Rapid eye movement sleep behaviour disorder in brain injury: A complex case requiring close coordination of care

1 Introduction

Neurorehabilitation is interdisciplinary and cross-sectorial, requiring the coordinated effort of diverse sectors, professions, patients and communities to manage complex condition-related disabilities (Failla and Wagner, 2015; Khan et al., 2016). A more holistic approach to experimental rehabilitation, such as the one demonstrated in this case, can incorporate individualized treatment plans into rehabilitation research to improve overall clinical care (Blackmore and Persaud, 2012; Albert and Kesselring, 2011). This case aims to highlight the benefit of collaboration between neurology, psychiatry, physiatry and rehabilitation therapists to successfully rehabilitate complex patients.

Mr. L is a 72-year-old Caucasian gentleman who presented to our institution from out of state. He initially came to Physical Medicine and Rehabilitation for assistance with neurorecovery following a stroke but was quickly noted to have significant issues with sleep, depression, and anxiety. His family psychiatric history was clinically significant for his mother with severe depression throughout her life, a father with possible bipolar disorder, an older brother with severe depression and several suicide attempts, a younger brother treated for obsessive compulsive disorder, a maternal grandmother with depression, and maternal aunt with an anxiety disorder.

Mr. L is a product of a typical pregnancy and birth; met developmental milestones within typical age ranges. There is no history of childhood behavioral problems including lighting fires, fighting, or animal cruelty. He was often kicked out of class for talking too much and would blurt things out. He reported being restless as a child and had a hard time sitting still but was never formally diagnosed with any neurodevelopmental disorders. There is no history of suspensions, expulsions, special education classes or need for an individualized education plan. He earned average grades in elementary, middle and high school. He completed a Bachelor’s degree.

Mr. L had a long history of “night terrors” behaviors, including screaming out, cursing, and thrashing, which about 15 years ago led to a serious injury to his wife. But he had never undergone sleep study for diagnosis. A few months prior to his presentation to the neuropsychiatry clinic, he had been diagnosed with rapid eye movement (REM) sleep behavior disorder (RBD) through a sleep medicine clinic. RBD involves a loss of muscle atony during REM sleep, thus allowing the patient to move in reaction to the content of dreams.

Substance use history was negative apart from drinking an occasional glass of wine.

Medical history prior to his stroke was positive for CHF, Type 2 Diabetes, essential hypertension, all of which were moderately well controlled up until the few months prior to his stroke. In 2019, he sustained a fall with head injury and loss of consciousness of unknown duration and “jerking movements.” He had also suffered several syncopal episodes after which he became amnestic, these episodes occurring three to four times between 2019 and 2021. At the time, a cardiac workup was negative.

In June of 2021 Mr. L had a right temporal intracranial bleed. He was hospitalized, underwent a craniotomy the same day as well as a repeat procedure during the hospital stay for continued increased intracranial pressure. The patient was briefly transferred to a subacute rehab before an intracranial infection developed and a craniectomy was required. The patient was again transferred to subacute rehab but this time function declined and sunken flap syndrome was diagnosed requiring repeat hospitalization and performance of cranioplasty with titanium plate. Post operatively patient was transferred to a skilled nursing facility to complete 12 weeks of antibiotics. He sustained several falls, one resulting in a broken left clavicle, had two to three new onset seizures and was also diagnosed with atrial fibrillation. After completing antibiotics his daughters moved him closer to them so they could care for him. That is when he sought management for rehabilitation at our institution.

2 Timeline

2021-06-04 Admitted out of state for stroke. Found to have a hemorrhagic stroke that required a craniotomy for decompression, and developed left hemiplegia and confusion.

2021-07-03 Transferred to subacute rehab July 4th.

2021-07-31 Discharged home on August 1st at which point his left side was mobile and he was talking. Four days later he developed a post-op infection for which he was readmitted and needed a craniectomy.

2021-09-03 Became lethargic, lost appetite and movement on left side and was diagnosed with sunken flap syndrome requiring admission for cranioplasty.

2021-09-10 Discharged to subacute rehab where he had multiple falls, injuries, bed sores and infections.

2021-10-12 Presented to Physical Medicine and Rehabilitation to establish care and begin therapies following recent stroke.

3 Narrative

After initial intake with a physiatrist specializing in spasticity management, patient was referred for physical therapy (PT), occupational therapy (OT) and speech language pathology (SLP) services as well as to a brain injury physiatrist, brain injury neuropsychiatrist and neurologists given overlapping issues with seizure history, sleep complaints and mood lability. The patient was also started on trazodone and recommended to return for potential injections for spasticity management.

