Deep brain stimulation for Parkinson's disease: A case for patient empowerment

Abstract

•Patient involved in identifying a dual-frequency DBS program to support Parkinson's symptoms.•DBS manufacturers encouraged to ensure all DBS systems enable patients to readily view DBS settings.•Clinicians encouraged to give more consideration to speech in the context of programming DBS for Parkinson's disease. I am a 52-year-old right-handed man, diagnosed with Parkinson's disease aged 40 years. In early 2020, my levodopa equivalent daily dose (LEDD) of 1375 mg comprised levodopa/carbidopa/entacapone, pramipexole, amantadine and selegiline; daytime levodopa frequency was 2–3 hourly. Unfortunately, medication was no longer adequately controlling my symptoms, with breakthrough bradykinesia, gait disturbance, impaired verbal fluency and dyskinesia. My Unified Parkinson's Disease Rating Scale (UPDRS)-III scores were 40 (medication-off) and 8 (medication-on). In May 2020, I underwent bilateral subthalamic nucleus deep brain stimulation (STN-DBS) surgery (Vercise Gevia™ with Cartesia™ directional leads; Boston Scientific, Valencia, CA). Medication was substantially reduced pre-operatively and DBS was activated the day after surgery. During the first month post-surgery, multiple DBS settings were explored: monopolar configurations utilizing different combinations of electrode contacts, with frequencies ≥100 Hz (primarily 130 Hz), pulse width 60 μs, and current ≤ 4 mA. Although STN-DBS can be an effective treatment for Parkinson's disease motor symptoms, speech and gait difficulties may prove refractory [[1]Coleman R.R. Ostrem J.L. When to consider deep brain stimulation for patient with Parkinson's disease, essential tremor, or dystonia.in: Marks Jr., W.J. Deep brain stimulation management. second ed. Cambridge University Press, 2015: 5-30Crossref Scopus (1) Google Scholar,[2]Aldridge D. Theodoros D. Angwin A. Vogel A.P. Speech outcomes in Parkinson's disease after subthalamic nucleus deep brain stimulation: a systematic review.Park Relat Disord. 2016; 33: 3-11https://doi.org/10.1016/j.parkreldis.2016.09.022Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar]. These difficulties were evident post-operatively in my case, with right-sided freezing of gait (FoG) and dysarthria causing me severe difficulty relative to pre-DBS. For the first time, I required the use of a wheelchair to mobilize within my local hospital. Of even greater concern, my wife reported major deterioration in my speech. My speech was partially improved by ceasing levodopa, but family and friends indicated it was still much worse than pre-DBS. To help identify a path forward, I commenced reading material on DBS programming. After reading Su et al. and Xie et al. [[3]Su D. Chen H. Hu W. Liu Y. Wang Z. Wang X. et al.Frequency-dependent effects of subthalamic deep brain stimulation on motor symptoms in Parkinson's disease: a meta-analysis of controlled trials.Sci Rep. 2018; 814456https://doi.org/10.1038/s41598-018-32161-3Crossref Scopus (34) Google Scholar,[4]Xie T. Padmanaban M. Bloom L. MacCracken E. Bertacchi B. Dachman A. et al.Effect of low versus high frequency stimulation on freezing of gait and other axial symptoms in Parkinson patients with bilateral STN DBS: a mini-review.Transl Neurodegener. 2017; 6: 13https://doi.org/10.1186/s40035-017-0083-7Crossref PubMed Scopus (44) Google Scholar], I wrote to my treating neurologist suggesting we try a DBS frequency of 60 Hz to address my difficulties with axial symptoms (McAuley MD, personal communication, June 1, 2020). One-month post-surgery, a 60 Hz-based program was implemented, utilizing the mid-tiers of both electrodes at current 5.5 mA and pulse width 60 μs. Within minutes, my wife noticed improvement in my speech clarity and breadth of vocabulary. My speech post-surgery was assessed by a speech pathologist (Dr. John E. Pierce, La Trobe University), who reported: “Speech recordings two weeks and three months post-surgery [at DBS frequencies >60 Hz] demonstrated mild to moderately-severe articulatory imprecision, as well as mild hypophonia with breathy voice quality; intelligibility was significantly affected. By contrast, speech recordings six months post-surgery [at a DBS frequency of 60 Hz] demonstrated no or mild articulatory imprecision with occasional, mild hypophonia and normal voice quality; intelligibility was significantly improved despite an increase in articulation rate (+0.7 syllables per second after pause removal during reading tasks). Overall, hypokinetic dysarthria had significantly improved, most notably in articulation and intelligibility.” This 60 Hz program supported my speech along with multiple other Parkinson's disease symptoms but did not address my debilitating FoG. In another letter to my treating neurologist (McAuley MD, personal communication, August 7, 2020), I queried whether use of the most ventral electrode contacts would address FoG, as reported by Koeglsperger et al. [[5]Koeglsperger T. Palleis C. Hell F. Mehrkens J.H. Bötzel K. Deep brain stimulation programming for movement disorders: current concepts and evidence-based strategies.Front Neurol. 