An overview of dysphagia rehabilitation for stroke patients

ABSTRACT Background: Dysphagia is characterized by difficulty in the swallowing pattern at any stage of this neuromuscular process. It is a frequent symptom after stroke. Objective: This study aimed to investigate the most commonly used phonoaudiological interventions as therapy for the treatment of swallowing disorders in patients with dysphagia after stroke. Methods: We performed a review of studies indexed in MEDLINE-PubMed, LILACS, Cochrane, and Clinical trials.gov focusing on speech-language interventions for adult dysphagic patients after stroke between January 2008 and January 2021. Results: Thirty-six articles of clinical trials were selected. Eleven different types of therapies have been studied. Studies on the efficacy of therapeutic interventions for the rehabilitation of adult patients with dysphagia after stroke are still scarce. Most techniques are combined with conventional therapy, so the effectiveness of the other techniques alone cannot be assessed. Conclusions: Therapeutic interventions should be selected in accordance with the possibilities and limitations of the patients, and especially with the findings of the clinical evaluation and with its objective.

Dysphagia after stroke carries the risk of aspiration pneumonia, malnutrition, dehydration, and death 3 . Dysphagia is a major complicating factor in the rehabilitation of such patients or of neurological patients in general. If associated with other risk symptoms such as drowsiness, disorientation or incontinence it may indicate an even worse prognosis 4,5 . Recent studies indicate an average frequency of dysphagia of 50% after stroke. It causes a large increase in hospital costs per patient. Patients with stroke who develop dysphagia have a longer length of hospital stay when compared to not dysphagic patients, requiring additional care for enteral diets and are more likely to need home care after discharge 6 .
Considering the need for early intervention for dysphagia in post-stroke patients to improve their quality of life and reduce sequelae, complications, hospital costs and hospitalization time, it is necessary to find effective treatment interventions. The objective of this study was to investigate the most commonly used phonoaudiological interventions as therapy for swallowing disorders in patients with dysphagia after stroke. In this review, we provided the most relevant information of dysphagia treatment after stroke published in recent years.

MeTHOdS eligibility criteria
Studies were selected according to predefined inclusion and exclusion criteria. "English-language full-text articles on clinical and controlled trials indexed in the previously selected electronic databases with adult populations presenting with oropharyngeal dysphagia as a symptom after stroke" was defined as inclusion criteria. Studies involving (1) pediatric population, (2) analysis of the application of evaluation protocols, (3) studies aiming at decannulation of tracheotomized patients, (4) studies involving esophageal dysphagia, and (5) studies in which the primary outcome was not related to the degree of dysphagia and improvement of the swallowing pattern were excluded.

Review question
The guiding question for the research was: "What interventions are reported as effective treatments for the rehabilitation of adult patients with dysphagia after stroke?".

Search strategy, study selection and data extraction
A review of articles published between January 2008 and January 2021 in indexed scientific journals was carried out in the following electronic databases: MEDLINE-PubMed, LILACS, Cochrane, and Clinical Trials.gov. The selection of descriptors was performed through consultation in a Brazilian platform for descriptors in health sciences (DeCS -Descritores de Ciências em Saúde). The selected English descriptors were: "dysphagia" AND "therapy" AND "stroke".
The articles were selected based on the screening of titles or abstracts. However, when title, keywords, and abstract did not have sufficient information to determine the inclusion according to the established criteria, a full-text review was conducted. After that, all the remaining papers were fully read, evaluated, and cataloged. All steps in this study were performed independently by two researchers following the protocol described above. Individual results were assessed and compared, and a consensus was reached through discussion.
The following data were extracted after the assessment of full text of all selected articles: country, number of patients, study design, outcome measures, types of intervention groups, intervention time, summary of the results, and conclusions. These data were then compiled into a standard table.

