Recovery of an injured corticospinal tract via an unusual pathway in a stroke patient: Case report.

RATIONALE: A few mechanisms of recovery from an injured corticospinal tract (CST) in stroke patients have been reported: recovery of an injured CST through (1) normal CST pathway, (2) peri-lesional reorganization, and (3) shifting of the cortical origin area of an injured CST from the other areas to the primary motor cortex. However, it has not been clearly elucidated so far. PATIENT CONCERNS: A 57-year-old male patient presented with complete weakness of the right extremities due to an intracerebral hemorrhage (ICH) in the left basal ganglia. At three weeks after onset, the patient showed severe weakness of his right upper and lower extremities (Motricity Index [MI]: 28/100, finger extensor: 0/5). At 6 months after onset, his weakness showed some recovery, however, right finger extensor did not show any recovery (MI: 51/100, finger extensor: 0/5). At 9 months after onset, weakness showed significant recovery, particularly right finger extensor (MI: 64/100, right finger extensor: 3/5) and similar motor function persisted until 11 months after onset (MI: 67/100, right finger extensor: 3/5). DIAGNOSES: The patient was diagnosed as the right hemiplegia due to ICH in the left corona radiata and basal ganglia.
INTERVENTIONS: Clinical assessment, transcranial magnetic stimulation (TMS), and diffusion tensor tractography (DTT) were performed at 1, 6, 9, and 11 months after onset. OUTCOMES: Discontinuation of the left CST at the midbrain level was observed on 1-month DTT and the corona radiata on 6-month DTT. However, on 9-month DTT, we observed a CST branch originating from the left posterior parietal cortex and then connecting to the main truck to the CST at the thalamic level and thickened on 11-month DTT. On 1-month TMS, no MEP was evoked from the left hemisphere; on 6-month TMS study, MEPs were obtained at a right hand muscle (latency: 22.8 ms, amplitude: 130 μV) and its amplitude was increased as 300 μV with similar latencies on 9- and 11-month TMS studies. LESSONS: Recovery of an injured CST via an unusual pathway was demonstrated in a hemiparetic patient with ICH, using DTT and TMS. We believe that our results suggest that precise evaluation for an injured CST using TMS and DTT might be necessary, particularly in young patients, even after 6 months from onset even though the stroke patients show clinical characteristics of severe injury of the affected CST.

Introduction

The corticospinal tract (CST) is the major neural tract for motor function in the human brain.[ The CST is essential for good motor recovery in stroke patients, therefore clarification of the recovery mechanism of an injured CST in stroke patients is clinically important.[ A few mechanisms of recovery from an injured CST in stroke patients have been reported: recovery of an injured CST through (1) normal CST pathway, (2) peri-lesional reorganization, and (3) shifting of the cortical origin area of an injured CST from the other areas to the primary motor cortex.[ However, it has not been clearly elucidated so far.

Diffusion tensor tractography (DTT) and transcranial magnetic stimulation (TMS) have commonly been used for evaluation of the state of an injured CST.[ DTT provides a three-dimensional evaluation of the integrity and pathway of the injured CST.[ However, DTT can produce false negative results throughout the white matter due to crossing fibers.[ By contrast, TMS can distinguish between the CST and non-CST, and estimated amount of the CST by analyzing the characteristics of the motor-evoked potential (MEP).[ However, TMS also has limitations including poor spatial resolution and the possibility of a false negative result due to excessive high threshold following stroke.[ As a result, combined use of DTT and TMS can enable more precise evaluation of an injured CST.

In this study, we report on a patient with intracerebral hemorrhage (ICH) who showed recovery of the injured CST via an unusual CST pathway, which was demonstrated using DTT and TMS.

