Transcranial Magnetic Stimulation and Traumatic Brain Injury

Mon, 03/08/2021 - 09:05

By: Debra J. Stultz MD

March is Brain Injury Awareness Month.  This year the theme from the Brain Injury Association of America is  #MoreThanMyBrainInjury. They report that each year at least 2.8 million Americans sustain a traumatic brain injury (TBI).  There have long been studies revealing possible pharmaco-resistance in TBI patients.  Barker-Collo et al. 2013(1) suggested TBI is linked with poorer outcomes.  Dinan and Mobayed 1992(2) reported decreased TBI patients' response compared to primary depression in 13 patients while using amitriptyline.  Ashman 2009(3), in a double-blind, randomized, controlled trial of 52 patients with TBI, studied sertraline up to 200 mg or placebo for ten weeks while following the Hamilton Rating Scale for Depression (HAM-D).  Both groups revealed improvement, with 59% of the sertraline group and 32% of the placebo group having a 50% decrease in the HAM-D.  Fann et al. 2017(4), in a randomized, double-blind, placebo-controlled group of 62 patients with TBI patients within one year of hospitalization for complicated mild to severe TBI, found no significant difference between placebo and those treated with sertraline. 

Patients having a traumatic brain injury are at increased risk of developing psychiatric disorders.  Reti et al. 2015(5) reported the lifetime prevalence of major depressive disorder following TBI is between 25 – 50%.  Moussavi 2019(6) reported that in most cases of mild traumatic brain injury (also called concussion), the symptoms usually disappear in the 1st 2 – 4 weeks.  However, the symptoms can persist for months or years following the injury; these patients are then referred to as having Persistent Post-Concussion Syndrome (PCS).  Koski 2015(7) stated in 15-25% of cases, PCS persists beyond the usual 3-month recovery period.  Always et al.  2016(8) reported a 5-year prospective study on 161 patients with moderate to severe TBI and revealed in the 1st five years post-injury, 75.2% were diagnosed with a psychiatric disorder.  After traumatic brain injury, the rates of mood disorders were 40% in the first year and 27.7% in the 5th year after injury.  Increased rates were seen for Major Depressive Disorder (18.7% - 28.3%), Depressive Disorder NOS (6.5% - 15-8%), Bipolar Disorder (up to 3.1%), and Dysthymia (up to 2%).  Kerr et al. 2012(9) studied 1044 members of the National Football League Retired Players Association between 2001 and 2010 and found that 10.2% of the respondents (106/1044) reported being clinically diagnosed with depression at some point of time during the nine years.  Approximately 65% self-reported at least one concussion during their careers.  They reported, "the association between concussions and depression was independent of the relationship between decreased physical health and depression."

As TBI is an increasingly prevalent event, and these patients may be resistant to the usual medications for depression, alternatives treatments are necessary.  Transcranial Magnetic Stimulation may be an important treatment option for these clients.  Previously, the fear of seizures with TMS treatment has been a rate-limiting issue in TBI patients.  Dhaliwal et al. 2015(10) stated, "patients with severe TBI do show an increased risk of unprovoked seizures," and "there is a strong connection between the severity of a brain injury and the subsequent risk of seizures; individuals with mild to moderate TBI have a substantially lower seizure risk than those with severe TBI." Reti et al. 2015(5) indicated, "TBI is associated with an increased risk of both early and late spontaneous seizures, a significant consideration in evaluating rTMS as a potential treatment for TBI depression.  Whilst the risk from rTMS is low; underlying neuropathology may somewhat increase that risk." They suggested that low-frequency rTMS might be less likely to trigger a seizure. 

Various reports of patients with a history of a head injury having a TMS-related seizure have been described.  Bernabeu et al. 2004(11) reported on TMS use in  a TBI patient who had a seizure while using fluoxetine, but they used a brief interstimulus interval.  Cavinato et al. 2012(12) described a 31-year-old male with a history of a severe TBI 8 months before TMS initiation.  He had a secondary generalized seizure on the 4th of 10 daily sessions.  TMS was delivered at 90% MT, 20 Hz, 1s train duration, and 1-minute inter-train interval to the dorsolateral prefrontal cortex (DLPFC).  The seizure developed three hours after treatment. Pape et al. 2014(13) reported on a 32-year-old male who had a TBI 9 years before TMS initiation who had an EEG-identified seizure during the treatment with no clinical expression.  Boes et al. 2016(14) reported on a 27-year-old male with MDE, GAD, alcohol use, and a history of 4 prior head injuries.  He was also sleep-deprived.  He developed a seizure during the 12th treatment session.  Muir et al. 2019(15) presented a patient having a seizure with a history of oxcarbazepine withdrawal the week before the seizure, autism, and multiple head injuries.

