL are potential markers of STN‐DBS response. With an MDS‐UPDRS part III improvement around 30% predicting SL improvement.
Keywords: deep brain stimulation, MDS‐UPDRS, Parkinson's disease, STN‐DBS, treatment outcome
Deep brain stimulation of the subthalamic nucleus (STN‐DBS) is a well‐established therapeutic option for patients with Parkinson's disease (PD) with motor fluctuations that are not adequately managed with conventional medical treatment. 1 , 2 , 3 While the efficacy of STN‐DBS is widely measured using change in the Movement Disorder Society Unified Parkinson's Disease Rating Scale (MDS‐UPDRS) part III, 4 , 5 , 6 , 7 there is no validated threshold to define an optimal response and the potential extrapolation of a 30% threshold for MDS‐UPDRS Part III to determine response to dopaminergic medication lacks empirical evidence. Furthermore, changes in Part III Off may not correlate to improvement in motor complications or quality‐of‐life, which are primary objectives for STN‐DBS indication. 8 , 9
Severity levels (mild, moderate, and severe) for MDS‐UPDRS parts have been published, correlating with several clinician‐ and patient‐rated scales. 10 However, to our knowledge, they have not been evaluated as an outcome in patients undergoing STN‐DBS. In the present study, we assessed the distribution of MDS‐UPDRS severity levels (parts II, III Off, and IV), and evaluated the impact of STN‐DBS on their improvement. Additionally, we evaluated whether the commonly used percentual improvement on part III Off accurately represents changes in the severity levels of the different MDS‐UPDRS.
Methods
The Institutional Research Board and Ethics Committee evaluated and approved the Protocol. Patients provided written informed consent for surgery and the further use of clinical information for research purposes.
Study Design and Subjects
A consecutive series of patients with PD 11 , 12 undergoing STN‐DBS were prospectively followed up using structured CAPSIT evaluations 13 with baseline and postoperative assessments at 6, 12, and 24 months. To be included in the analysis, patients required stable DBS programming parameters and medication regimes. Patients with periprocedural complications, incomplete follow‐up data, or compassionate DBS were excluded.
Surgical Procedure
Patients were implanted with bilateral STN‐DBS leads and a single pulse generator as detailed in Supplemental Material S1 and described elsewhere. 14
Clinical Assessment
Baseline and follow‐up assessments were carried out by a movement disorders specialist following CAPSIT 13 recommendations, using MDS‐UPDRS 15 parts II, III and IV, with part III scores evaluated in both the Off and On state after an overnight withdrawal of dopaminergic medication followed by 250/25 mg of levodopa‐carbidopa; the Abnormal Involuntary Movement Scale (AIMS) 16 ; the Parkinson's Disease Questionnaire 39‐item (PDQ‐39). 17 Montreal Cognitive Assessment (MoCA), 18 in the On state to evaluate cognition; Beck Depression Inventory II (BDI‐II), 19 Beck Anxiety Inventory (BAI), 20 and the Starkstein Apathy Scale (SAS). 21 MDS‐UPDRS severity levels were defined using the cut‐off points established by Martínez‐Martín et al, for MDS‐UPDRS II: mild ≤12, moderate 13–29, and severe ≥30; MDS‐UPDRS III: mild ≤32, moderate 33–58, and severe (≥59); and MDS‐UPDRS IV: mild ≤4, moderate 5–12 and severe ≥13. 10 SL response to STN‐DBS was defined as the decrease in MDS‐UPDRS SL (eg, change from severe to mild) in parts II, III Off, and IV. Given that patients with mild severity level could not improve further, they were analyzed separately.
Statistical Analysis
Continuous variables are presented using median and interquartile range, categorical variables are presented using frequencies and percentages. Demographic and baseline rating scale scores were compared between groups of SL response using the Kruskal‐Wallis test for continuous variables and the Chi‐square test for categorical variables. The change in administered rating scales after STN‐DBS was evaluated using the Wilcoxon sign‐rank test.