Case report

A 57-year-old, right-handed male patient presented with complete weakness of the right upper and lower extremities due to an ICH in the left corona radiata and basal ganglia (Fig. 1A). At three weeks after onset, he was transferred to the rehabilitation department for rehabilitation after conservative management for the ICH at the department of neurosurgery of a university hospital. The patient showed severe weakness of his right upper and lower extremities (Motricity Index [MI]: 28/100, and the finger extensor: 0/5)[ (Table 1). He participated in a comprehensive rehabilitative management program, including movement therapy, neurotrophic drugs (pramipexole: 1 mg, amantadine: 300 mg, ropinirole: 2 mg, and levodopa: 750 mg), and neuromuscular electrical stimulation therapy of the right finger extensors and ankle dorsiflexors.[ He was transferred to a local rehabilitation hospital after 1 month's rehabilitation and continued comprehensive rehabilitative therapy until 6 months after onset. At 6 months after onset, his motor weakness showed some recovery, however, his right finger extensor did not show any recovery (MI: 51/100, and the finger extensor: 0/5). After 6-month evaluation for the CST using DTT and TMS, he was re-admitted to the rehabilitation department of the same university hospital. He underwent more intensive rehabilitation for facilitation of the injured left CST including repetitive transcranial magnetic stimulation therapy (rTMS [MAGPRO, Medtronic Functional Diagnostics, Skovlunde, Denmark]: precentral knob, frequency of 10 Hz, intensity of 80% motor threshold, and a total of 160 pulses for 8 min, and seven sessions per week),[ increment of neurotrophic drugs (increased doses: pramipexole: 1 mg and ropinirole: 2 mg), and muscle wash for relieving spasticity of the right finger extensors because his right finger flexors showed severe spasticity as 2+ on the Modified Ashworth Scale.[ As a result, at 9 months after onset, his motor weakness showed significant recovery, particularly his right finger extensor (MI: 64/100, and the right finger extensor: 3/5) and similar motor function persisted until 11 months after onset (MI: 67/100, and the right finger extensor: 3/5). The patient provided signed, informed consent and our institutional review board approved the study protocol.

Figure 1

(A) T2-weighted images showing leukomalactic lesions in the left corona radiata and basal ganglia. (B) Results of diffusion tensor tractography (DTT). Discontinuation of the left CST at the midbrain level is observed on 1-month DTT and the corona radiata on 6-month DTT. However, on 9-month DTT, a CST branch originating from the left posterior parietal cortex (circle) and then connecting to the main trunk to the CST at the thalamic level is observed and this branch is thickened on 11-month DTT. (C) Results of transcranial magnetic stimulation (TMS). On 1-month TMS, no motor evoked potential (MEP) is evoked from the left hemisphere. On 6-month TMS study, MEP is obtained from the right abductor pollicis brevis muscle during stimulation of the left hemisphere with 100% of maximal output (the shortest latency; latency: 22.8 ms, amplitude: 130 μV) and its amplitude is increased as 300 μV with similar latencies (23.4 ms, 23.2 ms) on 9- and 11-month TMS studies.

Table 1

Changes of motor function in the patient.

Diffusion tensor imaging and transcranial magnetic stimulation

DTI data were acquired four times (1 month, 6 months, 9 months, and 11 months after onset) using a sensitivity-encoding head coil on a 1.5-T Philips Gyroscan Intera (Hoffman-LaRoche Ltd, Best, The Netherlands) with single-shot echo-planar imaging and navigator echo. Imaging parameters were as follows: acquisition matrix = 96 × 96; reconstructed to matrix = 192 × 192 matrix; field of view = 240 × 240 mm2; TR = 10,398 ms; TE = 72 ms; parallel imaging reduction factor = 2; EPI facto = 59; b = 1000 s/mm2; and a slice thickness of 2.5 mm. Fiber tracking was performed using the fiber assignment continuous tracking (FACT) algorithm implemented within the DTI task card software (Philips Extended MR Work Space 2.6.3). Each DTI replication was intra-registered to the baseline “b0” images to correct for residual eddy-current image distortions and head motion effect, using a diffusion registration package (Philips Medical Systems). For reconstruction of the CST, the first region of interest (ROI) was placed on the upper pons (portion of anterior blue color) on the color map with an axial image. The second ROI was placed on the mid pons (portion of anterior blue color) on the color map with an axial image. The termination criteria used for fiber tracking were FA < 0.1, angle < 27°.[

Discontinuation of the left CST at the midbrain level was observed on 1-month DTT and the corona radiata on 6-month DTT. However, on 9-month DTT, we observed a CST branch originating from the left posterior parietal cortex and then connecting to the main truck to the CST at the thalamic level and this branch was thickened on 11-month DTT (Fig. 1B).

