Post–Acquired Brain Injury Movement Disorders
HANNAH L. COMBS
KATHRYN J. DUNHAM
BRITTANY D. WALLS
AMELIA J. ANDERSON-MOONEY
It is widely accepted that movement disorders (MD) can develop as a consequence of an acquired brain injury (ABI) (Krauss & Jankovic, 2002), although challenges abound in the determination of etiology, appropriate assessment techniques, and effective treatments. Post-ABI MDs can vary significantly in symptom presentation and underlying pathogenesis on the basis of the influence of injury-related and patient-related factors, rendering understanding of those factors critical to treatment. A brief discussion of such pertinent factors is provided in what follows.
Review of historical writings reveals a variety of case reports on posttraumatic MDs. The possible link between trauma and development of a MD can be traced back as far as James Parkinson’s (1817) Essay on the Shaking Palsy. In this work, he observed that patients with what would eventually be termed Parkinson’s disease (PD) denied experiencing any traumatic injuries that could damage the brain stem, which would have been expected to cause disordered movement. Martland (1928) described the development of “punch drunk” syndrome with both behavioral and movement features after repeated boxing-related head injuries. Elaborating on this finding, Kremer, Russell, and Smyth (1947) reviewed a case series of seven patients that developed parkinsonian features after midbrain injuries of varying etiology, suggesting that the cause of the trauma is not as substantial as the affected area secondary to severe trauma. Continued case reports and reviews regarding posttraumatic MDs have been published (Koller, Wong, & Lang, 1989; O’Suilleabhain & Dewey, 2004) since the second half of the 20th century, highlighting increasing specificity regarding the neuroanatomical structures and pathways involved in post-ABI MDs.
When focal lesions are present, MD symptoms following ABI typically result secondary to strategic lesions in the basal ganglia or cerebellum, although lesions throughout the motor system have been implicated in the development of MD post ABI.
Tremor, which appears to be the most common symptom occurring after severe injuries (Krauss, Trankle, & Kopp, 1996), has been linked to lesions in the substantia nigra, thalamus, and cerebellum (Krauss et al., 1995).
Dystonia is typically the result of a lesion in the caudate, putamen, subthalamic nucleus, and thalamus (Krauss et al., 1992; Krauss, Mohadjer, Nobbe, & Mundinger, 1994).
Dyskinesia can result from lesions of the subthalamus, striatum, or thalamus (Koller, Weiner, Nausieda, & Klawans, 1979).
Post-ABI MD may also develop in the absence of focal lesions. For instance, there is some evidence that prior ABI with loss of consciousness increases the risk of later developing PD with its associated synuclein-related pathology (Bower et al., 2003). In addition, although some data suggest no increased risk for MDs in individuals exposed to repeated head injuries (Savica, Parisi, Wold, Josephs, & Ahlskog, 2012), other work has classified a disorder named “chronic traumatic encephalopathy” (CTE; formerly known as “dementia pugilistica”) in individuals who indeed develop MDs after chronic, repeated head injuries.
Although the literature remains controversial, as a clinical syndrome, CTE is characterized as a progressive tauopathy, involving cortical neurofibrillary tangles as well as damage to the cerebellum, septum pellucidum, and substantia nigra (Corsellis, Bruton, & Freeman-Browne, 1973; DeKosky, Blennow, Ikonomovic, & Gandy, 2013; Jordan, 2013). Two separate classification systems have been developed to differentiate stages of CTE pathology after repeated ABI in which movement symptoms or damage to brain structures related to movement are involved (McKee et al., 2013; Omalu et al., 2011).
However, the belief that any MD develops secondarily to preceding trauma is, by nature, always speculative. Generally, the milder the injury and the longer the interval between injury and onset of MD, the more speculative the causality becomes (O’Suilleabhain & Dewey, 2004).
Specifically, there is a strong research base to support the relationship between MDs and severe ABI, but the relationship with mild ABI is less strongly established (Curran & Lang, 1995; Jankovic, 1994; Krauss & Jankovic, 2002). Determining etiology by timeline is also flawed, because post-ABI MDs may have a delayed onset and variable progression over time (Katz, 1990). Despite this, some injury-specific connections are present in the literature.
CTE: When pathologically confirmed CTE is present, it is usually associated with repeated blows to the head, often due to sporting injuries in high-contact (e.g., football, boxing, and hockey) and/or high-velocity (e.g., motor racing) sports.
Moderate to severe ABIs: Links may be more definitively made between moderate to severe ABIs and MDs (Bazarian, Cernak, Noble-Haeusslein, Potolicchio, & Temkin, 2009; Johnson & Hall, 1992). MDs may develop particularly often secondary to penetrating injuries or hemorrhages occurring after diffuse impact (Krauss et al., 1995; Krauss & Jankovic, 1997).
