Fig. 5.1
Evaluation tools for swallowing function. (a) Videofluoroscopy (VFS). Black arrow shows aspirated barium below the vocal cord and arrowhead shows residue in pyriform sinus. (b) Fiberoptic endoscopic evaluation of swallowing (FEES). (1) Epiglottis, (2) esophagus, (3) vocal cord, (4) pyriform sinus, (5) fluid
5.2 Neurophysiology Related to rTMS in Post-stroke Dysphagia
A series of experiments from Hamdy et al. probed the role of the motor cortex in dysphagia after stroke using transcranial magnetic stimulation (TMS). Initial studies in healthy volunteers described how midline swallowing muscles are represented bilaterally in the motor cortex but in an asymmetric manner (Hamdy et al. 1996). This has led to the hypothesis that some subjects have a “dominant” swallowing hemisphere.
It was subsequently postulated that stroke affecting the dominant hemisphere was more likely to result in dysphagia (Hamdy et al. 1997). Twenty patients were recruited after their first stroke and eight of the patients were dysphagic. TMS was delivered to sites over both hemispheres in turn, and any resulting electromyographic (EMG) response at the pharyngeus muscle was recorded. Stimulation of the affected hemisphere produced similarly small EMG responses in both dysphagic and non-dysphagic patients. In contrast, stimulation of the unaffected hemisphere produced significantly smaller responses in the dysphagic patients. Although studied retrospectively, this did indeed suggest that lesions of the dominant hemisphere were more likely to result in dysphagia.
Furthermore, reorganization with increased pharyngeal representation in the non-dominant or unaffected hemisphere appears to be associated with recovery of swallowing function (Hamdy et al. 1998). Twenty-eight post-stroke dysphagic patients were recruited, and their cortical maps in response to TMS of both hemispheres were plotted at 1 week, 1 month, and 3 months after stroke. EMG responses of the thenar muscle were used as a control. The key finding was that dysphagic patients who recovered over time showed an increase in their cortical maps over the unaffected hemisphere at 1 month and 3 months. The patients who remained dysphagic did not show this change in their pharyngeal cortical maps. However, cortical representation of the thenar muscle reappeared in the affected hemisphere.
5.3 Clinical Application of rTMS on Dysphagia After Stroke
Several clinical rTMS studies having the purpose of enhancing the recovery of swallowing function after stroke have been conducted (Table 5.1). The first study was reported in 2009 by Verin et al. (Verin and Leroi 2009). Seven patients with poststroke dysphagia due to hemispheric or subhemispheric stroke for more than 6 months who were diagnosed earlier by videofluoroscopy participated. rTMS at 1 Hz was applied for 20 min per day for 5 days to the healthy hemisphere (focused on mylohyoid muscle) to decrease transcallosal inhibition. Swallowing function was evaluated before stimulation and reevaluated 1 week and 3 weeks after the start of rTMS using VFS and dysphagia handicap index. After rTMS, there was an improvement of swallowing coordination, with a decrease in swallow reaction time for liquids and paste and aspiration score significantly decreased for liquids and residue score also decreased for paste. It is meaningful that this was a first attempt to apply rTMS on poststroke dysphagia, but this study was just a small size clinical trial without controls and they did not use pharyngeal constrictors but the mylohyoid as a target.
Table 5.1
Summary of the rTMS clinical trials for post-stroke dysphagia treatment
Study (year) | Type of study | Number and type of patients | Onset duration | Target | Control | Stimulation parameters | Evaluations | Results | Side effects |
---|---|---|---|---|---|---|---|---|---|
Verin et al. (2009) | A noncontrolled pilot study | Seven patients (3 females, age = 65 ± 10 years) post-stroke dysphagia due to hemispheric or subhemispheric stroke Dx based on VFS | More than 6 months | Contralesional-mylohyoid | None | 1 Hz 20 % above the threshold value for 20 min per day every day for 5 days | The dysphagia handicap index and videofluoroscopy (0, 2 weeks) | The score was 43 ± 9 of a possible 120 which decreased to 30 ± 7 (p < 0.05) There was an improvement of swallowing coordination, with a decrease in swallow reaction time Aspiration and residue score significantly decreased | No |
Khedr et al. (2009) | Randomized controlled study | Twenty-six patients with post-stroke dysphagia due to monohemispheric ischemic stroke, real (n = 14) or sham (n = 12) Dx based on answers to a swallowing questionnaire, confirmed by bedside examination | Acute (5–10 days after stroke) | Lesional -proximal esophagus | Sham-tilted active coil | 10 trains of 3 Hz for 10 min (300 rTMS pulses) at an intensity of 120 % hand motor threshold for five consecutive days | Dysphagia Outcome and Severity Scale, BI, and grip strength were assessed (0, 1, 2 months) The motor-evoked potential (MEP) was assessed (0, 1 month) | Real rTMS led to a significantly greater improvement in dysphagia and motor disability that was maintained over 2 months of follow-up This was accompanied by a significant increase in the amplitude of the oesophageal MEP evoked from either the stroke or non-stroke hemisphere | No |
Khedr et al. (2010) | Randomized controlled study | Twenty-two patients with lateral medullary infarction or another brainstem infarction, active (n = 11) or sham (n = 11) | Acute | Each, both – proximal esophagus | Sham-tilted active coil | 10 trains of 3 Hz for 10 min (300 rTMS pulses) at an intensity of 130 % hand motor threshold for five consecutive days | Dysphagia Outcome and Severity Scale, Barthel Index, NIHSS, and grip strength were assessed (0, 1, 2 months) | Active rTMS improved dysphagia. The LMI group also improved the scores in the Barthel Index All improvements were maintained over 2 months of follow-up | No |
Park et al. (2013) | Randomized controlled study | Eighteen patients with unilateral hemispheric stroke oropharyngeal dysphagia, active (n = 9) or sham (n = 9) Dx based on VFS | More than 1 month | Contralesional -pharyngeal constrictor | Sham-tilted active coil | 10 trains of 5 Hz for 10 min (500 pulses) at intensity of 90 % hand motor threshold for 10 days | Videofluoroscopic dysphagia scale (VDS) and penetration-aspiration scale (PAS) (0, 2 weeks) | VDS and PAS score were decreased | No |
In the same year, Khedr et al. reported a double-blind randomized controlled rTMS trial (Khedr et al. 2009). Twenty-six patients with poststroke dysphagia due to monohemispheric stroke were randomly allocated to receive real (n = 14) or sham (n = 12) rTMS of the affected esophageal cortical area which was taken nearly to be symmetrically opposite the esophagus area of the unaffected hemisphere using a single-pulse motor-evoked potential. Each patient received 10 trains of 3-Hz stimulation at intensity of 120 % hand motor threshold for five consecutive days. Clinical ratings of dysphagia were assessed before and immediately after the last session and then again after 1 and 2 months, and real rTMS led to a significantly greater improvement compared with sham control in dysphagia that was maintained over 2 months of follow-up. Even though they did not use a VFS as an evaluation, it is very meaningful that this study was a randomized controlled trial and they showed long-term follow-up results.