ReSULTS
The search identified 154 references (117 in MEDLINE-Pubmed, 31 in Cochrane, 3 in Clinical trials, and 3 in LILACS) of which 90 were excluded based on the title and 4 were duplicates. Therefore, 60 studies were selected for inclusion according to their titles and abstracts, of which 38 clinical trials that met the inclusion criteria were included in this review. A flow diagram showing the study selection process is presented in Figure 1.
All included studies evaluated patients diagnosed with stroke. A total of 12 different therapies have been studied with a variety of study designs: [1] 44 .
Even among studies focusing on the same type of therapy a wide variety of outcome measures were found to assessing dysphagia. The sample sizes varied from 4 22 to 250 40 . More than half of the studies were from Asia, but some were from Europe and North America.
The following sections present a summary of the articles' results by type of interventions.

electrotherapy (nMeS)
Electrotherapy is a technique that can be used with motor stimuli, sensorial stimuli, or both. In addition, depending on the muscular function affected in the swallowing process and the degree of this change, variations in intensity, electric current pulse duration, electrodes number and position are applied. Despite all these factors, there is still little scientific evidence of the effectiveness of electrotherapy in improving the swallowing pattern in oropharyngeal dysphagia, especially when this technique is associated with conventional exercise therapy.
The Neuromuscular Electrical Stimulation (NMES) technique combined with Endoscopic Evaluation of Swallowing (EES) and traditional swallowing rehabilitation improved the swallowing quality in a study involving thirty-two patients with moderate to severe post-stroke dysphagia. In addition, patient satisfaction was high and there were no serious adverse events. Thus, the implementation of this promising combination in clinical practice was recommended 7 . Similarly, the effects of applying sensory-level electrical stimulation (SES) on masseter muscles in patients with acute stroke were evaluated in another study 8 . Applying SES (based on its oral and pharyngeal functions) on masseter muscles and using SES to generate cortical reorganization was effective in treating dysphagia in stroke patients.
In another study 17 , selected patients were randomly assigned to a VitalStim electrotherapy group, a conventional swallowing therapy group, and electrotherapy plus conventional therapy group. The results suggested that VitalStim combined with conventional therapy is capable of improving dysphagia after stroke. Xia et al. 18 also evaluated the effects of VitalStim in their patients and confirmed its effectiveness. A limitation of this study, however, was the absence of a placebo stimulation group.
The combined application of electrical stimulation and conventional therapy in patients with acute oropharyngeal dysphagia secondary to acquired brain injury 9 resulted in better outcomes than when conventional therapy with placebo stimulation was adopted. A study conducted by Rofes et al. 10 evaluated and compared the efficacy and safety of a 10-day surface electrical stimulation (e-STIM) treatment in sensory and motor intensities in patients with chronic oropharyngeal dysphagia after chronic stroke. This study showed that e-STIM is a safe and effective therapy to improve swallowing. However, further investigation involving a control group, a larger number of patients, a prolonged follow-up, and the effect on clinical outcomes is needed to confirm the clinical utility of this therapy. Konecny and Elfmark (2018) showed that after four weeks of standard therapy with suprahyoid muscles electrical stimulation, the duration of oral and pharyngeal transit time was statistically improved 11 . In another study, electrical stimulation associated with conventional therapy was performed. Electrodes were placed adjacent to the suprahyoid and upper and lower parts of the thyroid, in the geniohyoid region, and in the mylohyoid region. When compared to conventional therapy, a significant improvement was noted. However, the position of electrodes did not generate significant differences 12 .
Another study investigated the effects of forced swallowing combined to neuromuscular electrical stimulation on the hyoid bone movement and on the swallowing function in stroke patients 13 . The experimental group showed an increase in the anterior and superior movement of the hyoid bone and an improvement in the pharyngeal phase swallowing function. The neuromuscular electrical stimulation combined with thermal-tactile stimulation were found to be a better treatment for patients with deglutition disorders after stroke than isolated thermal-tactile stimulation therapy 14 .
Electrical stimulation was performed by Park et al. 15 using two sets of electrodes placed in the segmentation area of the infrahyoid and sternum-hyoid muscles. When using sensorial EE with forced swallowing, no significant improve was observed in any of the evaluated parameters. However, the studied methodology can only be applied to selected patients, as many patients with dysphagia fail to elevate the hyolaryngeal complex during motor electrical stimulation.
The effects of NMES associated with electromyographic biofeedback (EMG-BF) were also investigated 19 . EMG-BF is known to be an effective therapy for stroke rehabilitation. In this pilot study, all subjects received NMES combined with EMG-BF in the suprahyoid area. The results demonstrated that NMES combined with EMGBF had the potential to improve oropharyngeal swallowing in stroke patients with dysphagia.
In a more recent study, the effects of neuromuscular transcutaneous electrical stimulation (NMES) in 33 patients affected by dysphagia after sub-acute stroke were evaluated. Both groups showed improvements 16 . Another recent study analyzed the McNeill's dysphagia therapy (MDTP) with NMES for the treatment of post-stroke dysphagia 20 . MDTP showed a greater positive change than the NMES group, including increased oral intake and improved functional outcome three months after the stroke. These data support the inclusion of intense short-term behavioral interventions for an efficient allocation of resources for acute stroke rehabilitation.
Studies that used electrotherapy as a therapeutic approach are detailed in Table 1.

