Caretaker views on deep brain stimulation for cognitively impaired patients with Parkinson’s disease

Abstract

:

Neuropsychological assessment is crucial in the presurgical evaluation of patients with Parkinson’s disease (PD) who are contemplating deep-brain stimulation (DBS). No standardized screening test battery currently exists. Our movement disorder group most frequently employs the Mattis dementia rating scale (MDRS) and usually advises against DBS for PD patients with MDRS ≤130. We reviewed patient-reported outcomes and satisfaction with DBS in these borderline patients.

Methods:

We retrospectively reviewed a single-center database of 696 DBS patients to identify individuals with PD and an MDRS score ≤130. Telephone interviews were conducted with the patient’s primary caretaker (PCT) to assess long-term satisfaction with the procedure. Electronic medical records were reviewed to analyze patient demographics, preoperative assessments, and surgical complications.

Results:

We identified 19 DBS patients and interviewed 6 PCTs. Five (83%) PCTs reported they were “very satisfied” with long-term DBS outcomes, and one (17%) reported they were “satisfied.” All PCTs reported improved patient quality of life and motor symptoms, would urge their loved one to undergo surgery again, and have recommended DBS surgery to others. Three PCTs reported eventual worsened cognition, while one reported improved cognition.

Conclusion:

A MDRS score ≤130 by itself does not preclude a poor outcome with DBS for PD. A standardized battery of preoperative neuropsychological testing for DBS is needed to establish better evidenced-based “cutoff ” scores and to improve candidate selection.

INTRODUCTION

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is an established therapy for Parkinson’s disease (PD) that has been shown to improve patients’ motor scores and decrease patients’ need for anti-Parkinsonian medication.[16] STN-DBS is most effective in certain PD patients who are identified using a series of inclusion and exclusion criteria.[13] There are contradictory views regarding candidacy for STN-DBS, particularly amongst patients with early dementia or those with preoperative cognitive assessments bordering on cutoff criteria. Here, we describe our findings of patient caregiver surveys to assess how they think STNDBS affected their loved ones.

A patient’s cognition is often measured with the Mattis dementia rating scale (MDRS) to decide if they are a good candidate for STN-DBS.[12] A leading PD work group recommended excluding PD patients with early signs of dementia from STN-DBS due to early evidence of cognitive decline after pallidotomies and a known association of basal ganglia circuitry with memory.[5] In practice, this translates to patients with an MDRS score below 120 or 130 being considered ineligible for STN-DBS and either offered DBS at a different target with possibly less medication reduction or not offered the surgery at all.[14]

Some studies have documented PD patients experiencing more cognitive decline following electrode implantation than in the natural development of PD,[3] but other studies claim the observed postimplantation decline is still within the expected range for PD patients, especially considering the advanced disease state of most STN-DBS candidates.[10] Some groups have even claimed that STN-DBS does not correlate with any significant cognitive decline.[2,8] When specifically looking at patients with low preoperative MDRS scores, some studies have pointed out a lack of the expected benefit, while other groups showed no connection between a low MDRS score and STN-DBS outcomes.[4,6,15,17,19-21] Given the often-contradictory study data, it remains an open question whether PD patients are appropriate surgical candidates when they have low preoperative MDRS scores. We surveyed the primary caretakers (PCTs) of patients receiving bilateral STN-DBS despite an MDRS score ≤130 to assess long-term satisfaction with the procedure and to identify future areas of research.

MATERIALS AND METHODS

This study was deemed exempt by the Allegheny Health Network Institutional Review Board (AHN IRB 2020-283).

We retrospectively reviewed PD patient charts from a single center to identify patients who had a preoperative MDRS score ≤130 and were treated with bilateral STN-DBS from August 01, 1997, to June 30, 2020. PCTs were contacted by telephone during the month of February 2021. Three attempts were made to contact each PCT, and a scripted voicemail message was left for each unsuccessful attempt.