A ROC curve analysis was conducted to determine the optimal cutoff score for percentual improvement of MDS‐UPDRS III Off that accurately represents a change in severity levels of MDS‐UPDRS III, III Off, and IV. For each ROC Curve, patients with mild severity level in the corresponding subscore were excluded. A multiple regression model was developed to predict PDQ‐39 SI response, with changes in MDS‐UPDRS parts III Off, IV, II, LEDD, BDI, and BAI as predictive variables. A p‐value less than 0.05 was considered significant.
Results
We screened 65 patients who underwent STN‐DBS between 2013 and 2021, of which 14 were excluded: 13 due to incomplete follow‐up data (during the initial phase of the Covid‐19 pandemic) and one due to hardware complications (skin erosion and infection that led to electrode removal). Therefore, our analysis included 51 subjects, 16 (34.1%) female, with a median age at DBS surgery of 60.0 (13.0), and a median disease duration of 12.0 (5.0) years. Patients had a median (IQR) of 7.0 (3.0) programming sessions at follow‐up, with monopolar stimulation settings being used in all patients, with median amplitude 1.88 (0.50) mA, pulse width 59 (10) μs, and frequency 130 (0) Hz. The whole group experienced a statistically significant decrease across all administered scales except for cognition and apathy (Table 1).
TABLE 1.
Demographics, baseline and follow‐up evaluations of patients
| Baseline | Follow‐up | Statistical comparison a | Median difference | ||
|---|---|---|---|---|---|
| Median (IQR) | Median (IQR) | Z | p‐value | ||
| Sex, female, n (%) | 16 (34.1) | ‐ | ‐ | ‐ | |
| Age at DBS | 60.0 (13.0) | ‐ | ‐ | ‐ | |
| Disease duration | 12.0 (5.0) | ‐ | ‐ | ‐ | |
| MDS‐UPDRS | |||||
| Part II | 13.0 (7.0) | 8.0 (7.0) | −5.20 | <0.001 | −6.0 |
| Part III Off | 44.0 (14.0) | 24.0 (9.0) | −6.09 | <0.001 | −21.0 |
| Part III On | 21.0 (11.0) | 14.0 (8.5) | −4.38 | <0.001 | −8.0 |
| Levodopa response (%) | 50.0 (21.1) | 42.1 (24.1) | −3.06 | 0.002 | −6.6 |
| Part IV | 7.0 (5.0) | 2.0 (4.0) | −4.50 | <0.001 | −5.0 |
| LEDD (mg/day) | 1520.0 (732.5) | 950.0 (575.0) | −4.95 | <0.001 | −375.0 |
| Global clinical impression | 4.0 (0.0) | 3.0 (0.0) | −5.41 | <0.001 | −1.0 |
| PDQ‐39 | |||||
| Summary index | 26.9 (17.7) | 16.9 (21.2) | −4.49 | <0.001 | −6.5 |
| Mobility | 40.0 (30.0) | 16.0 (32.5) | −4.52 | <0.001 | −15.0 |
| Activities of daily living | 37.5 (20.8) | 16.7 (25.0) | −5.19 | <0.001 | −20.8 |
| Emotional wellbeing | 25.0 (25.0) | 16.7 (20.9) | −2.37 | 0.018 | −4.1 |
| Stigma | 18.8 (37.5) | 6.3 (25.0) | −3.14 | 0.002 | −6.3 |
| Social support | 8.3 (16.7) | 8.2 (16.7) | −0.63 | 0.529 | 0.0 |
| Cognitive status | 18.8 (22.0) | 14.7 (25.0) | −1.05 | 0.292 | −4.1 |
| Communication | 25.0 (25.0) | 23.9 (33.4) | −0.37 | 0.711 | 0.0 |
| Bodily discomfort | 33.3 (33.3) | 16.7 (16.7) | −4.47 | <0.001 | −16.6 |
| MoCA | 26.0 (5.0) | 26.0 (4.0) | −0.56 | 0.574 | 0.0 |
| BDI‐II | 10.0 (8.0) | 7.0 (8.0) | −3.41 | <0.001 | −2.0 |
| BAI | 11.0 (11.0) | 5.0 (6.0) | −4.92 | <0.001 | −4.0 |
| SAS | 10.0 (8.0) | 10.0 (8.0) | −1.05 | 0.293 | 0.0 |
| DBS programming | |||||
| Number of sessions | ‐ | 7.0 (3.0) | ‐ | ‐ | |
| Average amplitude, mA | 1.88 (0.50) | 2.88 (0.52) | −6.03 | <0.001 | 0.9 |
| Average pulse width, μs | 59 (10) | 60 (6) | −4.22 | <0.001 | 0.0 |
| Average frequency, Hz | 130 (0) | 140 (10) | −4.38 | <0.001 | 0.0 |
Note: All values given as median (interquartile range) unless otherwise specified.