neuromodulation
The nervous system has the ability to modulate and modify itself in response to external stimuli. The term neuromodulation has been used to describe procedures in which electrical stimulation is applied directly to structures of the nervous system for therapeutic purposes. A summary of these approaches is shown in Table 2.

Repetitive Transcranial Magnetic Stimulation
Repetitive Transcranial Magnetic Stimulation (rTMS) has been proposed as an alternative treatment for dysphagia after stroke. It is a noninvasive technique that modulates brain activity using electromagnetic induction and thus induces physiological changes. An advantage of rTMS is that patients do not need to be actively engaged during treatment 21 .
One of the included studies indicated that 5 Hz rTMS applied over the tongue area of the motor cortex for 10 days was not effective in improving the swallowing function in patients with stroke and chronic dysphagia. However, given he small and unbalanced sizes of the groups in this study, the therapeutic effects of the protocol remain uncertain 21 . Another study also evaluated the therapeutic effect of 5 Hz high-frequency rTMS on the unaltered pharyngeal motor cortex in 4 poststroke dysphagic patients. In disagreement with the previous study, the authors indicated that 5Hz high-frequency rTMS applied to the tongue region of the motor cortex may be beneficial for patients with dysphagia after hemispheric unilateral stroke and with dysfunction in the swallowing phase. Further investigations with larger samples are required to support the benefit of this protocol 22 . Finally, a study of 40 patients showed that the use of high frequency (3 Hz) and low frequency (1 Hz) rTMS improved dysphagia (after 5 days) more than the simulated group, with the effects remaining for at least 3 months after the intervention 23 .
tDCS is a non-invasive brain stimulation method based on the principle of neuroplasticity. It provides a constant lowintensity electric current between the anode and the cathode applied to the scalp area associated with the segmentation of the cerebral cortex. In general, cathodic tDCS decreases cortical excitability and anodic tDCS increases cortical excitability 29 . Recently, noninvasive cortical stimulation has been used to improve neural plasticity and treat hemiplegia and aphasia. However, little is known about the possible effects of tDCS on swallowing function 30 , and few studies were conducted on the mater.
The association of the tDCS technique with conventional therapy was evaluated in patients with chronic post-stroke dysphagia. Although the result of this study shows that the bihemispheric anodic tDCS group did not have a statistically superior improvement compared with the control group, the detailed dysphagia outcome scale (using videofluoroscopy), patient symptom report, or patient and caregiver satisfaction may reflect the clinical improvement of dysphagia 29 . The study conducted by Shigematsu et al. 30 investigated the effects of cerebral pharyngeal cortex noninvasive stimulation combined with intensive swallowing therapy on dysphagia recovery and found that the combined therapies effectively improve poststroke dysphagia compared to isolated therapy.
Krueger et al. 31 evaluated patients with acute and dysphagic stroke that received contralesional anode stimulation or placebo tDCS for 4 consecutive days. Applying objective instrumental diagnosis in parallel with functional neuroimaging, a greater improvement in the swallowing function was observed after tDCS compared with the placebo intervention. Thus, tDCS seems to be a safe and beneficial therapeutic option for patients with oropharyngeal dysphagia during the early stage of stroke.

