Fig. 1
Cervical spinal cord stimulation (SCS). Radiography images show the location of the stimulation electrode and implantable pulse generator (IPG). Left, IPG under the anterior chest wall; Middle, lateral view of cervical X-ray; Right, antero-posterior (A-P) view of cervical X-ray
The families of all the patients provided their written informed consent for this procedure. This study was approved by the Committee for Clinical Trials and Research on Humans of our university and conformed with the principles outlined in the Declaration of Helsinki.
Measurement of Regional Cerebral Blood Flow Before and During SCS
Employing single-photon emission computed tomography (SPECT), we could measure the CBF of the whole brain before and during SCS in eight of the ten MCS patients who were treated with SCS. SPECT was performed using a Prism 2000XP gamma camera system (Shimazu, Kyoto, Japan). Using an ethyl cysteinate dimer, quantitative regional CBF images were converted from qualitative axial SPECT images by the application of Patlak plot graphical analysis with radionuclide angiography and Lassen’s linearization. We compared CBF before and during SCS.
Statistical Analysis
Changes in the regional (r) CBF of the whole brain induced by SCS in MCS patients were compared using the paired t-test.
Results
Electrophysiological Evaluation of VS and MCS Patients
As VS candidates for SCS therapy, we generally try to select patients who showed both the fifth wave in the ABR and N20 in SEP by electrophysiological evaluation [24–27]. However, it has not been so easy to find VS patients in whom both the fifth wave in ABR and N20 in SEP are detectable. Both measures were recorded in only 8 of the 21 VS patients treated with SCS in the present study. In contrast, we detected both the fifth wave in the ABR and N20 in SEP in 9 of our 10 MCS patients.
Phenomena Induced by 5-Hz Cervical SCS in VS and MCS
SCS did not induce strong arousal responses such as those that were observed by the deep brain stimulation (DBS) of the CM-pf complex and mesencephalic reticular formation in our previous reports [23, 25, 26]. However, 5-Hz cervical SCS induced muscle twitches of the bilateral upper extremities; these were not induced by DBS. While 5-Hz cervical SCS induced muscle twitches, 25-Hz cervical SCS induced muscle contraction of the upper extremities. Thus, we considered that 5-Hz cervical SCS is more suitable for neurorehabilitation and neuromodulation than higher-frequency cervical SCS.
In eight MCS patients, the average CBF without SCS was 38.8 ± 5.1 ml/100 g/min, while that during SCS was 47.51 ± 7.8 ml/100 g/min. SCS increased CBF diffusely in the brain, except at the lesion site, and the average CBF of the whole brain increased by 22.2 % during SCS compared with the CBF before SCS (p < 0.0001, paired t-test).
Long-Term Effect of SCS in VS Patients
Among the 21 VS patients treated by SCS, only 8 patients showed both the fifth wave in the ABR and N20 in SEP before SCS. Of these 8 patients, only 3 patients recovered from VS and became able to communicate through speech or other responses. The causes of brain injury in the 3 VS patients who recovered were head injury (1 case) and cerebrovascular accident (2 cases). These 3 VS patients were treated by SCS at 3, 5, and 8 months after the brain injury. The 5 other VS patients showing both the fifth wave in the ABR and N20 in SEP, and who failed to recover from VS, were treated by SCS at 13, 14, 20, 36, and 51 months after the initial brain injury and coma. In the 3 patients who recovered from VS, the head injury patient recovered at 14 months, and the two cerebrovascular accident patients recovered at 8 and 12 months after the initial brain injury and coma. All 3 patients who recovered from VS remained in a bedridden state with severe disability, determined on the basis of the Glasgow Outcome Scale [10].
Long-Term Effect of SCS in MCS Patients
Giacino et al. [5] proposed criteria for determining emergence from MCS, characterized by reliable and consistent demonstration of one or both of the following: (1) functional interactive communication and (2) functional use of two different objects. On the basis of these proposed criteria, it was determined that seven of our ten patients emerged from MCS following SCS therapy.