When contacted, PCTs were asked to participate in a 10-question semi-structured interview about the patient’s experiences after DBS surgery and their assessment of the patient’s quality of life, motor symptoms, and cognition. The first question asked PCTs to rate their satisfaction with the overall outcome of the surgery using a 1–5 Likert scale. The next eight questions allowed interviewees to answer “yes,” “no,” or “unsure” in response to the question, accompanied by an open-ended prompt to expand on each response. The final question was open-ended and allowed PCTs to provide any additional comments, concerns, or advice for future patients considering DBS surgery.

The survey results were supplemented with a patient chart review to collect each patient’s preoperative neuropsychiatric and functionality evaluation results, duration of disease, and time from implantation to the survey. Preoperative evaluation results included Hoehn and Yahr stages, Schwab and England activities of daily living scores, and MDRS scores. In the case of deceased patients, the follow-up time was calculated from implantation to date of death.

Descriptive statistics were performed on the surveys utilizing Microsoft Excel Statistical Analysis ToolPak (Redmond, WA). Interview transcripts were also analyzed for themes, and representative quotes were identified with an iterative approach among the co-authors.

RESULTS

We identified 19 patients with a confirmed diagnosis of PD and a preoperative MDRS score ≤130 during the study. Their MDRS scores ranged from 115 to 130, with a mean score of 126. Five of the 19 patients were deceased at the time of the interview. Seven PCTs were successfully contacted, and six agreed to participate in our investigation. Patient characteristics of the six patients are listed in Table 1. Three of the six patients were deceased at the time of the interview. At the time of DBS surgery, the patients had an average age of 66 years old (range: 54–78 years), and 5 (83%) of the patients were male.

Table 1:

Patient (Pt.) demographics and characteristics at date of service and record of years since implant surgery.

During their preoperative evaluation, three patients scored 130 on the MDRS, two scored between 125 and 129, and one scored 120. Their scores ranged from 120 to 130, with an average score of 127 ± 4.1. Half of the patients were at a Hoehn and Yahr stage 3, with two patients at stage 2.5, and one at stage 2. In terms of their Schwab and England activities of daily living scores, four patients scored 70% or higher in functionality. Preoperative symptoms were recorded for four of the patients: Three patients reported tremors, three reported rigidity, one reported gait festination, and one reported freezing. Five patients suffered from mild to moderate depression at the time of implantation. The time between the patients’ DBS surgery and PCT interviews ranged from 3.1 to 14.4 years.

Overall, the PCTs were pleased with the outcome of the surgery; 5 (83%) reported they were “very satisfied” with the long-term outcome, and 1 (17%) reported they were “satisfied.” All 6 PCTs reported improvement in the patient’s quality of life and motor symptoms. They also said that they would urge their loved one to go through surgery again and have recommended DBS surgery to friends considering it. Quantitative results of the survey can be seen in Table 2.

Table 2:

Survey results for the nine structured questions asked of caregivers about how the DBS procedure affected their loved ones.

The PCTs’ perspectives on patient cognition were more nuanced. Four of the 6 PCTs noted changes to the patient’s cognition, largely to the patient’s detriment. One patient, who had the implant for over 5 years, was described as “more aware, and [with a] clearer mind.” However, the other three patients were described by their PCTs as suffering from diminished cognition. Pertinent excerpts from the interviews are listed in Figure 1.

Figure 1:

Primary caretakers’ perspectives regarding patient cognition.

Regarding the patient with an MDRS score of 120, 3.1 years passed between implantation and the interview. Their PCT noted cognitive decline in their loved one at approximately 2.5 years after implantation. However, they cited possible exacerbating factors, such as “mini-strokes.”

DISCUSSION

This study presents the longest follow-up data in the literature for patients with low MDRS scores after undergoing bilateral STN-DBS. Overall, our study suggests that patients with low preoperative MDRS scores see durable benefit from STNDBS according to their PCTs. All PCTs in our study reported high satisfaction with the procedure, improvement in patient quality of life and motor symptoms, said they would urge their loved one to go through with it again, and have since then recommended it to other patients. Approximately half of the PCTs noted cognitive decline in their loved ones at varied times postoperation. However, some cognitive decline is expected, given that the natural history of PD is characterized by a two-fold increase in cognitive impairment in subjects when compared to controls.[1]

Several themes about patient cognition were noted from the interview transcripts. First, PCTs described cognitive decline occurring later in the patient’s disease course (2– 12 years postoperatively). This has strong implications for future study design regarding PD patient cognition and patient outcomes. Studies either must be much larger to have enough power to identify early decline, utilize more sensitive study instruments, or follow patients for longer to get an accurate post-DBS course on this patient population. Second, the patient’s decline was often clouded by other factors. For example, some PCTs pointed out advanced age as a contributing factor, and others noted inciting “mini-strokes” or unrelated orthopedic surgery. Finally, the PCTs often separated audio-visual disturbances, such as hallucinations, from their assessment of the patient’s cognition.