While the patient was still experiencing poor sleep since the stroke characterized by insomnia, high levels of anxiety and issues with behavioral control, there were no longer any symptoms of RBD. This change was most likely secondary to discontinuation of selective serotonin reuptake inhibitor (SSRI) antidepressants following the stroke which had been used throughout the years when RBD was an issue. In addition to trazodone, Sertraline low dose was started by the first physiatrist the patient met given the reports of dysphoria and years requiring an antidepressant. Upon meeting our brain injury physiatrist, the patient reported he had been using Sertraline at night, so it was switched to daytime to avoid activating properties just prior to sleep. Melatonin was added and trazodone discontinued to try to minimize nighttime administration of serotonergic agents before sleep, as this can cause or worsen RBD. Sertraline was continued given unclear history at this juncture as well as patient reports of worsened depression and anxiety post stroke when SSRI was discontinued.

Concurrently to establishing care with multiple physicians, patient presented to outpatient rehabilitation therapy clinic for comprehensive multidisciplinary evaluations from OT, PT, and SLP. Therapists identified severe cognitive impairments in most cognitive domains although relatively intact language functioning. The patient had severe left neglect. Additionally, patient was limited by partial left upper extremity weight bearing while healing from a clavicle fracture sustained during a fall at subacute rehab, on top of spasticity in the same limb, impaired whole-body coordination, decreased standing balance, decreased endurance, poor sleep hygiene and decreased safety awareness. Given this range of impaired motor, cognitive, and emotional functioning, Mr. L had markedly diminished daily life functioning and was dependent on family members to assist with activities of daily living (ADLs). Assessment of some areas of functioning were limited by weight bearing precautions as well as his limited cognitive status. OT Functional Independence Measurement (FIM) scores were max to total assist. SLP evaluation with the Repeatable Battery for the Assessment of Neuropsychological Status Update (RBANS) was concluded to show impaired cognitive functioning (see Table 1).

As initial therapy course was complicated by dual-diagnosis of brain injury and sleep disorder, person- and family-centered interventions were required in order to facilitate progress toward established goals of reducing impairment and improving daily life functioning. Initially, patient’s daughter was provided with education and resources related to behavior management and de-escalation techniques to be used in home environment. The team maintained consistent open communication and collaboration with the patient, family and private-duty caregiver throughout the plan of care, adjusting recommendations as-needed. His engagement in rehabilitation therapy activities was limited by cognitive impairments and low mood. He had two hospital visits in the first month, one for a fall where he was discharged from the emergency department and the other for pneumonia which required hospitalization. Approximately two months in the treatment course the patient experienced reduction in activity tolerance and decreased ability to participate in full therapy schedule due to lethargy and inability to sustain attention.

Through team discussion, it was decided, given reports of severe mood lability during the nighttime as well as ongoing need for anti-epileptics, that Levetiracetam would be switched to Lamotrigine in an attempt to remove a potential iatrogenic contributor as well as provide mood stabilization. After two weeks of this new medication regimen, family and therapists reported improved mood especially during the day. The electroencephalogram (EEG) confirmed no epileptiform activity or seizures soon after.

As part of the comprehensive intervention program, there was a need to address Mr. L’s anxiety level, which was a source of distraction during the day and a disrupter for sleep. Intervention approach required extensive validation and education related to medical complexity. Recommendations included online and peer support groups, journaling as a therapeutic outlet, and listening to podcasts or books on tape which were of interest, yet unrelated to personal worries. During an occupational therapy session, therapeutic activity for guided emotional processing with visuomotor component, OT assisted patient with identifying key areas of fear and anxiety, writing into contained “bubbles” on mirror. The patient identified the following areas as primary stressors; relationship strain, fear of passing away due to medical complications, fear of having another stroke, and loss of identity. OT guided patient in identifying situations within versus beyond his control, and emphasized education on following medical advice for health, remaining heart healthy, and staying focused on short term goals. The patient was receptive. Improvements in mood stability and lower anxiety allowed for better therapy participation which in turn resulted in notable improvements in Mr. L’s daily life functioning.

Sleep continued to be an ongoing issue affecting Mr. L’s functioning. At follow-up visits, Mr. L reported no issues falling asleep, but if awakened overnight would become anxious and then could not fall back asleep. The patient would be restless and need to get out of bed, sometimes requiring using a stationary bike to discharge restless sensations in legs. To further improve sleep patient was advised to stop fluid intake at least two hours before bedtime as nocturia seemed to be a frequent cause of awakening. In addition, brain injury physiatrist and neuropsychiatrist discussed splitting nighttime clonazepam to provide an additional dose in the middle of the night instead of just at bedtime to help with anxiety when awakened. Additionally, neurology managed titration of Lamictal and discussion was held regarding restarting Wellbutrin which had helped patient before seizures and had been less impactful on sleep. Given low risk of seizure being triggered especially with extended-release formulation team decided to proceed with the addition of Wellbutrin after Lamictal was increased.