Increasingly, studies are revealing Transcranial Magnetic Stimulation is being used successfully without seizures in patients with a history of brain injury and with benefit for various symptoms/disease states.  Consentino et al. 2010(16) used low-frequency rTMSto the right temporal lobe in a patient having posttraumatic complex auditory hallucinations of continuous music. The  hallucinations were significantly reduced with treatment.    Fitzgerald et al. 2011(17) presented a study using TMS in a depressed patient with a mild TBI history 14 years before starting TMS.  The patient was given daily bilateral rTMS with 1 Hz treatment over the right DLPFC, followed by 10 Hz treatment over the left DLPFC.  The patient had improvement in both mood and cognition after four weeks and no reported seizuzre.  Bonni et al.(18) 2013 used continuous theta-burst stimulation over the left posterior parietal cortex to improve cognitive symptoms in a patient with a visuospatial deficit.  Kreuzer et al. 2013(19) treated a TBI patient with TMS for severe tinnitus after a head injury with five treatment series of 1 Hz to the left primary auditory cortex at 110% MT and no reported seizure.  George et al. 2014(20) used high-frequency rTMS over the left DLPFC with a figure-eight core at 120% MT and 10 Hz for 30 minutes three times daily for three days, comparing it to sham-controlled for treating suicidality.  58% of the patients also had a history of TBI, and no seizures were reported. Neville et al. 2015(21) completed a randomized controlled trial of 36 patients with TBI divided into two groups and administered ten sessions of 10 Hz TMS over the left DLPFC, which demonstrated improvement in depression and cognitive functioning.  Nielson et al. 2015(22) reported on a 48-year-old man with a severe TBI history five years before TMS was administered with low frequency right dorsolateral prefrontal cortex stimulation daily for six weeks.  The patient demonstrated a 49% improvement in his Hamilton Depression Rating Scale(23) with treatment.  Their article set forth that those who have not had a seizure within two years of injury have a 90% lower risk of seizure based on work by Englander et al. 2003(24).

Koski et al. 2015(7) treated 12 patients with post-concussive symptoms (headaches, depression, and cognitive deficits) following mild TBI using 20 sessions of rTMS to the left DLPFC at 5-sec trains, 10 Hz, and 110% Motor Threshold.  Their patients demonstrated a decrease of 14.6 points (p= 0.009) of post-concussive symptoms. The patients had a fMRI assessment before and after treatment with clinical assessment at three months follow-up.  The patients demonstrated fMRI task-related activation peaks in the DLPFC were increased after rTMS, and reported fewer sleep disturbances and better mental focus.   Rutherford et al. 2017(25) studied 13 patients with mild TBI delivering 13 treatment sessions of rTMS to the left DLPFC at 20 Hz in 1.5-second trains of 30 pulses and an inter-stimulation separation of 28.5 seconds.  Their study suggested rTMS may be effective for some of the self-reported symptoms of post-concussive disorder.

Paxman et al. 2018(26) safely used TMS in a 61-year-old male patient with mild TBI patient when treating chronic dizziness with ten sessions of rTMS to the left DLPFC, 70% motor threshold, and a frequency of 10 HZ.  The patient had decreased dizziness severity and frequency by greater than 50% at three months and reduced scores on the Dizziness Handicap Inventory(27).   Lee and Kim 2018(28) studied 13 patients divided into an experimental group and a sham group.  The patients were given rTMS to the right DLPFC for ten sessions and demonstrated improvements in mood based on the Montgomery-Asberg Depression Rating Scale(7) and cognition using the Trail Making Test(29) and the Stroop Color-Word Test(30).  Iliceto et al. 2018(31) treated a 37-year-old man with a severe TBI secondary to a suicide attempt having a 60-foot fall who had a history of anxiety and bipolar disorder.  The patient received 30 treatments of 6 Hz TMS to the left DLPFC at 120% MT and a 26-second inter-stimulation interval using the Neurostar system.  Following the PHQ-9, he had a 70.8% improvement in mood.

Saunders and Bermudes 2018(32) described a 55-year female with a TBI and loss of consciousness during her series of TMS treatments.  The event was unrelated to the TMS, and the patient was hospitalized for four days.  TMS was restarted 11 days after the injury without incident .  In 2018 Siddiqi et al. (33) used 20 bilateral TMS sessions in a retired NFL defensive lineman. The patient reported at least 12 previous concussions. Using the Montgomery – Asberg Depression Rating Scale, the patient documented improved scores from 32 to 9. 