Overall, our patients and PCTs were satisfied with STN-DBS despite the reported cognitive decline in approximately half of the patients in this study. This is in line with other PCT-centered research that surveyed PD patients and their PCTs 8.2 ± 2.6 years post-STN-DBS and demonstrated a high rate of long-term patient/PCT satisfaction.[7] Holistic satisfaction of patients and caregivers must be balanced with possible cognitive decline secondary to STN-DBS.

DBS patients with low MDRS scores are an understudied population, since most movement disorder centers opt not to perform DBS surgery on patients with MDRS scores ≤130.[5] Floden et al. presented a series of 106 patients who underwent STN-DBS, 44 of whom underwent bilateral implantation.[6] In their analysis, MDRS scores did not significantly influence patient quality of life outcomes at 6 months. Furthermore, the group of patients with MDRS scores <130 (24 patients; ten with bilateral stimulation) saw a small increase in their MDRS scores at their postoperative visit.[6] In contrast, Witt et al. conducted a study that included patients with “borderline” MDRS scores (130–137) and found that low-scoring patients failed to demonstrate quality of life improvement.[20]

Existing literature has not investigated MDRS scores as a predictive factor for STN-DBS outcomes; however, there have been studies attempting to quantify the cognitive changes in patients after intervention. There have been varied reports of cognitive decline after STN-DBS, with some groups reporting no change in MDRS scores postoperatively and others reporting cognitive decline, though not out of proportion to the known natural progression of PD.[2,8] Notably, Aybek et al. found that a third of their patients developed dementia 6 months after STN-DBS, suggesting a possible relationship between the surgery and their cognitive decline.[3] However, Gruber et al. reported that DBS surgery was associated with a 1.6 point per year decline in MDRS scores postoperatively and does not impart a disease-modifying effect on cognition.[10] Other groups have noted cognitive decline out of proportion to natural history, for example, Smeding et al. reported that 36% of their cohort showed cognitive decline compared to the medically managed group.[18]

Determining the true relationship of STN-DBS on cognitive outcomes is increasingly challenging due to the heterogeneity of patients and diversity of cognitive baselines. This study arrives at conflicting conclusions due to a small sample size as well. Moreover, the MDRS itself has been subject to growing criticisms based on its susceptibility to confounding by education level. In addition, patients with advanced PD have been shown to score worse on neuropsychiatric tests, even in the absence of dementia or depression.[7,9]

Limitations

One limitation of our investigation is the lack of postoperative MDRS scores for the patients in this study. We postulate that our cohort’s postoperative MDRS scores may decrease, given the current understanding of STN-DBS and PD, as many of the PCTs in our study noted an eventual cognitive decline. We believe that PCTs’’ cognition assessments corresponded with formal assessments for conditions such as Alzheimer’s disease, insofar as their accounts of cognitive decline in our patient population may serve as a proxy for significant declines in MDRS scores.[11] Our study is also limited by inherent long-term recall bias.

CONCLUSION

This study has the longest follow-up published in the literature for PD patients with low MDRS scores who underwent bilateral STN-DBS. Furthermore, it suggests that this surgical procedure can still be highly beneficial for patients up to 14 years postoperatively with low cognitive reserve. Further investigation is needed to confirm the long-term benefits of DBS in this population and to determine whether the MDRS remains the gold standard for preoperative psychometric evaluation.

Ethical approval:

Institutional Review Board approval is not required as it is a retrospective study.

Declaration of patient consent:

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given consent for clinical information to be reported in the journal. The patient understands that the patient’s names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript, and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.