Sleep medicine specialist was consulted given that Mr. L’s history was suggestive of iatrogenically caused RBD while on high doses of SSRI prior to stroke. Given ongoing anxiety and depression sertraline was planned for discontinuation pending polysomnography results and Mirtazipine was started by neuropsychiatry in consult with sleep medicine physician to help with sleep onset and anxiety. A sleep study to further clarify the differential diagnosis was conducted with consideration of obstructive sleep apnea (OSA), given physical exam of crowded airway as well as risk after stroke, versus restless leg syndrome (RLS) based on reported leg movements at night and need to move around when awakened. Sleep study showed no RBD but mild OSA. Given this evidence, Doxepin (6 mg) at bedtime was started and Sertraline was tapered and then discontinued given concern for potential to trigger a new episode of iatrogenic RBD.

During the next therapy visit on the following day, patient reported feeling much better after receiving a restful night’s sleep since being prescribed doxepin. This improvement carried forward and patient had his peak therapy performance. At follow-up one month later, therapists had reported improvements in sustained attention. Gait improved with bilateral AFOs (ankle foot orthoses) with better stability and speed though safety still limited by left sided neglect.

At this point the main barrier to further progress with therapy were joint pain and stiffness in hands as well as ongoing anxiety symptoms. Of note, there were no significant complaints of sleepiness. Since sleep was improving but depression remained mirtazipine dose was increased. One month after these adjustments, the patient completed discharge evaluations with therapists approximately six months after staring at our institution. FIM scores improved for OT measures and while two measures of the RBANS (attention and visuospatial) remained low the rest improved. Additionally, all PT measures showed improvement.

Patient and family both noted throughout the initial months that the biggest difficulties hindering progress with rehabilitation post stroke were anxiety and sleep. The two issues were closely linked, but it was clear they felt neither had been addressed adequately and that no prior team had looked at the patient holistically or in conjunction with rehabilitation therapy services.

While multiple outpatient visits were required to first clarify the etiology of the complaints and then to adjust medications adequately, they felt the process led to clear improvements in therapy sessions and at home. Prior to medication adjustments they had hired multiple caregivers to assist with patients care needs as well as to monitor the patient while he slept. Many of these caregivers left given the burden of care related to nighttime behavioral dyscontrol. The rate of turnover slowed after our initial interventions improved behaviors and eventually patient was able to be managed in an assisted living facility rather than through full-time private caregiving in the home once sleep and mood were under better control.

5 Discussion

Sleep dysfunction is common after brain injuries (Fleming et al., 2020). In the acute phase there are multiple factors contributing to this, not least of all the issues of being in a hospital, particularly in intensive care (Mertel et al., 2020). However, sleep issues cause by brain injury itself persist and negatively affect rehabilitation and recovery (Fleming et al., 2020).

The most common sleep disturbance after stroke is disordered breathing which can both cause stroke and be caused by stroke (Hermann and Bassetti, 2016). This diagnosis is still under-treated. REM sleep behavior disorder, wherein patient have absent limb atony and act out vivid dream, is a rarer finding post-stroke. The overall prevalence was recently estimated at 11% of stroke survivors, though it is more common in brainstem lesions (Tang et al., 2014).

Given our patient’s psychiatric issues were exacerbated by significantly disrupted sleep, clarifying the etiology of poor sleep became the primary concern. This complicated case highlights importance of adequately assessing sleep dysfunction following brain injury. In this case, a team was required given the patient’s complicated stroke type, premorbid psychiatric history and subsequent rehabilitation needs. Each team member’s expertise was needed but more important was the integration of findings into a combined plan.

While it was difficult for the patient to meet so many specialists, we were able to keep progressing the patient’s function through frequent and clear communications amongst the team.

As the full workup was underway and while the patient waited to be seen by each team member, the physicians all still gave guidance to each other to allow medication changes that would avoid exacerbating RBD, such as changing anti-epileptic medications for better mood stability, using agents for sleep and depression that did not have a strong serotonergic effect.

Had the physicians operated independently in this case it is likely adjustments to medications would have been made which would have caused RBD symptoms to return and exacerbated poor sleep and mood (Trotti, 2010). Additionally, having similar communication with therapists allowed for quicker assessment of the impact of these changes and made it easier to monitor for adverse reactions.

6 Conclusion

This case of severe sleep dysfunction following brain injury highlights the importance of sleep for recovery. Additionally, our patient’s complexity not only highlights the need for effective team communication to manage unusual cases. Only through clear communication among team members was the correct diagnosis reached allowing for optimal treatment and improvement with therapies. Lastly, this case serves as an example of multi-disciplinary collaboration among brain injury specialties that ultimately improved patient care.