Dysphagia

Evidence Reviewed as of before: 18-01-2017
Author(s)*: Katie Sharpe MHSc Student; Dr. Rosemary Martino, MSc PhD; Dr. Nicol Korner-Bitensky, PhD OT; Tatiana Ogourtsova, PhD Cand MSc BSc OT
Patient/Family Information Table of contents

Introduction

A swallowing disorder (dysphagia) is characterized by difficulty or discomfort in swallowing. The difficulty typically arises while ingesting foods and/or liquids. Swallowing disorders following stroke are common, affecting 22% to 65% of patients, and may persist for many months. Swallowing disorders require immediate attention and if ignored may result in serious morbidity or even mortality, especially when identified in patients with acute stroke.

Ramsey D.J.C., Smithard D.G., Kalra L. (2003). Early Assessments of Dysphagia and Aspiration Risk in Acute Stroke Patients. Stroke. 34;1252-1257.

Patient/Family Information

Authors*: Rosemary Martino, MSc PhD; Katie Sharpe MHSc (student)

What is a swallowing disorder?


A swallowing disorder (also called dysphagia) is difficulty or discomfort in swallowing. As a result, it can be difficult to eat and drink. When eating, food is placed in the mouth and is then chewed with the teeth to form a compact ball or bolus. Once the bolus of food is formed, the tongue moves the bolus to the back of the mouth. At this point, the swallow is automatically triggered by the brain. The muscles of the back of the tongue and the throat (also called pharynx) squeeze to move the bolus of food through the pharynx and down a tube called the “esophagus”. At the end of the tube, the bolus reaches the stomach. Drinking liquids is very similar to eating foods. The main difference is that when drinking liquids, a bolus of liquid is formed without the need to chew. During both drinking and eating, an important step in swallowing is the automatic closure of the airway or windpipe when the bolus passes through the throat. This closure of the airway prevents food or liquid from going into your lungs. Swallowing difficulties can occur at any point along the swallow, from when the food or drink enters the mouth, to when the bolus passes through the esophagus and into the stomach. The following are examples of common swallowing difficulties along different points of the swallow:

  • In the mouth:

    • If the lips are not able to close firmly, the food or liquid may drool from the mouth.
    • If the tongue is unable to move around the mouth, there may be food left in the mouth after the swallow.
  • In the throat:

    • If the airway to your lungs is not closed off tightly, food or liquid may accidentally spill into the lungs. This is referred to as “aspiration”. Extended amounts of aspiration can cause a lung infection, such as pneumonia.
    • If the muscles of the throat are unable to squeeze the bolus (food or liquid) down into the esophagus, there may be food or liquid left over in the throat after the swallow.
  • In the esophagus:

    • If the muscles at the top of the esophagus are weak, food may come back up from the esophagus to the throat. This will cause food to remain in the throat after the swallow.
    • If the muscles at the bottom of the esophagus are weak, food may come back up from the stomach. This may create pain in the chest and/or a bad acidic taste in the mouth.

How frequent are swallowing disorders?

Swallowing disorders following a stroke are common. Approximately 55% of people who have a stroke have swallowing difficulties during the first days and weeks. Many people regain their swallowing ability within the first month after the stroke. However, around three months after a stroke, as many as 35% of people still have some swallowing difficulties.

What causes swallowing disorders after a stroke?

Swallowing difficulties are caused by damage to the brain. The specific swallowing difficulties vary according to the specific area of the brain affected.

  • If the area of the brain that controls muscle movements is affected, then it may be difficult to trigger the muscles of the lips, cheek, tongue, throat, or esophagus to move the bolus. If the area of the brain that controls sensation is affected, then it may be difficult to taste flavors, feel different textures, or identify the temperature of foods or drinks.
  • Certain medications that treat important illnesses may also cause swallowing difficulties. For example, some medications may decrease saliva production thereby creating a dry mouth. If the mouth is dry, it is very difficult to form a bolus of food.
  • The lack of teeth may also cause swallowing difficulties. For example, loose dentures make it difficult to chew foods.
  • Inability to move the hand or fingers after a stroke may cause difficulties in directing food or liquid to the mouth for swallowing.

Can swallowing disorders caused by a stroke be treated?

Yes. In most cases, swallowing disorders can be treated or at least managed. There are a variety of helpful strategies and procedures depending on the cause of the problem. These include behavioural interventions (described below), use of special devices such as spill-proof cups or spoons, medications, and surgery. The information provided here is specific to rehabilitation – and does not include a discussion of surgery or medication. Medication and surgery may be used to treat some swallowing difficulties, and you should discuss this with your physician. There are three main reasons why it is important to treat swallowing difficulties after a stroke:

  • to make sure that your nutritional and hydration (liquid intake) requirements are being meet;
  • to prevent aspiration-related complications, such as pneumonia;
  • to maximize the enjoyment that comes from eating and drinking.

If swallowing difficulties are related to your inability to cut and manage your food because you have difficulty using one hand, specific functional interventions will be needed. For example, you may benefit from specialized utensils to help place foods or liquids in your mouth. Alternatively, assistance with feeding may be necessary by a family member, therapist, or nurse. It is important to know that swallowing problems can be treated or controlled no matter the cause. Don’t be afraid. Talk to your doctor or nurse OR have someone talk to him or her for you. They will be able to help you find the best treatment for your specific problem.

What are behavioural interventions?

Behavioural interventions for swallowing disorders after a stroke include: Safe eating strategies: Self-feeding is strongly encouraged whenever possible. Whether you are an independent eater or you require assistance, there are a number of helpful strategies that can be used to increase swallowing safety:

  • if you require eye-glasses, hearing aids, and/or dentures, ensure that you are wearing these at mealtime;
  • eat and drink only when you are fully alert;
  • sit in an upright position, with your torso at a 90° angle to the ground (pillows can be used to support you);
  • eat slowly and allow adequate time for swallowing between bites or sips;
  • take small mouthfuls (teaspoon size);
  • never combine liquids and solids in the same bite;
  • place food on the strong side (the side less effected by the stroke) of the mouth;
  • take 2 or more swallows per bite to ensure food is cleared from the mouth and throat;
  • try not to talk while chewing or swallowing – save conversation for between bites;
  • stay sitting upright for at least 30 minutes after the meal to help food move down into the stomach;
  • if you are having swallowing difficulties, it is a good idea to eat while family and other care-givers (nurses, friends who are visiting) are nearby to supervise you and help you eat safely.

Optimum eating environment: An ideal environment for eating is one that is calm with minimal noise and distractions, and has good lighting. Changes in head posture: There are a number of helpful swallowing postures for your head that may be recommended to you. For example, if one side of your throat is weaker than the other, it may help to turn your head towards the weaker side when swallowing, as this directs the food down your stronger side. Changes in the texture or thickness of food and drink: The following are some of the diet textures that may be recommended to you:

  • pureed food (e.g., applesauce, yogurt, and mashed potatoes);
  • minced or ground food (e.g., meatloaf, shepherd’s pie, and cottage cheese);
  • soft or easy to chew food;
  • soup and drinks that have been thickened to a nectar-like, honey-like, or pudding-like consistency.

These texture recommendations are usually made following a swallowing assessment performed by a health professional with expertise in swallowing disorders. These recommendations will be discussed with you and your family. Avoidance of certain foods:

  • “Dry particulates” or foods that are dry and come in small pieces (e.g., corn, peas, dry rice, noodles, dry cookies, nuts, raisins, hard candies, etc.), as these are difficult to chew;
  • Bread products and peanut butter, as these can stick in your throat;
  • Spicy and acidic foods (e.g., fried food, coffee, tea, cola, and chocolate), as they promote acid reflux.

Oral muscle exercises: Exercises to strengthen the lips, tongue, and jaw may help to increase your ability to chew and control the movement of food in your mouth. Your therapist should show you these exercises and practice them with you. Swallow maneuvers: There are a number of special maneuvers that can help to improve your swallow. Some maneuvers may not be safe for stroke survivors as they temporarily increase your blood pressure. Ask your speech-language pathologist or other members of your healthcare team if there are any swallow maneuvers appropriate for you. Proper oral hygiene: Ensure that after every meal your mouth is cleaned of all food that may have gotten stuck in your teeth or dentures. Also, your mouth should be kept moist at all times.

Are behavioural interventions effective for swallowing disorders?

Experts have researched the effectiveness of behavioural interventions for swallowing disorders. Some of these studies have shown promising outcomes. Here is a brief overview of what we know:

  • Changes in posture: One study looked at patients who aspirated when eating in the upright position. Significant improvement was achieved in some patients by adjusting the position of their head and neck when swallowing. So, as mentioned earlier it may help to turn your head towards the weaker side when swallowing, as this directs the food down your stronger side.
  • Changes in the texture or thickness of fluids: Studies have shown that thickening fluids to a honey or milkshake texture may successfully reduce the risk of aspiration, and so, the risk of pneumonia. However, studies have also shown that people placed on a modified texture diet (where your drinks are thickened) have a higher risk of dehydration from not taking in enough regular liquids. Therefore, it is critical that a proper swallowing assessment be conducted to determine the need for this treatment.
  • Combined Behavioural Strategies: Studies have looked at treatment involving a combination of the strategies we have discussed, including oral muscle exercises, changes in posture, and modified texture diets. The results suggest that this combination is helpful for better and safer swallowing and nutrition.