Pharyngeal electrical stimulation (PeS)
In one of the included studies, PES interventions were performed at the bedside. The effects of PES on dysphagia in stroke patients remained inconclusive because the recruitment goal was smaller than predicted. Despite this, there is an indication for the use of this treatment considering some potentially favorable results, such as the observed improvement in the number of safe swallows. In addition, PES was well tolerated without any adverse effects 25 . In another study with the same objective, it was found that PES did not reduce radiological aspiration or clinical dysphagia 24 .  In addition, there are currently a wide variety of candidate genes that can be studied in the context of brain plasticity and response to PES. BDNF is the most abundant growth factor in the brain and is involved in long-term brain plasticity. It has attracted much interest and is considered a candidate for neurological and swallowing function recovery in patients treated with electrical stimulation of the pharynx 26 . The study conducted by Essa et al. 26 aimed to test the possible influence of a single but common BDNF polymorphism on the functional recovery in a population with dysphagia after stroke. An association between the Val66Met BDNF allele and level of swallowing recovery was observed when pharyngeal stimulation was performed. On the other hand, the BDNF showed no correlation in the simulated group, suggesting that such genetic polymorphisms may be less relevant in natural recovery than in treatment-induced recovery.
A summary of studies using the pharynx electrostimulation technique is shown in Table 3.

Tongue pressure resistance exercise and precision training
Tongue function can affect both the oral and the pharyngeal stages of the swallowing process. Adequate tongue strength is vital for safe oropharyngeal swallowing. Table 3 has a summary of the studies on tongue pressure resistance exercises and precision training.
Kim et al. 42 investigated the effect of tongue-pressure resistance training (TPRT) on tongue strength and oropharyngeal swallowing function in patients with stroke and dysphagia. The results showed that TPRT increased tongue muscle strength and improved swallowing function in patients with post-stroke dysphagia. This study also confirmed that TPRT improved the oral and pharyngeal phases of deglutition. Therefore, TPRT is recommended as an easy and simple rehabilitation strategy to improve swallowing in patients with dysphagia. However, these results do not reflect a pure TPRT effect, as this therapy was conducted in conjunction with conventional therapy 42 . Another study published the following year aimed to investigate the effects of tongue pressure strength and accuracy training (TPSAT) on tongue pressure strength and its ability to improve quality of life in patients with dysphagia after stroke. TPSAT consisted of an isometric exercise of anterior and posterior tongue strength and an isometric tongue precision exercise. TPSAT combined with traditional therapy improved outcomes compared to pre-intervention levels 41 .

CTaR exercise
Recently, CTAR (Chin Tuck Against Resistance) exercise has been reported as a treatment for pharyngeal dysphagia. However, clinical evidence of its effect is still unclear. Park et al. 32 investigated the effect of CTAR on the swallowing function in patients with dysphagia after subacute stroke and found that the exercise improved swallowing.
Game-based CTAR was also proposed 34 . The experimental group performed game-based CTAR, while the control group performed traditional head lifting exercises. The LES 100 (Cybermedic Inc., Iksan in South Korea) consists of a tablet screen, a resistance bar, and a Bluetooth connector, and it implements a game-based exercise in which the chin is tucked down against a bar in order to strengthen suprahyoid muscles. The game-based CTAR not only has a similar effect on the swallowing function of patients with dysphagia as the lifting exercise, but is also a less rigorous, more enjoyable and interesting rehabilitation method.
Because the CTAR involves hand-holding a device, physically weak patients may find it difficult. A study investigated the effect of modified CTAR (mCTAR) in patients with poststroke dysphagia 35 and found that it reduced aspiration and improved nutritional levels of patients. I can thus be assumed that the mCTAR is beneficial for physically vulnerable patients with dysphagia who have limited hand strength and movement.
The aim of the study was to investigate the effect of jaw opening exercise (JOE) and hyoid bone movement compared to head lifting exercise, or Shaker exercise (HLE) in patients with dysphagia after stroke. The JOE/CTAR group performed an exercise using a resistance bar. The Shaker group performed traditional exercises. The total duration of the intervention was 6 weeks. The thickness of the digastric and mylohyoid muscles was measured by ultrasound. The CTAR and Shaker had similar effects in increasing the thickness of the suprahyoid muscle and improving the movement of the hyoid bone. However, CTAR required less perceived effort than Shaker 36 .