Severe ABI: Krauss, Trankle, and Heinz-Kopp (1996) reviewed the prevalence of MD in a sample of 221 adults with severe ABI, with follow-up occurring 3.9 years post injury on average. In this group, 22.6% of patients developed MDs, the most common symptom of which was tremor (19%) and dystonia (4.1%). Prevalence may be higher in children after severe ABI, with literature reflecting rates from 13% to 66% (Krauss & Jankovic, 2002). One survey including 289 children after severe ABI demonstrated a 45% rate of tremor specifically (Johnson & Hall, 1992).
Moderate and Mild ABI: MDs are thought to occur less commonly in this group. Although transient tremors that do not require intervention may be more common, rates of persistent tremor are estimated to be approximately half of those after severe ABI, with one study estimating the maximum prevalence of persistent, mild tremors after mild to moderate ABI at 10% (Krauss, Trankle, & Kopp, 1997). This sample included both children and adults.
Neurodegenerative disorders: Beyond the known increased risk of Alzheimer’s disease associated with both moderate and severe ABI (Plassman et al., 2000), patients with a positive ABI history can also develop progressive neurodegenerative disorders involving movement. The most commonly recognized neurodegenerative disorders developing after ABI are CTE and PD, with characteristic disease courses and symptom presentations.
CTE: Onset of clinical symptoms of CTE can be quite delayed. In athletes, symptoms may not emerge until 10 to 20 years after the end of an athlete’s career (Bazarian et al., 2009). By definition, CTE includes the presence of motor symptoms, which typically present as slurring of speech, uncoordinated gait, tremor, or spasticity in addition to headache, mood changes, and cognitive changes (Jordan, 2013). The movement pattern may appear to be parkinsonian in some patients (Krauss & Jankovic, 2002).
PD: Pathogenic connections between PD and ABI are inconsistent in the literature, although some available evidence is compelling. The risk of PD is elevated with more complicating symptoms, including loss of consciousness or more severe injury overall (Bower et al., 2003). In an examination of 93 twin pairs (both monozygotic and dizygotic), a history of ABI with amnesia or loss of consciousness was associated with a greater risk for PD, which was compounded when those injuries required hospitalization or were followed by additional ABI (Goldman et al., 2006). PD itself is characterized by a distinctive pattern of levodopa-responsive movement symptoms, including asymmetrical resting tremor, bradykinesia, rigidity, and postural instability (Lang & Lozano, 1998).
Nondegenerative movement disorders: The presentation of MD that are not related to PD or CTE can be highly varied, including tremors and other symptoms and clinical courses that can confound even skilled diagnosticians.
Onset timelines: Onset of MD symptoms may be significantly delayed after the ABI occurs, with latencies of weeks to years after injury (Krauss & Jankovic, 2002). In some samples, tremors were noted to develop between 2 weeks and 6 months post ABI, and dystonia developed between 2 months and 2 years afterward (Krauss et al., 1997).
Symptoms: Post-ABI movement symptoms often occur with spasticity, generalized weakness, and apraxia (O’Suilleabhain & Dewey, 2004). Beyond this, tremors and dystonia are among the most consistently noted symptoms, particularly after severe ABI (Curran & Lang, 1995; Jankovic, 1994).
Spasticity: Commonly experienced after moderate to severe ABI, spasticity is characterized by increased muscle tone that interferes with usual muscle contractures. This can be severe enough to interfere with independence in activities of daily living, including basic mobility and self-care (Elovic, Simone, & Zafonte, 2004).
Myoclonus: Myoclonic movements involve sudden jerking movements that may be unpredictable. These movements are often less rhythmic and smaller in amplitude when compared with tremors (O’Suilleabhain & Dewey, 2004).
Tremor: Post-ABI tremors include both postural and kinetic tremors, the latter often being more disabling. Often affecting the arms, such tremors can be present at rest and during action, increasing in amplitude toward the action’s end point. Tremors often range in frequency from 2.5 to 4 Hz, but can be very coarse, with amplitudes larger than 10 cm (Krauss & Jankovic, 2002).
Dystonia: Involuntary muscle contractures resulting in twisted or contorted postures can occur, typically involving one side of the body (hemidystonia). This may co-occur with tremor or myoclonus and be present at rest (Krauss & Jankovic, 2002).
Other posttraumatic hyperkinesias: Although occurring less frequently, additional hyperkinetic symptoms may develop post ABI, including ballism, chorea, and tics/tourettism (Krauss & Jankovic, 2002).