Clinician Information

Note: When reviewing the findings, it is important to note that they are always made according to randomized clinical trial (RCT) criteria – specifically as compared to a control group. To clarify, if a treatment is “effective” it implies that it is more effective than the control treatment to which it was compared. Non-randomized studies are no longer included when there is sufficient research to indicate strong evidence (level 1a) for an outcome.

There are many interventions pertaining to the treatment of dysphagia following stroke. This module focuses on treatments that include: oral or pharyngeal stimulation, electrical stimulation, tactile-thermal application, olfactory stimulation, biofeedback, lingual exercises and swallowing training. Studies were excluded from the module based on one or a combination of the following criteria: a study that is not a randomized clinical trial (RCT), a RCT where both groups received the same type of treatment with variable intensities between groups, a RCT where the intervention involves a nasogastric (NG) tube feeding and/or percutaneous endoscopic gastrostomy (PEG), a RCT where the intervention is of pharmacological nature, and a RCT where the population is comprised of less than 50% of patients with stroke. Moreover, studies pertaining to compensatory-type of interventions (e.g. texture modification) were excluded from this module.

To date, 27 studies have investigated the effectiveness of remedial-type interventions available to treat those with identified swallowing disorders, including oral electrical stimulation, swallowing exercises, acupuncture and olfactory stimulation. Sixteen  studies are high quality RCTs and 11 studies are of fair quality.

Results Table

View results table

Outcomes

Acute phase - Acupuncture

Functional independence
Effective
1b

One high quality RCT (Xia et al., 2016) investigated the effect of acupuncture on functional independence in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive acupuncture + standard swallowing training or standard swallowing training alone. Functional independence was measured by the modified Barthel Index at baseline and at post-treatment (4 weeks). Significant between group differences in functional independence were found at post-treatment, favoring acupuncture with standard swallowing training vs. standard swallowing training alone.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that acupuncture with standard swallowing training is more effective than standard swallowing training alone in improving functional independence in patients with acute stroke and subsequent dysphagia.

Functional severity of dysphagia
Effective
1b

One high quality RCT (Xia et al., 2016) investigated the effect of acupuncture on functional severity of dysphagia in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive acupuncture + standard swallowing training or standard swallowing training alone. Functional severity of dysphagia was measured by the dysphagia Outcome and Severity Scale at baseline and at post-treatment (4 weeks). Significant between-group differences in functional severity of dysphagia were found at post-treatment, favoring acupuncture with standard swallowing training vs. standard swallowing training alone.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that acupuncture with standard swallowing training is more effective than standard swallowing training alone in improving functional severity of dysphagia in patients with acute stroke and subsequent dysphagia.

Swallowing function
Effective
1b

One high quality RCT (Xia et al., 2016) investigated the effect of acupuncture on swallowing function in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive acupuncture + standard swallowing training or standard swallowing training alone. Swallowing function was measured by the Standardized Swallowing Assessment at baseline and at post-treatment (4 weeks). Significant between-group differences in swallowing function were found at post-treatment, favoring acupuncture with standard swallowing training vs. standard swallowing training alone.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that acupuncture with standard swallowing training is more effective than standard swallowing training alone in improving swallowing function in patients with acute stroke and subsequent dysphagia.

Swallowing related quality of life
Effective
1b

One high quality RCT (Xia et al., 2016) examined the effects of acupuncture on swallowing related quality of life in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive acupuncture + standard swallowing training or standard swallowing training alone. Swallowing related quality of life was measured with the Swallowing Related Quality of Life scale at baseline and at post-treatment (4 weeks). Significant between-group differences in swallowing related quality of life were found at post-treatment, favoring acupuncture with standard swallowing training vs. standard swallowing training group.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that acupuncture with standard swallowing training is more effective than standard swallowing training alone in improving swallowing related quality of life in patients with acute stroke and subsequent dysphagia.

Acute phase - Acupunture & neuromuscular electrical stimulation (NMES)

Swallowing function
Effective
2a

One fair quality RCT (Zhao et al., 2015) investigated the effect of combined acupuncture and neuromuscular electrical stimulation (NMES) on swallowing function in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive acupuncture + NMES or acupuncture alone. Swallowing function was measured by Kubota’s water test at baseline and post-treatment (2 weeks). A significant between-group difference in change in swallowing function from baseline to post-treatment was seen, in favour of acupuncture + NMES vs. acupuncture alone.

Conclusion: There is limited evidence (Level 2a) from 1 fair quality RCT that acupuncture and NMES is more effective than acupuncture alone in improving swallowing function in individuals with acute stroke and subsequent dysphagia.

Acute phase - Oral care

Microbiological growth
Not effective
2a

One fair quality RCT (Chipps et al., 2014) investigated the effect of oral care on growth of Staphylococcus aureus in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive a standardized oral care program (i.e. timed tooth brushing with a battery powered toothbrush, tongue brushing, flossing, mouth rinse, and lip care performed twice daily by trained nurse) or usual oral care as per hospital policy. Growth of S.aureus was measured by a microbiological swab sample test at baseline and at post-treatment (10 days). No significant between-group differences in microbiological growth were found at post-treatment.

Conclusion: There is limited evidence (Level 2a) that a standardized oral care program is not more effective than usual oral care in preventing microbiological growth in patients with acute stroke and subsequent dysphagia.

Nutritional status
Not effective
2a

One fair quality RCT (Chipps et al., 2014) investigated the effect of oral care on nutritional status in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive a standardized oral care program (i.e. timed tooth brushing with a battery powered toothbrush, tongue brushing, flossing, mouth rinse, and lip care performed twice daily by trained nurse) or usual oral care as per hospital policy. Nutritional status was measured by the Functional Oral Intake Scale (FOIS) at baseline and at post-treatment (10 days). No significant between-group differences in nutritional status were found at post-treatment.

Conclusion: There is limited evidence (Level 2a) that a standardized oral care program is not more effective than usual oral care in improving nutritional status in patients with acute stroke and subsequent dysphagia.

Oral cavity health
Not effective
2a

One fair quality RCT (Chipps et al., 2014) investigated the effect of oral care on oral cavity health in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive a standardized oral care program (i.e. timed tooth brushing with a battery powered toothbrush, tongue brushing, flossing, mouth rinse, and lip care performed twice daily by trained nurse) or usual oral care as per hospital policy. Cavity health was measured by the Revised-THROAT at baseline and at post-treatment (10 days). No significant between-group differences in oral cavity health were found at post-treatment.

Conclusion: There is limited evidence (Level 2a) that a standardized oral care program is not more effective than usual oral care in preventing oral cavities in patients with acute stroke and subsequent dysphagia.

Swallowing ability
Not effective
2a

One fair quality RCT (Chipps et al., 2014) investigated the effect of oral care on swallowing ability in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive a standardized oral care program (i.e. timed tooth brushing with a battery powered toothbrush, tongue brushing, flossing, mouth rinse, and lip care performed twice daily by trained nurse) or usual oral care as per hospital policy. Swallowing ability was measured by the Mann Assessment of Swallowing Ability at baseline and at post-treatment (10 days). No significant between-group differences in swallowing ability were found at post-treatment.

Conclusion: There is limited evidence (Level 2a) that a standardized oral care program is not more effective than usual oral care in improving swallowing ability in patients with acute stroke and subsequent dysphagia.

Acute phase - Oral electrical stimulation

Airway protection
Not effective
1b

One high quality RCT (Power et al., 2006) investigated the effect of oral electrical stimulation on airway protection in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low frequency oral electrical stimulation at the faucial pillar or sham stimulation. Airway protection was measured by the Penetration-Aspiration Scale at baseline and at post-treatment (1 session of 60 minutes duration). No significant between-group difference in airway protection was found at post-treatment.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that oral electrical stimulation is not more effective than a comparison intervention (sham stimulation) in improving airway protection in patients with acute stroke and subsequent dysphagia.

Swallowing timing
Not effective
1b

One high quality RCT (Power et al., 2006) investigated the effect of oral electrical stimulation on swallowing timing in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low frequency oral electrical stimulation at the faucial pillar or sham stimulation. Swallowing timing (oral transit time, pharyngeal transit time, swallow response time, laryngeal closure duration, cricopharyngeal opening duration) was measured by videofluoroscopy at baseline and at post-treatment (1 session of 60 minutes). There were no significant between-group differences in any measure of swallowing timing at post-treatment.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that oral electrical stimulation is not more effective than a comparison intervention (sham oral electrical stimulation) in improving swallowing timing in patients with acute stroke and subsequent dysphagia.

Acute phase - NMES

Airway protection
Not effective
1b

One high quality RCT (Huang et al., 2014) investigated the effect of neuromuscular electrical stimulation (NMES) and traditional swallowing therapy on airway protection in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES + traditional swallowing therapy, NMES alone, or traditional swallowing therapy alone. Airway protection was measured by the Penetration Aspiration Scale at baseline and post-treatment (3 weeks). No significant between-group differences in airway protection were found at post-treatment.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that NMES and traditional swallowing therapy is not more effective than comparison interventions (NMES alone, traditional swallowing therapy alone) in reducing penetration/aspiration in patients with acute stroke and subsequent dysphagia.