Shaker exercise
The Shaker exercise (SE) has been considered a popular rehabilitation training for dysphagia 33 . This is an isometric and isotonic exercise based on the upward and forward movement of the larynx structures resulting from the traction of the thyroid, mylohyoid, and geniohyoid muscles and the anterior belly of the digastric muscle. First, patients perform 3 head raises for 60 s in a supinated position without movement; there is a 60 s pause between the elevations. Next, participants perform 30 repeated head raises in the supine position. Participants raise their head high enough to observe the toes without raising the shoulders 37 .
Gao & Zhang 33 compared the effects of Shaker exercises, CTAR and conventional exercises on dysphagia and psychological status. Traditional rehabilitation included tongue exercises such as tongue extension movement and mouth exercises such as mouth opening, teeth clicking, and voluntary swallowing. The main conclusion of this study was that the CTAR exercise has a similar effect on improving swallowing function as the Shaker exercise. However, the rehabilitation effect of CTAR exercises on dysphagia should be more explored in younger patients with stroke, since all patients assessed in this study were 60 years old or older.
Choi et al. 37 investigated the effects of the Shaker exercise on aspiration and oral diet level in stroke survivors with dysphagia. This study suggested that the SE is an effective exercise for swallowing function recovery in stroke survivors, reducing aspiration and improving oral diet level. As aspiration severity is closely related to the feeding tube and to the oral diet level, the results of this study indicate that performing SE can lead to tube withdrawal in stroke survivors with dysphagia. Some limitations, such as a relatively small sample, no follow-up after the intervention, and failure to observe long-term effects prevent the results of this work from being generalized.
Important data from the articles about CTAR and SE are shown in Table 4.

Modified jaw opening exercise (MJOe)
The viability and effectiveness of a new method (modified jaw opening exercise -MJOE) for promoting anterior displacement of the hyoid bone during swallowing was studied. The MJOE differs from the conventional JOE, in which an upward vertical resistance is applied to the jaw while the mouth is closed with the tongue held in the swallowing tilting position to prevent mouth opening. In the MJOE, surface electrodes connected to the sternohyoid muscle in the mandibular midline were connected to the biofeedback equipment. The results showed that MJOE is feasible in elderly post-stroke patients, without adverse events and promotes anterior displacement of the hyoid bone during swallowing 43 .

Mendelsohn maneuver
The Mendelsohn maneuver, a voluntary prolongation of laryngeal elevation during swallowing, has been widely used as a compensatory strategy to improve the opening of the upper esophageal sphincter (UES) and bolus flow. When used as a rehabilitation exercise, it significantly improves the duration of the hyoid movement and the duration of the UES opening 27 .
McCullough et al. 28 performed a research to determine if the intensive exercise using the Mendelsohn maneuver would improve swallowing physiology. The Mendelsohn maneuver, used as a rehabilitation exercise, improved the duration of the anterior and superior maxillary movement of the hyoid and the duration of the UES opening. With a similar goal, McCullough et al. 27 stated that it seems possible that the use of the Mendelsohn maneuver as a rehabilitation exercise may have a greater impact on swallowing durations than on structural movements. Changes in the coordination of structural movements with duration measures, however, require further investigation. When the Mendelsohn maneuver was used as a compensation mechanism, duration measures also appeared to be more affected than measures of structural movements. Thus, the data reported in this research support the use of the Mendelsohn maneuver as an exercise to improve the swallowing physiology 27 .
A synthesis of the results discussed above is shown in Table 5.
acupuncture Acupuncture is a simple, inexpensive, primary medical procedure that has been widely used in China and other parts of East Asia for many years. Needles are inserted at acupuncture points to produce a "qi" response in which the patient feels pain or heaviness in the area around the needle 38 .
Xia et al. 38 evaluated the effect of acupuncture on swallowing function in patients with dysphagia after stroke. The intervention group received standard therapy and acupuncture and the control group received only standard therapy. Although it was concluded that acupuncture combined with conventional swallowing therapy may be beneficial, the study had a significant limitation due to the lack of a control group for acupuncture alone. In addition, short-term evaluation and lack of follow-up were factors that prevented the evaluation of a long-term therapeutic effect.
Another study found that acupuncture combined with swallowing therapy can improve the swallowing function in poststroke patients 39 . The study conducted by Mao et al. 39 proved that acupuncture in combination with standard swallowing therapy was effective for post-stroke dysphagia, corroborating the findings presented by Xia et al. 38 . However, several limitations prevent this conclusion from being generalized, so it cannot be said that acupuncture alone is capable of providing a high level of rehabilitation.
A similar study was conducted by Chen et al. 40 . This study has shown that acupuncture is safe and has several additional effects in improving neurological deficits, swallowing disorder, cognitive impairment, and lower limb function. However, no significant improvement in the upper limb function was observed during this short-term study.
A summary of the results in the articles using acupuncture techniques is shown in Table 5.