Abbreviations: AIMS, Abnormal Involuntary Movements Scale; BAI, Beck Anxiety Inventory; BDI‐II, Beck Depression Inventory II; DBS, deep brain stimulation; GCI, Global Clinical Impression; LEDD, Levodopa Equivalent Daily Dose; MDS‐UPDRS, Movement Disorder Society‐Unified Parkinson's Disease Rating Scale; MoCA, Montreal Cognitive Assessment; PDQ‐39 SI, Parkinson's Disease Questionnaire 39‐Item; SAS, Starkstein Apathy Scale.
Comparison baseline versus follow‐up scores using Wilcoxon signed‐rank test.
MDS‐UPDRS Severity Level Analysis
Baseline and follow‐up distribution of severity levels is shown in Fig. S1. After excluding 5 (9.8%) patients with baseline mild MDS‐UPDRS III Off, we found that 39 (84.8%) patients had improved severity level. In comparison, after excluding nine (17.6%) patients with mild MDS‐UPDRS IV, we found that 31 (73.8%) had improved severity level.
ROC Curve analysis (Fig. 1) assessed the ability of changes in MDS‐UPDRS III Off to predict improvements in MDS‐UPDRS severity levels. For improvement in MDS‐UPDRS III Off severity level, a 30.3% reduction in MDS‐UPDRS III Off yielded very good discrimination ability (AUC = 0.99, 95% CI = 0.96–1.00, p < 0.001; sensitivity 94.9%, specificity 100.0%). For improvement in MDS‐UPDRS IV severity level, a 30.3% reduction in MDS‐UPDRS III Off exhibited very good discrimination ability (AUC = 0.89, 95% CI = 0.78–1.00, p < 0.001; sensitivity 90.3%, specificity 72.7%). For improvement in MDS‐UPDRS II severity level, a 32.0% reduction in MDS‐UPDRS III Off showed fair discrimination ability (AUC = 0.83, 95% CI = 0.62–1.00, p = 0.015; sensitivity 81.8%, specificity 66.7%). Finally, when evaluating simultaneous improvements in all three MDS‐UPDRS II, III Off, and IV severity levels, a 46.8% reduction in MDS‐UPDRS III Off provided moderate discrimination ability (AUC = 0.71, 95%CI = 0.57–0.85; p = 0.015; sensitivity 75.0%, specificity 65.7%).
Figure 1.
ROC curves. Receiver operating characteristic (ROC) curves for prediction of MDS‐UPDRS (II, III Off, IV, and all) severity level improvement based on the percentual change in MDS‐UPDRS III Off.
The multiple regression model statistically significantly predicted the change in PDQ‐39: (F = 9.980, adj. R 2 = 0.42, p < 0.001). However, only MDS‐UPDRS parts III Off and BDI added significantly to the prediction statistically (Table S1).
The individual analysis of the five patients with mild MDS‐UPDRS III Off SL (Table S2) showed a trend towards improvement in MDS‐UPDRS III Off (p = 0.068), decreasing LEDD in four patients, but not in MDS‐UPDRS IV (p = 0.593) or PDQ‐39 SI (p = 0.416).