Leung et al. 2018(34) studied 29 patients looking at depression and headaches in a veteran population with either real or sham treatment at 10 Hz and 80% MT to the left prefrontal cortex. Using the HAM-D, depression in the real group demonstrated significant improvement, and the sham group was mostly unchanged.  With respect to headaches, the patients demonstrated decreased prevalence and intensity. 

Stultz et al. 2019(35) presented a case of a 23-year-old male athlete with a history of four sports-related concussions (two of which required hospitalization) having significant depression, generalized anxiety, panic, and OCD symptoms. The patient received 34 TMS treatments and nine booster sessions without a seizure and with improvement in mood and anxiety.  He was treated with the H1 coil at 120% MT to the left DLPFC while following the Beck Depression Inventory and the PHQ-9.  Ahmed et al. 2019(36) studied depression in mild to moderate TBI in 12 patients using the Magstim Rapid2 with BrainSight Neuronavagation to the right and/or left dorsolateral prefrontal cortex while following the PHQ-9 and the physician administered HAM-D.  They reported improved depression, anxiety, and post-concussion symptoms with decreased levels on both the PHQ-9 and HAM-D. 

Siddiqi et al. 2019(37) completed a randomized study of 15 patients who were given 20 sessions of bilateral rTMS (4000 left excitatory and 1000 right inhibitory) stimulation or sham treatment with the use of rTMS targeted stimulation having individualized resting-state network mapping of the dorsal attention network and default mode network in patients with concussions or moderate TBI.  Their study followed the Montgomery-Asberg Depression Rating Scale (MADRS) with a mean improvement of 56% +/- 14% in the active group and 27% +/- 25% with Sham treatment.  MADRS improvement was inversely correlated with functional connectivity between the right-sided stimulation site and the subgenual anterior cingulate cortex.  Active treatment led to increased sgACC-DMN connectivity.    No seizures or other significant adverse events were reported. 

Moussavi et al. 2019(6) completed a randomized, placebo-controlled, double-blind study on 18 patients with Post-Concussion Syndrome. One half received real TMS, and one half received sham.  Their research indicated TMS improvement in those with a shorter duration of injury (<one year) based on the Rivermead Post-Concussion Symptoms Questionnaire (38).  The secondary outcome measure used was the MADRS scale for depression.

Stilling et al. 2019(39) studied posttraumatic headache and post-concussion symptoms in a double-blind, randomized, controlled trial of 20 participants with ten sessions to the left DLPFC at 10 Hz and 70% MT.  They followed the headache frequency at one month, a headache diary, and a PHQ-9 at the onset, one-month, three-month, and six months post-treatment.  They found decreased depression ratings in the real group at one-month post-treatment, with no change in the sham group.  This study demonstrated improvement in the severity of headache, depression, post-concussion symptoms, and quality of life, but findings were below clinical significance thresholds.  Among their patient's 60% returned to work in the real group, whereas only 10% of the sham-controlled patients returned. 

Hoy et al. 2019(40) studied 21 patients in a randomized, double-blind placebo-controlled trial of rTMS using 20 treatments to the bilateral left and right DLPFC and found a significant reduction in the MADRS with both groups but no significant effect in depression between the two groups. They also found significant improvement in cognition with active treatment on executive functioning and working memory.

Meek et al. 2020(41) used Accelerated TMS of twice-daily 1 Hz rTMS over the right DLPFC in 15 patients with mild TBI for 30 sessions.  Improvements were noted in post-concussion symptoms, depression, anxiety, disability, and pain ratings.  Cognitive improvements were found in verbal fluency, working memory, selective attention, and cognitive processing speed. 

 Garland et al. 2020(42) have an ongoing study of bilateral prefrontal TMS for TBI treatment and PTSD in veterans using 30 treatments of weekday treatments followed by a two-week taper of 3 and then 2 sessions per week.  Their study is a double-blind, prospective, randomized, sham-control study of 3500 pulses to the left DLPFC at 10 Hz and 1500 pulses to the right DLPFC at 1 Hz. 

As described above, there are increasing numbers of TMS studies in patients having had a TBI with benefits in multiple areas, including depression, PTSD, headaches, cognition, tinnitus, dizziness, etc., and some with mixed or no results.   Additionally, these studies are demonstrating TMS treatment without seizures.  While TMS-related seizures are still an issue in treatment initiation, Siddiqi 2019(43) suggested seizures in TMS may be elevated primarily in penetrating-hemorrhagic injuries rather than diffuse-multifocal injury based on previous reports(44).  When considering TMS treatment, factors to consider with respect to seizures  are the severity of the injury, the lapse of time between injury and treatment, co-existing medications/disorders, and other seizure risks. One should also weigh the benefits of TMS treatment versus denial of treatment in a population that may be resistant to other treatment options. 

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