Biomechanical swallowing parameters
Effective
2a

One fair quality RCT (Xia et al., 2011) investigated the effect of neuromuscular electrical stimulation (NMES) on biomechanical swallowing parameters in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES + traditional swallowing therapy, NMES alone, or traditional swallowing therapy alone. Biomechanical swallowing parameters were measured by the Videofluoroscopic Swallowing Study (VFSS) at baseline and at post-treatment (4 weeks). Significant between-group differences in biomechanical swallowing parameters were found at post-treatment favoring NMES + traditional swallowing therapy vs. NMES alone, and favouring NMES + traditional swallowing therapy vs. traditional swallowing therapy alone.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES combined with traditional swallowing therapy is more effective than comparison interventions (NMES alone, traditional swallowing therapy alone) in improving biomechanical swallowing parameters in patients with acute stroke and subsequent dysphagia.

Functional oral intake
Effective
2a

Two fair quality RCTs (Woo Lee et al., 2014), Zhang et al., 2016) investigated the effect of neuromuscular electrical stimulation (NMES) on functional oral intake in patients with acute stroke and subsequent dysphagia.

The first fair quality RCT (Woo Lee et al., 2014) randomized patients to receive either NMES sensory approach + traditional swallowing therapy or traditional swallowing therapy alone. Functional oral intake was measured by the Function Oral Intake Scale (FOIS) at baseline, post-treatment (3 weeks) and at follow-up (6 and 12 weeks). Significant between-group differences in functional oral intake were found at all time points, favoring NMES ­ traditional swallowing therapy vs. traditional swallowing therapy alone.

The second fair quality RCT (Zhang et al., 2016) randomized patients to receive NMES sensory approach, NMES motor approach, or no NMES; all groups received traditional swallowing therapy. Functional oral intake was measured by the FOIS at baseline and at post-treatment (4 weeks). Significant between-group differences in functional oral intake were found at post-treatment, in favour of NMES sensory approach vs. NMES motor approach, in favour of NMES sensory approach vs. no NMES, and in favour of NMES motor approach vs. no NMES.

Conclusion: There is limited evidence (Level 2a) from two fair quality RCTs that NMES sensory approach + traditional swallowing therapy is more effective than comparison interventions (NMES motor approach + traditional swallowing therapy, traditional swallowing therapy alone) in improving functional oral intake among patients with acute stroke and subsequent dysphagia.
Note
: Furthermore, there is limited evidence (Level 2a) from one fair quality RCT that NMES motor approach + traditional swallowing therapy is more effective than a comparison intervention (traditional swallowing therapy alone) in improving functional oral intake in patients with acute stroke and subsequent dysphagia.

Functional severity of dysphagia
Effective
1b

One high quality RCT (Huang et al., 2014) investigated the effect of neuromuscular electrical stimulation (NMES) and traditional swallowing therapy on functional severity of dysphagia in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES + traditional swallowing therapy, NMES alone, or traditional swallowing therapy alone. Functional severity of dysphagia was measured by the Functional dysphagia Scale at baseline and post-treatment (3 weeks). Significant between-group differences in functional severity of dysphagia (solids, thick liquids) were seen at post-treatment, favoring NMES + swallowing therapy vs. NMES alone, and favoring NMES + swallowing therapy vs. traditional swallowing therapy alone. However, no significant between-group differences were found for soft diet and thin liquids.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that NMES and traditional swallowing therapy is more effective than comparison interventions (NMES alone, traditional swallowing therapy) in improving functional severity of dysphagia (solids and thick liquids only) in patients with acute stroke and subsequent dysphagia.
Note:
There were no significant between-group differences on consumption of soft diet or thin liquids.

Muscle electrical activity
Effective
2a

One fair quality RCT (Xia et al., 2011) investigated the effect of neuromuscular electrical stimulation (NMES) on muscle electrical activity in patients with acute stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES + traditional swallowing therapy, NMES alone or traditional swallowing therapy alone. Muscle electrical activity was measured by surface electromyography at baseline and at post-treatment (4 weeks). Significant between-group differences in muscle electrical activity were found at post-treatment, favoring NMES + traditional swallowing therapy vs. NMES alone, and favouring NMES + traditional swallowing therapy vs. traditional swallowing therapy alone.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES combined with traditional swallowing therapy is more effective than comparison interventions (NMES alone, traditional swallowing therapy alone) in improving muscle electrical activity in patients with acute stroke and subsequent dysphagia.

Nutritional status
Not effective
1b

One high quality RCT (Huang et al., 2014) investigated the effect of neuromuscular electrical stimulation (NMES) and traditional swallowing therapy on nutritional status in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES + traditional swallowing therapy, NMES alone, or traditional swallowing therapy alone. Nutritional status was measured by the Functional Oral Intake Scale at baseline and post-treatment (3 weeks). No significant between-group differences in nutritional status were found at post-treatment.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that combined NMES and traditional therapy is not more effective than comparison interventions (NMES alone, traditional swallowing therapy alone) in improving nutritional status in patients with acute stroke and subsequent dysphagia.

Swallowing function
Effective
2a

Two fair quality RCTs (Xia et al., 2011, Zhang et al., 2016) investigated the effect of neuromuscular electrical stimulation (NMES) on functional swallowing in patients with acute stroke and subsequent dysphagia.

The first fair quality RCT (Xia et al., 2011) randomized patients to receive NMES + traditional swallowing therapy, NMES alone or traditional swallowing therapy alone. Swallowing function was measured by the Standardized Swallowing Assessment (SSA) at baseline and at post-treatment (4 weeks). Significant between-group differences in swallowing function were found at post-treatment, favoring NMES + traditional swallowing therapy vs. NMES alone, and favouring NMES + traditional swallowing therapy vs. traditional swallowing therapy alone.

The second fair quality RCT (Zhang et al., 2016) randomized patients to receive NMES sensory approach, NMES motor approach, or no NMES; all groups received traditional swallowing therapy. Functional swallowing was measured by the Water Swallow Test and the SSA at baseline and at post-treatment (4 weeks). Significant between group differences were found on both measures of functional swallowing at post-treatment, in favour of the NMES sensory approach vs. NMES motor approach, in favour of NMES sensory approach vs. no NMES, and in favour of NMES motor approach vs. no NMES.

Conclusion: There is limited evidence (Level 2a) from two fair quality RCTs that NMES + traditional swallowing therapy and NMES sensory approach + traditional swallowing therapy are more effective than comparison interventions (NMES alone, NMES motor approach + traditional swallowing therapy, traditional swallowing therapy alone) in improving functional swallowing among patients with acute stroke and subsequent dysphagia.
Note:
Furthermore, there is limited evidence (Level 2a) from one fair quality RCT that NMES motor approach + traditional swallowing therapy is more effective in improving functional swallowing than a comparison intervention (traditional swallowing therapy alone) in patients with acute stroke and subsequent dysphagia.

Swallowing related quality of life
Effective
2a

Two fair quality RCTs (Xia et al., 2011, Zhang et al., 2016) investigated the effect of neuromuscular electrical stimulation (NMES) on swallowing related quality of life in patients with acute stroke and subsequent dysphagia.

The first fair quality RCT (Xia et al., 2011) randomized patients to receive NMES + traditional swallowing therapy, NMES alone, or traditional swallowing therapy alone. Swallowing-related quality of life was measured by the Swallowing-Related Quality of Life Scale (SWAL-QOL) at baseline and at post-treatment (4 weeks). Significant between-group differences in swallowing-related quality of life were found at post-treatment, favoring NMES + traditional swallowing therapy vs. NMES alone, and favouring NMES + traditional swallowing therapy vs. traditional swallowing therapy alone.

The second fair quality RCT (Zhang et al., 2016) randomized patients to receive NMES sensory approach, NMES motor approach, or no NMES; all groups received traditional swallowing therapy. Swallowing-related quality of life was measured by the SWAL-QOL at baseline and at post-treatment (4 weeks). Significant between-group differences in swallowing-related quality of life were found at post-treatment, in favour of NMES sensory approach vs. NMES motor approach, in favour of NMES sensory approach vs. no NMES, and in favour of NMES motor approach vs. no NMES.

Conclusion: There is limited evidence (Level 2a) from two fair quality RCTs that NMES + traditional swallowing therapy and NMES sensory approach + traditional swallowing therapy are more effective in improving swallowing-related quality of life than comparison intervention (NMES alone, NMES motor approach+ traditional swallowing therapy, traditional swallowing therapy alone) in patients with acute stroke and subsequent dysphagia.
Note:
Furthermore, there is limited evidence (Level 2a) from one fair quality RCT that NMES motor approach + traditional swallowing therapy is more effective than a comparison intervention (traditional swallowing therapy alone) in improving swallowing-related quality of life among patients with acute stroke and subsequent dysphagia.