In nine of the ten MCS patients, both the fifth wave in the ABR and N20 in SEP were detectable before SCS. All seven patients who recovered from MCS following SCS were among this group. The cause of brain injury in these seven patients was head injury (6 cases) and cerebrovascular accident (1 case), and the patients were treated by SCS at 3 months (4 patients), 8 months (1 patient), and 9 months (2 patients) after the initial brain injury. Among these seven patients, one showed improvement to only moderate disability at 1 year after the start of SCS therapy, as determined using the Glasgow Outcome Scale [10], and became able to walk by himself. Although the other six patients required the use of a wheelchair, four were able to use the wheelchair by themselves with some assistance. The other two patients were unable to handle the wheelchair by themselves even with some assistance. The two MCS patients who showed the fifth wave in the ABR and N20 in SEP but did not recover from MCS were treated with SCS at 11 and 12 months after the initial brain injury.
Discussion
Electrophysiological Evaluation and Timing of SCS
We have reported that electrophysiological evaluation is useful for estimating the resting brain function of VS and MCS patients, and we have recorded ABR, SEP, pain-related P250, and used continuous electroencephalogram (EEG) frequency analysis for the treatment of VS with DBS [24, 27]. In the present study, we performed only ABR and SEP for electrophysiological evaluation, because SCS for VS patients was applied mainly in our satellite hospital where pain-related P250 and continuous EEG frequency analysis are typically not recorded before SCS treatment. In general, ABR is used for the evaluation of brainstem function and SEP for the evaluation of thalamocortical function in the brain.
In this study, 3 of the 21 VS patients and 7 of the 10 MCS patients showed recovery of consciousness. All patients who recovered from VS or MCS showed the fifth wave in the ABR and N20 in SEP before SCS therapy. Based on these results, we consider that at least the fifth wave in the ABR and N20 in SEP must be detected by electrophysiological evaluation in order for SCS therapy to be effective in treating VS or MCS.
This study indicated that the timing for starting SCS is also very important. Three patients recovered from VS with SCS treatment, and all of these patients were started on SCS within 8 months after the onset of the initial brain injury and the comatose state. In addition, seven patients recovered from MCS with SCS treatment, and all of these seven patients underwent SCS within 9 months after the onset of the initial brain injury and comatose state. The other VS or MCS patients who showed the fifth wave in the ABR and N20 in SEP, but were treated with SCS 9 months or more after the onset of the initial brain injury and comatose state, did not recover from VS or MCS. Thus, we think that not only electrophysiological evaluation but also the timing of the start of SCS is critical for the treatment of VS and MCS. Although the neurological findings in VS and MCS are quite different, the effective timing for the start of SCS was not very different between the two groups.
Anatomical findings on computed tomography (CT) or magnetic resonance (MR) images are also useful for evaluating severe brain damage, such as bilateral diffuse injury of the thalamus or cerebral cortex; however, it is usually difficult to evaluate resting brain function correctly in the more mildly damaged brain [26]. CBF is usually lower in VS and MCS patients than in normal subjects, and some reports indicate the importance of CBF for the selection of candidates for SCS [11]; however, we must recognize that chronic stage CBF does not always represent the severity of acute brain anoxia.
Long-Term SCS for VS
The Multi-Society Task Force on PVS indicated that recovery of consciousness in post-traumatic VS is unlikely after 12 months, and that recovery from nontraumatic VS after 3 months is exceedingly rare [21, 22]. In our study, three patients recovered from VS following cervical SCS; one head injury patient recovered at 14 months, and two cerebrovascular accident patients recovered at 8 and 12 months after the initial brain injury. Based on the report from The Multi-Society Task Force on PVS, the recovery from VS in our three patients would be classified as rare if the recovery had occurred spontaneously. However, we could not demonstrate definite evidence that the SCS was useful for the recovery of VS patients in this study. Otherwise, we have reported that DBS of the CM-pf complex is useful for the treatment of VS patients when candidates are selected on the basis of an electrophysiological evaluation [25, 26, 28]. If the option of treating VS patients with SCS therapy exists, the fifth wave in the ABR and N20 in SEP should be verified as detectable, and the SCS should be started within 8 months after the initial brain injury.
Chronic DBS of the mesencephalic reticular formation and the thalamic CM-pf complex for the treatment of VS was first reported by Tsubokawa et al. [23, 24] and Chohadon and Richer [2]. Unilateral DBS of the intact side of the thalamic CM-pf complex can induce a very strong arousal response in VS patients [23, 25, 26, 28]. It seems important to increase the arousal level in VS patients for them to recover from the VS [6, 8, 16, 19, 20]. The fact that SCS does not induce an arousal response, although SCS can increase CBF, may be a clear instance of its difference from DBS therapy for VS patients.
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