Cervical isometric exercises
Cervical isometric exercises to improve dysphagia and cervical spine malalignment was applied in 70 patients in a randomized controlled trial. The exercises were carried out in all 4 directions (by placing their hand or the hand of their personal assistant on their head and contracting their neck muscles under forward-backward-sideward resistance). Swallowing was improved in the experimental group compared to the control group 44 .

diSCUSSiOn
The purpose of this review was to assess recently studied therapies for dysphagia rehabilitation. Numerous studies of a wide range of interventions were included. However, they differed not only in terms of the therapy conducted, but also in terms of sample size, outcome measurement methods, intervention times and follow-up time. These differences presented a challenge to combine and summarize the results, and to compare and define which is the most effective treatment for post-stroke dysphagia. Table 3. Interventional clinical studies using electrostimulation of the larynx, tongue pressure resistance exercise and precision training for patients after stroke.    Considering that this neuromuscular process is complex and involves dozens of muscles and six pairs of cranial nerves, there are many symptoms that affect a dysphagic individual. Therefore, it is difficult to elaborate a single exercise protocol (in the case of conventional therapy) that will effectively improve the condition. Scientific evidence highlights the benefits of conventional therapy in improving the swallowing pattern of a dysphagic individual. However, the search for new therapeutic techniques that can increase this benefit is constant.

References
Studies on the efficacy of therapeutic interventions for rehabilitation of adult patients with dysphagia after stroke are still limited. Most techniques are used in combination with conventional therapies, which makes measuring the efficacy of other techniques alone inconclusive. Among the reviewed therapies, electrotherapy, associated or not with conventional therapy, was the most frequently used. In both cases, it proved to be a method with significant results for the rehabilitation of dysphagia. Similarly, neuromodulation applied in areas such as the motor cortex of the tongue and pharynx, as mentioned in the included studies, also lead to an improvement in the swallowing pattern. Tongue pressure resistance exercises and precision training, the Shaker exercise and acupuncture also showed significant results for rehabilitation.
Neuromodulation is not a possibility in many healthcare institutions that admit patients with acute stroke, making this therapy technique difficult to access, especially for low-income patients. An advantage of the SE is that it is a non-invasive therapy, does requires no any additional cost or equipment and can be easily performed at the bedside with the assistance of a caregiver 37 . However, a limitation of the SE is that coordinated movements and resistance are required, and many patients in the acute phase of stroke do not have this capability. Pharyngeal electrical stimulation (PES) is also considered a promising treatment for dysphagia after stroke. However, the results of the studies included in this review are contrary to this. With regard to tongue pressure resistance exercise, it is important to emphasize that isometric and isotonic exercises are commonly used in conventional therapy to improve the amplitude and increase the force of tongue movements. The tongue is an essential organ for the proper functioning of the safe swallowing process.
The majority of the studies used videofluoroscopy of swallowing as the gold standard evaluation method. The method allows the swallowing dynamics to be visualized from the preparatory phase to the opening of the upper esophageal sphincter. It is also possible to identify the tracheal aspiration, laryngeal penetration, and oral and pharyngeal residues, which is important for a detailed analysis of the various changes that may occur in a dysphagia disorder of any degree. Videofluoroscopy helps in selecting the most appropriate technique and therapeutic plan to improve the swallowing pattern. Ideally, this examination should be available in all health centers admitting patients in the acute phase of stroke.
In conclusion, this review highlights the main interventions for dysphagia of patients after stroke. Among the techniques used, conventional therapy remains the best strategy, achieving positive results alone or combined with various rehabilitation therapies. However, greater consistency between science and clinical practice is needed to allow a comparison between different techniques. Dysphagia is a potentially treatable symptom in post-stroke patients and deserves attention, and its treatment may increase patients' quality of life. In addition, even if conventional therapy is empirically considered essential for the rehabilitation process, its effect would be strengthened by studies that scientifically support this technique.