Acute phase - Pharyngeal electrical stimulation

Airway protection
Effective
1b

One high quality RCT (Jayasekeran et al., 2010) investigated the effect of pharyngeal electrical stimulation on airway protection in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation or sham pharyngeal electrical stimulation for 3 consecutive days. Airway protection was measured by the Penetration-Aspiration Scale using the videofluoroscopic examination at baseline and at 2 weeks from the beginning of the treatment. Significant between-group differences in airways protection were found at 2 weeks, favoring pharyngeal electrical stimulation vs. sham stimulation. 

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that pharyngeal electrical stimulation is more effective than sham stimulation in improving airway protection in patients with acute stroke and subsequent dysphagia.

Functional independence
Not effective
1b

One high quality RCT (Jayasekeran et al., 2010) investigated the effect of pharyngeal electrical stimulation on functional independence in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation or sham pharyngeal electrical stimulation for 3 consecutive days. Functional independence was measured by the Barthel Index at baseline and at discharge from the hospital. No significant between-group differences in functional independence were found at discharge.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that pharyngeal electrical stimulation is not more effective than sham stimulation in improving functional independence in patients with acute stroke and subsequent dysphagia.

Functional severity of dysphagia
Effective
1b

One high quality RCT (Jayasekeran et al., 2010) investigated the effect of pharyngeal electrical stimulation on functional severity of dysphagia in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation or sham pharyngeal electrical stimulation for 3 consecutive days. Functional severity of dysphagia was measured by the dysphagia Severity Rating Scale at baseline and at 2 weeks from the beginning of the treatment. Significant between-group differences in functional severity of dysphagia were found at 2 weeks, favoring pharyngeal electrical stimulation vs. sham stimulation. 

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that pharyngeal electrical stimulation is more effective than sham stimulation in improving functional severity of dysphagia in patients with acute stroke and subsequent dysphagia.

Length of hospitalization
Effective
1b

One high quality RCT (Jayasekeran et al., 2010) investigated the effect of pharyngeal electrical stimulation on length of hospitalization in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation or sham pharyngeal electrical stimulation for 3 consecutive days. Length of hospitalization was measured at discharge from hospital. Significant between-group differences in length of hospitalization were found, favoring pharyngeal electrical stimulation vs. sham stimulation. 

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that pharyngeal electrical stimulation is more effective than sham stimulation in reducing length of hospitalization in patients with acute stroke and subsequent dysphagia.

Temporal swallowing measures
Not effective
1b

One high quality RCT (Jayasekeran et al., 2010) investigated the effect of pharyngeal electrical stimulation on temporal swallowing measures in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation or sham pharyngeal electrical stimulation for 3 consecutive days. Temporal swallowing measures were measured by videofluoroscopic examination at baseline and at 2 weeks from the beginning of the treatment. No significant between-group differences in temporal swallowing measures were found at 2 weeks.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that pharyngeal electrical stimulation is not more effective than sham stimulation in improving temporal swallowing measures in patients with acute stroke and subsequent dysphagia.

Acute phase - Swallowing therapy

Death or institutionalization
Effective
1b

One high quality RCT (Carnaby et al., 2006) investigated the effect of swallowing therapy on incidence of death or institutionalization in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low intensity swallowing therapy (swallowing compensatory strategies, environmental modification, safe swallowing advice, dietary modifications, 3 times per week), high intensity swallowing therapy (direct swallowing exercise, dietary modifications, 5 times per week) or usual care (patient management by the attending physician for 1 month or for the duration of hospitalization). Results from the low intensity and high intensity groups were combined due to minimal differences between the groups. Incidence of death or institutionalization was measured at 6-month follow-up. Significant between-group differences in incidence of death or institutionalization were found favoring swallowing therapy vs. usual care.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that swallowing therapy is more effective than a comparison intervention (usual care) in reducing the incidence of death or institutionalization in patients with acute stroke and subsequent dysphagia.

Functional independence
Not effective
1b

One high quality RCT (Carnaby et al., 2006) investigated the effect of swallowing therapy on functional independence in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low intensity swallowing therapy (swallowing compensatory strategies, environmental modification, safe swallowing advice, dietary modifications, 3 times per week), high intensity swallowing therapy (direct swallowing exercise, dietary modifications, 5 times per week) or usual care (patient management by the attending physician for 1 month or for the duration of hospitalization). Results from the low intensity and high intensity groups were combined due to minimal differences between the groups. Functional independence was measured by the Barthel Index and Modified Rankin Scale at baseline and at 6-month (follow-up). No significant between-group differences in functional independence were seen at 6 months.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that swallowing therapy is not more effective than a comparison intervention (usual care) in improving functional independence in patients with acute stroke and subsequent dysphagia.

Functional swallowing
Effective
1b

One high quality RCT (Carnaby et al., 2006) investigated the effect of swallowing therapy on functional swallowing in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low intensity swallowing therapy (swallowing compensatory strategies, environmental modification, safe swallowing advice, dietary modifications, 3 times per week), high intensity swallowing therapy (direct swallowing exercise, dietary modifications, 5 times per week) or usual care (patient management by the attending physician for 1 month or for the duration of hospitalization). Results from the low intensity and high intensity groups were combined due to minimal differences between the groups. Functional swallowing (i.e. return to pre-stroke diet without swallowing complications) was measured at 6-month follow-up. At 6 months there were significant between-group differences in functional swallowing, favoring swallowing therapy vs. usual care.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that swallowing therapy is more effective than a comparison intervention (usual care) in improving functional swallowing in patients with acute stroke and subsequent dysphagia.

Medical complications and aspiration pneumonia
Effective
1b

One high quality RCT (Carnaby et al., 2006) investigated the effect of swallowing therapy on swallowing-related medical complications including aspiration pneumonia in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low intensity swallowing therapy (swallowing compensatory strategies, environmental modification, safe swallowing advice, dietary modifications, 3 times per week), high intensity swallowing therapy (direct swallowing exercise, dietary modifications, 5 times per week) or usual care (patient management by the attending physician for 1 month or for the duration of hospitalization). Results from the low intensity and high intensity groups were combined due to minimal differences between the groups. Incidence of swallowing-related medical complications and aspiration pneumonia was measured at 6-month follow-up. Significant between-group differences in the incidence of swallowing-related medical complications and aspiration pneumonia were found at 6 months, favoring swallowing therapy vs. usual care.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that swallowing therapy is more effective than a comparison intervention (usual care) in reducing the incidence of swallowing-related medical complications and aspiration in patients with acute stroke and subsequent dysphagia.

Return to normal diet
Not effective
1b

One high quality RCT (Carnaby et al., 2006) investigated the effect of swallowing therapy on return to normal diet in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive low intensity swallowing therapy (swallowing compensatory strategies, environmental modification, safe swallowing advice, dietary modifications, 3 times per week), high intensity swallowing therapy (direct swallowing exercise, dietary modifications, 5 times per week) or usual care (patient management by the attending physician for 1 month or for the duration of hospitalization). Results from the low intensity and high intensity groups were combined due to minimal differences between the groups. Return to normal diet was measured at 6-month follow-up. A significant between-group difference in the number of people who had returned to their normal (pre-stroke) diet was seen at 6 months, favoring usual care vs. swallowing therapy.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that swallowing therapy is not more effective than a comparison intervention (usual care) in improving return to normal diet in patients with acute stroke and subsequent dysphagia. In fact, patients who received standard care were more likely to return to their typical diet by 6 months post-stroke than patients who received swallowing therapy.

Acute phase - Transcranial direct current stimulation (tDSC)

Functional severity of dysphagia
Effective
1a

Two high quality RCTs (Kumar et al., 2011, Joo Yang et al., 2012) investigated the effect of transcranial direct current stimulation (tDCS) on functional severity of dysphagia in patients with acute stroke and subsequent dysphagia.

The first high quality RCT (Kumar et al., 2011) randomized patients to receive anodal tDCS or sham tDCS to the sensorimotor cortical representation of swallowing in the unaffected hemisphere with standardized swallowing maneuvers. Functional severity of dysphagia was measured by the dysphagia Outcome and Severity Scale at baseline and at post-treatment (5 days). Significant between-group differences in severity of dysphagia were found at post-treatment, favoring anodal tDCS vs sham tDCS.

The second high quality RCT (Joo Yang et al., 2011) randomized patients to receive anodal tDCS or sham tDCS to the pharyngeal motor cortex of the affected hemisphere during conventional swallowing training. Functional severity of dysphagia was measured by the Functional dysphagia Scale at baseline, post-treatment (2 weeks) and at 3-month follow-up. While no significant between-group differences in functional severity of dysphagia were seen at post-treatment, significant differences were found at 3-month follow-up, favoring anodal tDCS vs. sham tDCS.

Conclusion: There is strong evidence (Level 1a) from two high-quality RCTs that tDCS during conventional swallowing training is more effective than sham tDCS in improving functional severity of dysphagia in patients with acute stroke and subsequent dysphagia.
Note
: One of the high quality RCTs saw a significant difference in favour of anodal tDCS vs. sham tDCS at 3-month follow-up only.