2019; 10: 410https://doi.org/10.3389/fneur.2019.00410Crossref PubMed Scopus (83) Google Scholar]. My neurologist activated the tip of the left-STN and we tried different combinations of frequency, pulse width and strength of current. Four months post-surgery, a dual-frequency program involving 60 Hz to the mid-tiers of each electrode and 179 Hz to the most ventral left-STN contact was implemented; this resulted in improved gait in addition to supporting my speech and other Parkinson's symptoms. DBS program changes took several hours to fully impact my gait and speech. Between clinical reviews, I used the patient programmer to adjust the DBS current and recorded the impact on my movements and speech using a video camera, together with a smartwatch for step count. This approach enabled me to refine this dual-frequency program by adjusting the strength of current at the left-STN tip. The final program (Fig. 1) has remained unchanged since December 2020, when my UPDRS-III score was 2 with stimulation-on plus pramipexole, selegiline and amantadine (450 mg LEDD). Twelve months post-surgery, FoG was still problematic. Levodopa was reintroduced, which improved gait but impaired my speech. Therefore, after 4 weeks, I requested to cease levodopa. My daily dose of pramipexole was then increased from 1.5 to 2.25 mg, which assisted my gait and did not cause speech problems. Fifteen months post-surgery, my UPDRS-III score was 3 with stimulation-on, combined with pramipexole and amantadine (425 mg LEDD). Two-and-a-half years post-surgery, I can think and speak clearly, as measured by my ability to continue working in a high-level role; pre-DBS, I was preparing to retire due to ill health. FoG still causes me difficulty. An individual's ability to understand their clinician's management plan can help to attain a positive outcome. I feel this axiom is especially relevant to DBS, given the uncertainties associated with the choice of device settings [[6]de Oliveira Goderio Jr., C. Moro E. Montgomery Jr., E.B. Programming: general aspects.in: Temel Y. Fundamentals and clinics of deep brain stimulation. first ed. Springer, 2020: 93-126Crossref Google Scholar]. I understand the therapeutic impact of DBS frequency is particularly poorly understood; however, advances in neuroimaging may guide optimization of frequency in clinical care [[7]DiMarzio M. Madhavan R. Hancu I. Fiveland E. Prusik J. Joel S. et al.Use of functional MRI to assess effects of deep brain stimulation frequency changes on brain activation in Parkinson disease.Neurosurgery. 2021; 88: 356-365https://doi.org/10.1093/neuros/nyaa397Crossref PubMed Scopus (10) Google Scholar]. The DBS system I received does not enable me to view the program settings that define the electrical pulses being sent to my brain; this design is intrinsically disempowering for patients and limits the ability of a patient to understand their DBS management plan. Manufacturers of DBS devices should ensure all their devices enable DBS recipients to read the current (or voltage), pulse width and frequency, per active electrode contact. My personal experience indicates that speech difficulties appear to receive limited attention during DBS programming. Clear speech is incredibly important to me, and I needed to continually emphasize this priority to my treating clinicians. Clinicians should consider how effectively they address the impact of DBS programming on speech when it is a priority for their patient. This may include working in partnership with patients who seek to measure and report on the severity and impact of their Parkinson's symptoms in daily life. My experience with DBS motivated me to discuss DBS programming with others who have undergone DBS surgery. I also note Merner et al. report that patients' desire to control their own DBS programming declined over time in an observational study from pre-DBS to six months post-DBS surgery [[8]Merner A.R. Frazier T. Ford P.J. Cooper S.E. Machado A. Lapin B. et al.Changes in patients' desired control of their deep brain stimulation and subjective global control over the course of deep brain stimulation.Front Hum Neurosci. 2021; 15642195https://doi.org/10.3389/fnhum.2021.642195Crossref PubMed Scopus (1) Google Scholar]. Personally, I relate to Merner and colleagues’ theme of “shared control”; that is, I want to report my symptoms, make suggestions, and have an expert team adjust the DBS settings accordingly. Ultimately, clinicians have the challenge of identifying an adequately supportive combination of DBS settings and medication for each individual, often within tight time constraints. This can be particularly difficult given the uncertainty of how DBS pulses interact with the human brain. In that context, the following suggestions may help individuals with DBS implants to engage during DBS programming:•At the commencement of a DBS programming session, ask the neurologist to explain the strategy they will employ that session to identify a DBS program with a greater therapeutic benefit.•Between clinic reviews, record the impact of different DBS programs on your symptoms. For example, record videos of moving or speaking, or the time required to complete set tasks. Such records may assist in reporting to your neurologist the impact of DBS outside the clinic environment.•Maintain a record of the settings for each DBS program prescribed. Just as one can discuss Parkinson's medication at a local support group, this enables discussion of DBS programs in a similar manner. Such information also provides a mechanism to check that the intended DBS settings have been programmed.•DBS systems typically have a mechanism to allow the recipient to switch between programs pre-set by the neurologist. When leaving DBS clinic, ensure that the best program for you upon entering that clinic is still available. If the impact of new DBS settings only becomes fully apparent after leaving the clinic, it may be helpful to revert to that previous program. Empowering people with Parkinson's disease and DBS implants to engage during DBS programming may secure greater benefits from this remarkable technology.