Discussion
This study represents the first attempt to evaluate the modification of disease severity through the severity levels of MDS UPDRS 10 in patients undergoing STN‐DBS to provide an empirical validation of the percentual modification in MDS‐UPDRS III in the Off state as a marker for optimal surgery response. Our findings show that over 80% of patients improved MDS‐UPDRS III Off SL, and over 70% improved MDS‐UPDRS IV SL following STN‐DBS, highlighting the effectiveness of functional surgery in patients with PD. However, changes in severity levels of the UPDRS III did not predict significant changes in QoL as measured by PDQ‐39.
Furthermore, ROC curve analysis showed that a 30% change from baseline MDS‐UPDRS III Off score predicted improvements in SL of Parts II and IV, with notable sensitivity and specificity for Part IV. Although there were notable improvements in metrics such as MDS‐UPDRS III Off, MDS‐UPDRS IV, and LEDD reduction, our multiple regression model showed that these metrics only explained 23% of the variance in quality of life. This supports the notion that factors other than motor response contribute to modifications in quality of life, as has been previously reported. 8
Although commonly employed, based on the threshold for levodopa responsiveness using a 30% improvement in Part III Off to define optimal response to DBS lacks empirical validation. However, we confirmed that a percentual modification of around 30% (30.3%) best represented an improvement in severity level not only as expected for MDS‐UPDRS part III Off but also for part IV, while changes close to 50% (46.8%) were necessary to predict a change of severity across all three parts of the UPDRS (II, III Off, and IV) simultaneously (Fig. S1).
Evaluating the response to functional surgery is challenging due to the multidimensional aspects of the disease, 22 , 23 with many contributors to patient disability, including motor symptoms in both the OFF and ON state, non‐motor symptoms, and motor fluctuations. 24 , 25 , 26 Until recently, quality of life measurements have not always been the center of evaluation in most of the literature regarding outcomes of DBS. 4 , 5 , 6 , 7 While MDS‐UPDRS III is a valuable tool, our results align with previous studies showing that neither its raw score nor the severity levels derived from it correlate with improvements in quality of life (QoL) measures. Similarly, a recent systematic review of 18 studies of PD patients who received STN‐DBS found that improvements in quality of life were not consistently predicted by demographic features or by PD rating scales, which further supports our findings. 8 , 9
Finally, the individual analysis of the patients with mild MDS‐UPDRS III Off, who were excluded from the general analysis because they could not reduce their severity level, also demonstrated improvements across all scales. This underscores the importance of individualized assessments for defining response to DBS, taking into account the varying baseline severity levels of patients.
Our study is not exempt from limitations. First, we included only the assessment from the 12‐month evaluation, considering that at this time stable programming parameters are usually achieved and there is less risk of bias from disease progression on the effect of STN‐DBS. Second, our approach was focused on MDS‐UPDRS scores, which are only one metric of success after DBS, and future studies focusing on other metrics such as medication reduction are needed. Third, our modest sample size may limit the statistical power of our findings. Larger studies with extended longitudinal follow‐up times are warranted to confirm the potential of MDS‐UPDRS SL improvement as a marker of STN‐DBS success. Our results also highlight the complexity of evaluating the quality of life in patients who have undergone DBS surgery and the need for a multidimensional approach.
Author Roles
(1) Research Project: A. Study conception and design, B. Organization, C. Execution. (2) Statistical Analysis: A. Data acquisition, B. Data analysis and interpretation, C. Review and Critique; (3) Manuscript Preparation: A. Writing of the first draft, B. Review and critique for important intellectual content; (4) Final approval of the version to be submitted.
S.A.C.T.: 1A, 1B, 1C, 2A, 2B, 3A, 4.
I.C.: 1A, 1B, 1C, 2A, 2B, 3A, 4.
M.R.: 1A, 1C, 2C, 3B, 4.
M.W.: 1A, 1C, 2C, 3B, 4.