Swallowing timing
Not effective
1b

One high quality RCT (Joo Yang et al., 2012) investigated the effect of transcranial direct current stimulation (tDCS) on swallowing timing in patients with acute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive anodal tDCS or sham tDCS to the pharyngeal motor cortex of the affected hemisphere during conventional swallowing training. Swallowing timing (oral transit time, pharyngeal transit time and total transit time) was measured by Videofluoroscopic Swallowing Study (VFSS) at baseline, post-treatment (2 weeks) and at 3-month follow-up. No significant between-group differences in swallowing timing were found at any time point.

Conclusion: There is moderate evidence (Level 1b) from one high-quality RCT that tDCS during conventional swallowing training is not more effective than sham tDCS in improving swallowing timing in patients with acute stroke and subsequent dysphagia.

Subacute phase - Dysphagia therapist

Aspiration pneumonia
Not effective
1b

One high quality RCT (DePippo et al., 1994) investigated the effects of dysphagia therapist-led intervention on aspiration pneumonia in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive: (a) minimal input from a dysphagia therapist (diet and swallowing exercises managed by self or a family member); (b) moderate input from a dysphagia therapist (therapist-managed diet, self-managed swallowing exercises); or (c) intensive input from a dysphagia therapist (therapist-managed diet and swallowing exercises). Incidence of aspiration pneumonia was measured at post-treatment (end point during the inpatient stay) and at follow-up (1 year post-stroke). No significant between-group differences in occurrence of aspiration pneumonia were found at either time point. However, there was a significant difference in time to pneumonia onset, whereby patients who received moderate input from the dysphagia therapist developed pneumonia sooner than patients who received minimal input.
Note: This study did not monitor frequency of dysphagia therapist intervention in group C.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that amount of input from a dysphagia therapist does not alter incidence of aspiration pneumonia among patients with subacute stroke and dysphagia.
Note:
However, patients who received moderate input from the dysphagia therapist developed pneumonia sooner than patients who received minimal input.

Dehydration
Not effective
1b

One high quality RCT (DePippo et al., 1994) investigated the effect of dysphagia therapist-led intervention on dehydration in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive: (a) minimal input from a dysphagia therapist (diet and swallowing exercises managed by self or a family member); (b) moderate input from a dysphagia therapist (therapist-managed diet, self-managed swallowing exercises); or (c) intensive input from a dysphagia therapist (therapist-managed diet and swallowing exercises). Incidence of dehydration was measured at post-treatment (end point during the inpatient stay) and at follow-up (1 year post-stroke). No significant between-group differences in occurrence of dehydration were found at either time point.
Note: This study did not monitor for frequency of dysphagia therapist intervention in group C.

Conclusion: There is moderate evidence (level 1b) one high quality RCT that amount of input from a dysphagia therapist does not alter incidence of dehydration among patients with subacute stroke and dysphagia.

Malnutrition
Not effective
1b

One high quality RCT (DePippo et al., 1994) investigated the effect of dysphagia therapist-led intervention on malnutrition in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive: (a) minimal input from a dysphagia therapist (diet and swallowing exercises managed by self or a family member); (b) moderate input from a dysphagia therapist (therapist-managed diet, self-managed swallowing exercises); or (c) intensive input from a dysphagia therapist (therapist-managed diet and swallowing exercises). Malnutrition was measured by time until calorie – nitrogen deficit at baseline, post-treatment (end point during the inpatient stay) and at follow-up (1 year post-stroke). No significant between-group differences in malnutrition were found at any time point.
Note: This study did not monitor for frequency of dysphagia therapist intervention in group C.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that amount of input from a dysphagia therapist does not alter incidence of malnutrition among patients with subacute stroke and dysphagia.

Subacute phase - NMES

Bolus viscosity tolerance
Effective
1b

One high quality RCT (Terre & Mearin, 2015) investigated the effect of NMES on bolus viscosity at which aspiration occurred in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES or sham NMES; both groups received conventional swallowing therapy. Bolus viscosity at which aspiration occurred was measured by videofluorscopic examination at baseline, post-treatment (1 month) and follow-up (3 months). Significant between-group differences for bolus viscosity at which aspiration occurred were found at post-treatment, favoring NMES vs. sham NMES. These differences did not remain significant at follow-up.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that NMES is more effective, in short-term, than sham NMES in improving bolus viscosity at which aspiration occurs in patients with subacute stroke and subsequent dysphagia.

Esophageal strength and coordination
Not effective
1b

One high quality RCT (Terre & Mearin, 2015) investigated the effect of NMES on esophageal strength and coordination in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES or sham NMES; both groups received conventional swallowing therapy. Esophageal strength and coordination were measured by esophageal manometry method (basal pressure, relaxation, pharyngeal contraction) at baseline, post-treatment (1 month) and follow-up (3 months). There were no significant between-group differences in esophageal strength and coordination at any time point.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that NMES is not more effective than sham NMES in improving esophageal strength and coordination in patients with subacute stroke and subsequent dysphagia.

Functional oral intake
Effective
1b

One high quality RCT (Terre & Mearin, 2015) investigated the effect of NMES on functional oral intake in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES or sham NMES; both groups also received conventional swallowing therapy. Functional oral intake was measured by the Functional Oral Intake Scale at baseline, post-treatment (1 month) and follow-up (3 months). Significant between-group differences in functional oral intake were seen from baseline to post-treatment, favoring NMES vs. sham NMES; these improvements did not remain significant at 3-month follow-up.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that NMES is more effective, in short-term, than sham NMES in improving functional oral intake in patients with subacute stroke and subsequent dysphagia.

Satisfaction with treatment
Effective
1b

One high quality RCT (Terre & Mearin, 2015) investigated the effects of NMES on satisfaction with treatment in patients with subacute stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES and conventional swallowing therapy or sham NMES and conventional swallowing therapy. Satisfaction with treatment was measured by a 7-Point Likert Scale at post-treatment (1 month) and follow-up (3 months). Significant between-group differences were found for satisfaction with treatment at post-treatment, favoring the NMES vs. sham NMES. These significant differences were not maintained at follow-up.

Conclusion: There is moderate (Level 1b) evidence from one high quality RCT that NMES is more effective, in short-term, than sham NMES in improving satisfaction with treatment in patients with subacute stroke and subsequent dysphagia.

Chronic phase - Functional magnetic stimulation

Swallowing performance over time
Effective
1b

One high quality RCT (Momosaki et al., 2013) investigated the effect of functional magnetic stimulation (FMS) on swallowing performance over time in patients with chronic stroke and subsequent dysphagia. This high quality RCT randomized patients to receive real FMS or sham FMS over the suprahyoid muscle group. Swallowing performance over time was measured by the Timed Water-Swallow Test (inter-swallow interval, speed, capacity) at baseline and post-treatment (1 x 10-minute session). Significant between-group differences were found for swallowing speed and capacity at post-treatment, favoring real FMS vs. sham FMS.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that real FMS is more effective than sham FMS in improving swallowing speed and capacity in patients with chronic stroke and subsequent dysphagia.

Chronic phase - NMES

Biomechanical swallowing parameters
Not effective
2a

One fair quality RCT (Bulow et al., 2008) investigated the effect of neuromuscular electrical stimulation (NMES) on biomechanical swallowing parameters in patients with chronic stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES or traditional swallowing therapy. Biomechanical swallowing parameters were measured by videofluoroscopic examination at baseline and post-treatment (3 weeks). No significant between-group differences were found in biomechanical swallowing parameters at post-treatment.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES is not more effective than a comparison intervention (traditional swallowing therapy) in improving biomechanical swallowing parameters in patients with chronic stroke and subsequent dysphagia.

Functional nutrition
Not effective
2a

One fair quality RCT (Bulow et al., 2008) investigated the effects of NMES on functional nutrition in patients with chronic stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES or traditional swallowing therapy. Functional nutrition was measured by the Actual Nutrition Scale at baseline and post-treatment (3 weeks). No significant between-group differences were found for functional nutrition at post-treatment.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES is not more effective than a comparison intervention (traditional swallowing therapy) in improving functional nutrition in patients with chronic stroke and subsequent dysphagia.

Oral motor function
Not effective
2a

One fair quality RCT (Bulow et al., 2008) investigated the effect of NMES on oral motor function in patients with chronic stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES or traditional swallowing therapy. Oral motor function was measured by the Oral Motor Function Scale at baseline and post-treatment (3 weeks). No significant between-group differences were found in oral motor function at post-treatment.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES is not more effective than a comparison intervention (traditional swallowing therapy) in improving oral motor function in patients with chronic stroke and subsequent dysphagia.

Self-evaluation of dysphagia
Not effective
2a

One fair quality RCT (Bulow et al., 2008) investigated the effect of  NMES on self-evaluation of dysphagia in patients with chronic stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive NMES or traditional swallowing therapy. Self-evaluation of dysphagia was measured using a 5-point Visual Analogue Scale at baseline and post-treatment (3 weeks). No significant between-group differences were found for self-evaluation of dysphagia at post-treatment. 

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that NMES is not more effective than a comparison intervention (traditional swallowing therapy) in improving self-evaluation of dysphagia in patients with chronic stroke and subsequent dysphagia.