TMS was also performed four times (1 month, 6 months, 9 months, and 11 months after onset) using a Magstim Novametrix 200 magnetic stimulator with a 9-cm mean diameter circular coil (Novametrix Inc., USA). Cortical stimulation was performed with the coil held tangentially over the vertex. The left hemisphere was stimulated by a counterclockwise current, and the right hemisphere was stimulated by a clockwise current. Motor-evoked potentials (MEPs) were obtained from both abductor pollicis brevis muscles in a relaxed state. The excitatory threshold (ET) was defined as the minimum stimulus required to elicit an MEP with a peak-to-peak amplitude of 50 μV or greater in two out of four attempts. Stimulation intensity was set at the ET plus 20% of the maximum stimulator output.

On 1-month TMS, no MEP was evoked from the left hemisphere, even though stimulation intensity was increased to 100% of maximal output. By contrast, on 6-month TMS study, MEPs were obtained at the right abductor pollicis brevis muscle during stimulation of the left hemisphere with 100% of maximal output (the MEP of shortest latency; latency: 22.8 ms, amplitude: 130 μV) and its amplitude was increased as 300 μV with similar latencies (23.4 ms, 23.2 ms) on 9 -and 11-month TMS studies (Fig. 1C).

Discussion

In this study, we followed up DTT and TMS for an injured CST in a patient with ICH who showed recovery of the injured CST via an unusual pathway. We believe that the injured left CST recovery was based on the evidences of motor recovery of the right finger extensor, and the characteristics of the MEP on the right hand muscle:

although the CST is involved in the motor control of all muscles of the extremities, previous studies have reported that the affected finger extensor is the most representative indicator of recovery of an injured CST,[ and

the latency of a MEP can discriminate whether the MEP originated from the CST because the latency of the MEP indicates the fastest velocity of a neural tract.[

We believe that this patient had the following characteristics that differed from the motor recovery of usual hemiparetic stroke patients:

the injured left CST recovery was occurred via an unusual motor pathway originating from the posterior parietal cortex connected to the CST at the thalamic level. This appeared to be attributed to the variety of the cerebral origin of the CST originating from the fronto-parietal cortices, including the primary motor cortex, the secondary motor area, and the somatosensory cortex,[

most of the motor recovery in stroke patients occurs within 6 months after onset.[ However, this patient showed significant motor recovery of the right finger extensor by the more active rehabilitation since 6 months after onset when we found the evidence of the minimally recovered left CST on the 6-month MEP even though the patient's motor function coincided with a severe injury of the affected CST,[ and

more precise evaluation of the injured left CST by combined study using DTT and TMS; on 6-month evaluation, we observed the injured left CST on TMS even though DTT showed discontinuation of the injured left CST; in contrast, on 9- and 11-month DTT, we confirmed the three-dimensional configuration of a branch from the left posterior parietal cortex connected to the main trunk of the left CST at the thalamic level.

In conclusion, recovery of an injured CST via an unusual pathway (from the posterior parietal cortex) was demonstrated in a hemiparetic patient with ICH, using DTT and TMS. We believe that our results suggest the following take home message: precise evaluation for an injured CST using TMS and DTT might be necessary, particularly in young patients, even after 6 months from onset even though the stroke patients show clinical characteristics of severe injury of the affected CST.

Author contributions

Data curation: Sung Ho Jang, Young Jin Jung.

Investigation: Chul Hoon Chang.

Writing – original draft: You Sung Seo.