D.C.: 1A, 1C, 2C, 3B, 4.
M.M.: 1A, 1C, 2C, 3B, 4.
Disclosure
Ethical Compliance Statement: The Protocol was evaluated and approved by Fleni's Institutional Research Board and Ethics Committee. Patients provided written informed consent for surgery and the further use of clinical information for research purposes. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.
Funding Sources and Conflict of Interest: No specific funding was received for this work. The authors declare that there are no conflicts of interest relevant to this work.
Financial Disclosures for the Previous 12 Months: SACT was supported by the Edmond J. Safra Foundation Fellowship in Movement Disorders (Class of 2023) and receives funding as Member of the National Researcher System from Mexico's National Council for Science and Technology (Consejo Nacional de Ciencia y Tecnología, CONACYT). IC is supported by an entry‐level fellowship granted by the Fund for Scientific and Technological Research (Fondo para la Investigación Científica y Tecnológica, FONCYT), Argentina.
Supporting information
Data S1. Surgical procedure details. Details regarding surgical procedure, devices implanted, and post‐surgical management of patients included.
Figure S1. MDS‐UPDRS Severity Level Distribution.
Legend: Bar chart composite showing the baseline and follow‐up distribution for severity levels in MDS‐UPDRS II (upper left), III Off (upper right), and IV (lower left).
TABLE S1. Multiple regression model. B, unstandarized regression coefficient; CI, confidence interval; LL, lower limit; UL, upper limit; SE B, standard error of the coefficient; Beta, standarized coefficient; R 2, coefficient of determination; Adj R 2, adjusted R 2. * p < 0.05, **p < 0.01, ***p < 0.001
TABLE S2. Analysis of mild MDS‐UPDRS III Off SL *Comparison baseline vs follow‐up scores using Wilcoxon signed‐rank test. All values given as median (interquartile range) unless otherwise specified. AIMS, Abnormal Involuntary Movements Scale; BAI, Beck Anxiety Inventory; BDI‐II, Beck Depression Inventory II; DBS, deep brain stimulation; GCI, Global Clinical Impression; LEDD, Levodopa Equivalent Daily Dose; MDS‐UPDRS, Movement Disorder Society‐Unified Parkinson's Disease Rating Scale; MoCA, Montreal Cognitive Assessment; PDQ‐39 SI, Parkinson's Disease Questionnaire 39‐Item; SAS, Starkstein Apathy Scale. **Upon individual analysis, LEDD decreased in all but one patient of this group
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data S1. Surgical procedure details. Details regarding surgical procedure, devices implanted, and post‐surgical management of patients included.
Figure S1. MDS‐UPDRS Severity Level Distribution.
Legend: Bar chart composite showing the baseline and follow‐up distribution for severity levels in MDS‐UPDRS II (upper left), III Off (upper right), and IV (lower left).
TABLE S1. Multiple regression model. B, unstandarized regression coefficient; CI, confidence interval; LL, lower limit; UL, upper limit; SE B, standard error of the coefficient; Beta, standarized coefficient; R 2, coefficient of determination; Adj R 2, adjusted R 2. * p < 0.05, **p < 0.01, ***p < 0.001
TABLE S2. Analysis of mild MDS‐UPDRS III Off SL *Comparison baseline vs follow‐up scores using Wilcoxon signed‐rank test. All values given as median (interquartile range) unless otherwise specified. AIMS, Abnormal Involuntary Movements Scale; BAI, Beck Anxiety Inventory; BDI‐II, Beck Depression Inventory II; DBS, deep brain stimulation; GCI, Global Clinical Impression; LEDD, Levodopa Equivalent Daily Dose; MDS‐UPDRS, Movement Disorder Society‐Unified Parkinson's Disease Rating Scale; MoCA, Montreal Cognitive Assessment; PDQ‐39 SI, Parkinson's Disease Questionnaire 39‐Item; SAS, Starkstein Apathy Scale. **Upon individual analysis, LEDD decreased in all but one patient of this group
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.