Chronic phase - NMES & effortful swallow

Airway protection
Effective
1b

One high quality RCT (Park et al., 2016) investigated the effect of combined NMES and effortful swallow on airway protection in patients with chronic stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES to the point of effortful swallow (motor NMES) or NMES alone (sensory NMES). Airway protection was measured by the Penetration-Aspiration Scale at baseline and post-treatment (6 weeks). Significant between group differences were found for airway protection at post-treatment, favoring motor NMES vs. sensory NMES.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that motor NMES is more effective than sensory NMES in improving airway protection in patients with chronic stroke and subsequent dysphagia.

Biomechanical swallowing parameters
Effective
1b

One high quality RCT (Park et al., 2016) investigated the effect of NMES and effortful swallow on biomechanical swallowing parameters in patients with chronic stroke and subsequent dysphagia. This high quality RCT randomized patients to receive NMES to the point of effortful swallow (motor NMES) or NMES alone (sensory NMES). Biomechanical swallowing parameters were measured by the Videofluoroscopic dysphagia Scale (VDS – total, oral phase, pharyngeal phase), and horizontal and vertical displacement of the hyoid bone on videofluoroscopic swallowing study at baseline and post-treatment (6 weeks). Significant between-group differences were found for all biomechanical swallowing parameters (except VDS – oral phase) at post-treatment, favoring motor NMES vs sensory NMES.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that motor NMES is more effective than sensory NMES in improving biomechanical swallowing parameters in patients with chronic stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - Combined central and peripheral neurostimulation

Airway protection
Effective
1b

One high quality RCT (Michou et al., 2014) investigated the effect of combined central and peripheral forms of neurostimulation on airway protection in patients with subacute or chronic stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation (PES), paired associative stimulation (PAS), repetitive transcranial magnetic stimulation (rTMS), or the respective sham treatments (i.e. sham PES, sham PAS, sham rTMS). Airway protection was measured by the Penetration-Aspiration Scale using videofluoroscopic assessment at baseline and 30 minutes post-treatment. When results of all three real modalities were combined, a significant between-group difference was found in airway protection, favoring combined central and peripheral neurostimulation vs. sham neurostimulation.

Conclusion: There is moderate (Level 1b) evidence from one high quality RCT that combined central and peripheral forms of neurostimulation is more effective than sham stimulation in improving airway protection in patients with subacute or chronic stroke and subsequent dysphagia.

Cortical excitability
Effective
1b

One high quality RCT (Michou et al., 2014) investigated the effect of combined central and peripheral forms of neurostimulation on cortical excitability in patients with subacute or chronic stroke and subsequent dysphagia. This high quality RCT randomized patients to receive pharyngeal electrical stimulation (PES), paired associative stimulation (PAS), repetitive transcranial magnetic stimulation (rTMS), or the respective sham treatments (i.e. sham PES, sham PAS, sham rTMS). Corticobulbar excitability of the pharyngeal motor cortex was measured at baseline and 30 minutes post-treatment. Significant between-group differences were found in corticobulbar excitability of the pharyngeal motor cortex of the unaffected hemisphere, favoring PES vs. sham PES and PAS vs. sham PAS. No significant between-treatment differences were found in corticobulbar excitability of the pharyngeal motor cortex of the unaffected hemisphere for rTMS vs. sham rTMS. Moreover, when results of all three real modalities were combined, a significant between-treatment difference was found in the corticobulbar excitability of the pharyngeal motor cortex of the unaffected hemisphere, favoring combined central and peripheral neurostimulation vs. sham neurostimulation.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that combined central and peripheral forms of neurostimulation is more effective than sham stimulation in improving corticobulbar excitability of the pharyngeal motor cortex of the unaffected hemisphere in patients with subacute or chronic stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - Mendelsohn maneuver

Airway protection
Not effective
2a

One fair quality RCT (McCullough & Kim, 2013; results also reported in McCullough et al., 2012) investigated the effect of the Mendelsohn maneuver on airway protection in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive the Mendelsohn maneuver or no treatment. Airway protection was measured by the Penetration-Aspiration Scale (PAS) at baseline, post-treatment (2 weeks) and at 3-month follow-up.  No significant between-group differences in airway protection were found at either time point.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that the Mendelsohn maneuver is not more effective than no treatment in improving airway protection in patients with stroke and subsequent dysphagia.

Biomechanical swallowing parameters
Not effective
2a

One fair quality RCT (McCullough & Kim, 2013) investigated the effect of Mendelsohn maneuver on biomechanical swallowing parameters in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive the Mendelsohn maneuver or no treatment. Biomechanical swallowing parameters were measured by Videofluoroscopic Swallowing Study (VFSS – hyoid maximum elevation, hyoid maximum anterior excursion, extent of upper esophageal sphincter opening) at baseline, post-treatment (2 weeks) and at 3-month follow-up.  There were no significant between-group differences in any biomechanical swallowing parameter at any time point.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that the Mendelsohn maneuver is not more effective than no treatment in improving biomechanical swallowing parameters in patients with stroke and subsequent dysphagia.

Functional severity of dysphagia
Not effective
2a

One fair quality RCT (McCullough & Kim, 2013; results also reported in McCullough et al., 2012) investigated the effect of the Mendelsohn maneuver on functional severity of dysphagia in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive the Mendelsohn maneuver or no treatment. Functional severity of dysphagia was measured by the dysphagia Outcome and Severity Scale (DOSS) at baseline, post-treatment (2 weeks) and at 3-month follow-up.  No significant between-group differences in functional severity of dysphagia were found at any time point.

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that the Mendelsohn maneuver is not more effective than no treatment in improving functional severity of dysphagia in patients with stroke and subsequent dysphagia.

Swallowing timing
Not effective
2a

One fair quality RCT (McCullough et al., 2012) investigated the effect of the Mendelsohn maneuver on swallowing timing in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive the Mendelsohn maneuver or no treatment. Swallowing timing was measured by Videofluoroscopic Swallowing Study (VFSS – duration of: hyoid maximum anterior excursion, hyoid maximum elevation, pharyngeal response, upper esophageal sphincter opening) at baseline and post-treatment (2 weeks). No significant between-group differences in swallowing timing were found at post-treatment.  

Conclusion: There is limited evidence (Level 2a) from one fair quality RCT that the Mendelsohn maneuver is not more effective than no treatment in improving swallowing timing in patients with stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - Motor electrical stimulation & effortful swallow

Airway protection
Insufficient evidence
5

One fair quality RCT (Park et al., 2012) investigated the effect of combined effortful swallow with infrahyoid motor electrical stimulation on airway protection in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive either infrahyoid motor electrical stimulation or infrahyoid sensory electrical stimulation. Airway protection was measured by the Penetration-Aspiration Scale (PAS) on effortful swallow at baseline and at post-treatment (4 weeks). Between-group differences in airway protection were not reported; there were no significant within-group differences in airway protection from baseline to post-treatment in either group.

Conclusion: There is insufficient evidence (Level 5) regarding the effect of motor electrical stimulation on airway protection. A fair quality RCT found no significant change in airway protection following motor or sensory electrical stimulation.

Biomechanical swallowing parameters
Insufficient evidence
5

One fair quality RCT (Park et al., 2012) investigated the effect of combined effortful swallow with infrahyoid motor electrical stimulation on biomechanical swallowing parameters in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive either infrahyoid motor electrical stimulation or infrahyoid sensory electrical stimulation. Biomechanical swallowing parameters were measured on effortful swallow by the Videofluoroscopic Swallowing Study (VFSS) at baseline and at post-treatment (4 weeks). Between-group differences in biomechanical swallowing parameters were not reported. Within-group comparison revealed a significant increase in vertical movement of the larynx from baseline to post-treatment in the motor electrical stimulation group, whereas the sensory electrical stimulation group showed no significant differences in biomechanical swallowing parameters from baseline to post-treatment.   

Conclusion: There is insufficient evidence (Level 5) regarding the effect of motor electrical stimulation on biomechanical swallowing parameters. However, a fair quality RCT found a significant increase in the vertical movement of the larynx from baseline to post-treatment in the motor electrical stimulation group but not the sensory electrical stimulation group.

Phase of stroke recovery not specific to one period - NMES & physical therapy

Biomechanical swallowing parameters
Effective
2a

One fair quality RCT (El-Tamawy et al., 2015) investigated the effect of physical therapy and neuromuscular electrical stimulation (NMES) on biomechanical swallowing parameters in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive physical therapy+NMES or medical care alone. Physical therapy was directed at strengthening and stimulating the elevator muscles of the larynx above and below the hyoid bone. Biomechanical swallowing parameters were measured by VideoFluoroscopic Swallowing Study (VFSS – oral transit time, hyoid elevation, laryngeal elevation, esophageal sphincter opening, aspiration/penetration) at baseline and post-treatment (6 weeks). Significant between group differences in all biomechanical swallowing parameters except oesophageal sphincter opening were found at post-treatment, favoring physical therapy+NMES vs. medical care alone.

Conclusion: There is limited (Level 2a) evidence that physical therapy + NMES is more effective than a comparison intervention (medical care alone) in improving biomechanical swallowing parameters in patients with stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - NMES & tactile-thermal stimulation

Airway protection
Effective
1b

One high quality RCT (Lim et al., 2009) investigated the effect of combined neuromuscular electrical stimulation (NMES) and thermal-tactile stimulation (TTS) on airway protection in patients stroke and subsequent dysphagia.  This high quality RCT randomized patients to receive combined NMES+TTS  or  TTS alone.  Airway protection during consumption of semi-solids and liquids was measured by the Rosenbek Penetration-Aspiration Scale at baseline and at post-treatment (4 weeks). Significant between-group differences in airway protection (semi-solids and liquids) were found at post-treatment, favoring NMES+TSS vs. TSS alone.  

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that combined neuromuscular electrical stimulation and tactile-thermal stimulation is more effective than tactile-thermal stimulation alone in improving airway protection in patients with stroke and subsequent dysphagia.

Swallowing function
Effective
1b

One high quality RCT (Lim et al., 2009)  investigated the effect of combined neuromuscular electrical stimulation (NMES) and thermal-tactile stimulation (TTS) on swallowing function in patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive combined NMES+TTS or TTS alone.  Swallowing function was measured by the Swallow Function Scoring system at baseline and post-treatment (4 weeks). Significant between-group differences in swallowing function were found at post-treatment, favoring combined NMES+TSS vs. TSS alone.

Conclusion: There is moderate evidence (Level 1b) from 1 high quality RCT that combined neuromuscular electrical stimulation and tactile-thermal stimulation is more effective than tactile-thermal stimulation alone in improving swallowing function in patients with stroke and subsequent dysphagia.

Swallowing timing
Effective
1b

One high quality RCT (Lim et al., 2009) investigated the effect of combined neuromuscular electrical stimulation (NMES) and thermal-tactile stimulation (TTS) on swallowing timing in patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive combined NMES+TTS or TTS alone.  Pharyngeal transit timing on consumption of semi-solids and liquids was measured by videofluoroscopic imaging at baseline and post-treatment (4 weeks). Significant between-group differences were found for swallow timing at post-treatment, favoring NMES+TSS vs. TSS alone.

Conclusion: There is moderate evidence (Level 1b) from 1 high quality RCT that combined neuromuscular electrical stimulation and tactile-thermal stimulation is more effective than tactile-thermal stimulation alone in improving swallow timing in patients with stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - Olfactory stimulation

Cough-reflex sensitivity
Not effective
2a

One fair quality RCT (Ebihara et al., 2006) investigated the effect of olfactory stimulation on cough reflex sensitivity in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive black pepper oil stimulation, lavender oil stimulation, or nasal inhalation of distilled water. Cough reflex sensitivity was measured at baseline and post-treatment (30 days). No significant between-group differences in cough reflex sensitivity were found at post-treatment.

Conclusion: There is limited evidence (Level 2a) from 1 fair quality RCT that olfactory stimulation using black pepper oil is not more effective than comparison interventions (lavender oil stimulation, nasal inhalation of distilled water) in improving cough-reflex sensitivity in patients with stroke and subsequent dysphagia.

Number of swallowing movements
Effective
2a

One fair quality RCT (Ebihara et al., 2006) investigated the effect of olfactory stimulation on the number of swallowing movements in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive olfactory stimulation using black pepper oil, lavender oil, or distilled water. The number of swallowing movements was measured at baseline and post-treatment (30 days). Significant between-group differences in the number of swallowing movements were found at post-treatment, favoring black pepper oil vs. lavender oil and favoring black pepper oil vs. distilled water.

Conclusion: There is limited evidence (Level 2a) from 1 fair quality RCT  that olfactory stimulation using black pepper oil is more effective than comparison interventions (lavender oil, distilled water)  in increasing the number of swallowing movements in patients with stroke and subsequent dysphagia.

Risk of aspiration
Effective
2a

One fair quality RCT (Ebihara et al., 2006) investigated the effect of olfactory stimulation on risk of aspiration in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive olfactory stimulation using black pepper oil, lavender oil or distilled water. Risk of aspiration was measured according to Serum Substance P release, at baseline and post-treatment (30 days). Significant between-group differences in Serum Substance P levels were found at post-treatment, favoring black pepper oil vs. lavender oil and favoring black pepper oil vs. distilled water, indicating reduced risk of aspiration following this treatment.

Conclusion: There is limited evidence (Level 2a) from 1 fair quality RCT that olfactory stimulation using black pepper oil is more effective than comparison interventions (lavender oil, distilled water) in reducing risk of aspiration in patients with stroke and subsequent dysphagia.

Swallowing reflex
Effective
2a

One fair quality RCT (Ebihara et al., 2006) investigated the effect of olfactory stimulation on swallowing reflex latency in patients with stroke and subsequent dysphagia. This fair quality RCT randomized patients to receive olfactory stimulation using black pepper oil, lavender oil, or distilled water. Swallowing reflex latency was measured by the Swallowing Reflex Timed test at baseline and post-treatment (30 days). Significant between-group differences in latency of swallowing reflex were found at post-treatment, favoring black pepper oil vs. lavender oil, and favoring black pepper oil vs. distilled water.

Conclusion: There is limited evidence (Level 2a) from 1 fair quality RCT that olfactory stimulation using black pepper oil is more effective than comparison interventions (lavender oil, distilled water) in improving latency of swallowing reflex in patients with stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - Repetitive transcranial magnetic stimulation (rTMS)

Airway protection
Insufficient evidence
5

One high quality RCT (Park et al., 2013) investigated the effect of repetitive transcranial stimulation (rTMS) on airway protection in patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive either active rTMS t or sham rTMS to the contralesional pharyngeal motor cortex. Airway protection was measured by the Penetration-Aspiration Scale (PAS) at baseline, post-treatment (2 weeks) and at 4-week follow-up. Between-group differences in airway protection were not reported; neither group demonstrated a significant change in airway protection from baseline to post-treatment and from baseline to follow-up. 

Conclusion: There is insufficient evidence (Level 5) regarding the effectiveness of rTMS vs. sham rTMS in improving airway protection in patients with stroke. One high quality RCT reported no significant change in airway protection following rTMS or sham rTMS.

Degree of dysphagia
Effective
1b

Two high quality RCTs (Khedr & Abo-Elfetoh, 2010, Park et al., 2013) investigated the effect of repetitive transcranial stimulation (rTMS) on degree of dysphagia in patients with stroke and subsequent dysphagia.

The first high quality RCT (Khedr & Abo-Elfetoh, 2010) randomized patients to receive either active rTMS or sham rTMS over the oesophageal motor cortex. Degree of dysphagia was measured by a 4-point non-standardized grading scale at baseline, post-treatment (5 days), and at 1-month and 2-month follow-up. Significant between-group differences in degree of dysphagia were found at all time points, favoring active rTMS vs. sham rTMS.

The second high quality RCT (Park et al., 2013) randomized patients to receive either active rTMS or sham rTMS to the contralesional pharyngeal motor cortex. Degree of dysphagia was measured by the Videofluoroscopic dysphagia Scale (VDS) at baseline, post-treatment (2 weeks) and 4-week follow-up. Between-group differences were not reported. However, within-group analysis showed significant improvement in degree of dysphagia from baseline to post-treatment and from baseline to follow-up in the active rTMS group only.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that that active rTMS is more effective than sham rTMS in improving degree of dysphagia in patients with stroke. Furthermore, a high quality RCT also reported a significant improvement in degree of dysphagia following rTMS.

Functional independence
Effective
1b

One high quality RCT (Khedr & Abo-Elfetoh, 2010) investigated the effect of repetitive transcranial stimulation (rTMS) on functional independence in patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive active rTMS or sham rTMS over the oesophageal motor cortex. Functional independence was measured by the Barthel Index at baseline, post-treatment (5 days) and at 1-month and 2-month follow-up. Significant between-group differences in functional independence were seen at all time points among patients with lateral medullary infarction (but not other brainstem infarctions), favoring active rTMS vs. sham rTMS.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that active rTMS is more effective than sham rTMS in improving functional independence in patients with stroke (specifically lateral medullary infarction but not brainstem infarction) and subsequent dysphagia.

Neurological recovery
Not effective
1b

One high quality RCT (Khedr & Abo-Elfetoh, 2010) investigated the effect of repetitive transcranial stimulation (rTMS) on neurological recovery of patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive either active rTMS or sham rTMS over the oesophageal motor cortex. Neurological recovery was measured by the National Institutes of Health stroke Scale (NIHSS) and the Hemispheric stroke Scale at baseline, post-treatment (5 days) and at 1-month and 2-month follow-up. No significant between-group differences in recovery were seen at any time point.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that active rTMS is not more effective than sham rTMS in improving neurological recovery of patients with stroke and subsequent dysphagia.

Phase of stroke recovery not specific to one period - tDCS

Functional severity of dysphagia
Effective
1b

One high quality RCT (Shigematsy et al., 2013) investigated the effect of transcranial direct stimulation (tDCS) with on functional severity of dysphagia in patients with stroke and subsequent dysphagia. This high quality RCT randomized patients to receive anodal tDCS or sham tDCS to the ipsilesional pharyngeal motor cortex; both groups received simultaneous conventional swallowing therapy. Functional severity of dysphagia was measured by the dysphagia Outcome and Severity Scale (DOSS) at baseline, post-treatment (10 days) and at 1-month follow-up. Significant between-group differences in functional severity of dysphagia were found at post-treatment and at follow-up, favoring anodal tDCS vs. sham tDCS.

Conclusion: There is moderate evidence (Level 1b) from one high quality RCT that anodal tDCS is more effective than sham tDCS in improving functional severity of dysphagia in patients with stroke and subsequent dysphagia.

References

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Chipps, E., Gatens, C., Genter, L., Musto, M., Dubis-Bohn, A., Gliemmo, M., Dudley, K., Holloman, C., Hoet, A.E., & Landers, T. (2014). Pilot study of an oral care protocol on poststroke survivors. Rehabilitation Nursing.  39(6), 294-304.
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DePippo K.L., Holas M.A., Reding M.J., Mandel F.S., Lesser M.L. (1994). Dysphagia therapy following stroke: A controlled trial. Neurology, 44, 1655-1660.
http://www.ncbi.nlm.nih.gov/pubmed/7936292

Ebihara T., Ebihara S., Maruyama M., Kobayashi M., Itou A., Arai H., Sasaki H. (2006). A randomized trial of olfactory stimulation using black pepper oil in older people with swallowing dysfunction. Journal of the American Geriatrics Society. 54, 1401-6.
http://www.ncbi.nlm.nih.gov/pubmed/16970649

El-Tamawy, M., Darwish, M.H., El-Azizi, H.S., Abdelalim, A.M., & Taha, S.I. (2015). The influence of physical therapy on oropharyngeal dysphagia in acute stroke patients. Egyptian Journal of Neurology Psychiatry and Neurosurgery, 52, 201-205.
https://www.researchgate.net/publication/281537852_The_influence_of_physical_therapy_on_oropharyngeal_dysphagia_in_acute_stroke_patients

Huang, K-L., Liu, T-Y., Huang, Y-C., Leong, C-P., Lin, W-C., & Pong, Y-P. (2014). Functional outcome in acute patients with oropharyngeal dysphagia after swallowing therapy. Journal of Stroke and Cerebrovascular Diseases, 23(10), 2547-53.
http://www.ncbi.nlm.nih.gov/pubmed/25245482

Jayasekeran, V., Singh, S., Tyrrell, P., Michou, E., Jefferson, S., Mistry, S., & Hamdy, S. (2010). Adjunctive functional pharyngeal electrical stimulation reverses swallowing disability after brain lesions. Gastroenterology, 138(5), 1737-1746.
http://www.sciencedirect.com/science/article/pii/S0016508510001617

Joo Yang, E.J., Baek, S-R., Shin, J., Lim, J.Y., Kim, Y.K., & Paik, N.J. (2012). Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restorative Neurology and Neuroscience, 30, 303-11.
http://www.ncbi.nlm.nih.gov/pubmed/22572022

Khedr, E. & Abo-Elfetoh, N. (2010). Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infraction. Journal of Neurology Neurosurgery and Psychiatry, 81, 495-99.
http://www.ncbi.nlm.nih.gov/pubmed/19828479

Kumar, S., Wagner, C.W., Frayne, C., Zhu, L., Selim, M., Feng, W., & Schlaug, G. (2011). Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke, 42, 1035-40.
http://www.ncbi.nlm.nih.gov/pubmed/21441148

Lim K.B., Lee H.-J.L., Lim S.-S., Choi Y.-I., (2009). Neuromuscular Electrical and Thermal-Tactile Stimulation for Dysphagia Caused by Stroke: A Randomized Controlled Trial. Journal of Rehabilitation Medicine, 41(3), 174-178.
http://www.ncbi.nlm.nih.gov/pubmed/19229451

McCullough, G.H., Kamarunas, E., Mann, G.C., Schmidley, J.W., Robbins, J.A., Crary, M.A. (2012). Effects of Mendelsohn maneuver on measures of swallowing duration post-stroke. Topics in Stroke Rehabilitation, 19(3), 234-43.
http://www.ncbi.nlm.nih.gov/pubmed/22668678

McCullough, G.H., & Kim, Y. (2013). Effects of Mendelsohn maneuver on extent of hyoid movement and UES opening post-stroke. Dysphagia, 28, 511-19.
http://www.ncbi.nlm.nih.gov/pubmed/23494471

Michou, E., Mistry, S., Jefferson, S., Tyrrell, P., & Hamdy, S. (2014). Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients. Brain Stimulation, 7(1), 66-73.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3893483/

Momosaki, R., Masahiro, A., Watanabe, S., Kakuda, W., Yamada, N., & Mochio, K. (2014). Functional magnetic stimulation using a parabolic coil for dysphagia after stroke. Neuromodulation, 17, 637-41.
http://www.ncbi.nlm.nih.gov/pubmed/24320695

Park, J-W., Kim, Y., Oh, J-C., & Lee, H-J. (2012). Effortful swallowing training combined with electrical stimulation in post-stroke dysphagia: a randomized controlled study. Dysphagia, 27, 521-27.
http://www.ncbi.nlm.nih.gov/pubmed/22447240

Park, J-W., Oh, J-C., Lee, J-W., Yeo, J-S., Ryu, K-H. (2013). The effects of 5Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterology and Motility, 25(4), 324-e250.
http://www.ncbi.nlm.nih.gov/pubmed/23279198

Park, J-S., Oh, D-H., Hwang, N-K., & Lee, J-H. (2016). Effects of neuromuscular electrical stimulation combined with effortful swallowing on spot-stroke oropharyngeal dysphagia: a randomized controlled trial. Journal of Oral Rehabilitation, 43, 426-34.
http://www.ncbi.nlm.nih.gov/pubmed/26969528

Power M. L., Fraser C.H., Hobson A., Singh S., Tyrrell P., Nicholson D.A., Turnbull I., Thompson D.G. & Hamdy S. (2006). Evaluating oral stimulation as a treatment for dysphagia after stroke. The Journal of Dysphagia, 49-55.
http://www.ncbi.nlm.nih.gov/pubmed/16544087

Shigematsy, T., Fujishima, I., & Ohno, K. (2013). Transcranial direct current stimulation improves swallowing function in stroke patients. Neurorehabilitation and Neural Repair, 27(4), 363-69.
http://www.ncbi.nlm.nih.gov/pubmed/23392916

Terré, R., & Mearin, F. (2015). A randomized controlled study of neuromuscular electrical stimulation in oropharyngeal dysphagia secondary to acquired brain injury. European Journal of Neurology, 22(4), 687-e44.
http://onlinelibrary.wiley.com/doi/10.1111/ene.12631/full

Woo Lee, K.W., Kim, S.B., Lee, J.H., Lee, S.J., Ri, J.W., & Park, G.J. (2014). The effect of early neuromuscular electrical stimulation therapy in acute/subacute ischemic stroke patients with dysphagia. Annals of Rehabilitation Medicine, 38(2), 153-9.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4026600/

Xia, W., Zheng, C., Zhu, S., & Tang, Z. (2016). Does the addition of specific acupuncture to standard swallowing training improve outcomes in patients with dysphagia after stroke? A randomized controlled trial. Clinical Rehabilitation, 30(3), 237-246.
http://www.ncbi.nlm.nih.gov/pubmed/25819076

Xia, W., Zheng, C., Lei, Q., Tang, Z., Hua, Q., Zhang, Y., & Zhu, S. (2011). Treatment of post-stroke dysphagia by VitalStim therapy coupled with conventional swallowing training. Journal of Huazhong University of Science and Technology, 31(1), 73-6.
http://www.ncbi.nlm.nih.gov/pubmed/21336727

Zhang, M., Tao, T., Zhang, Z-B., Zhu, X., Fan, W-G., Pu, L-J., Chu, L., & Yue, S-W. (2016). Effectiveness of neuromuscular electrical stimulation on patients with dysphagia with medullary infraction. Archives of Physical Medicine and Rehabilitation, 97, 355-62.
http://www.ncbi.nlm.nih.gov/pubmed/26606872

Zhao, J-W., Wang, Z-Y., Cao, W-Z., Zhang, Y-W., Song, S-C., Kang, W-G., & Yang, J-H. (2015). Therapeutic efficacy of swallowing neuromuscular electrical stimulation combined with acupuncture for post-stroke dysphagia. World Journal of Acupuncture-Moxibustion, 25(1), 19-23.
http://www.sciencedirect.com/science/article/pii/S1003525715300040

Excluded Studies:

Allison, M.C., Morris, A.J., Park, R.H.R., & Mills P.R. (1992). Percutaneous endoscopic gastrostomy tube feeding may improve outcome of late rehabilitation following strokeJournal of the Royal Society of Medicine85 (3), 147-149.
Reason for exclusion: Not RCT.

Carnaby-Mann, G.D. & Crary, M.A. (2008). Adjuctive neuromuscular electrical stimulation for treatment-refractory dysphagiaAnnals of Otology, Rhinology & Laryngology117(4), 279-87.
Reason for exclusionQuasi-experimental study design, not RCT.

Cheng, I., Chan, K., Wong, C.S., & Cheung, R. (2015). Preliminary evidence of the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) on swallowing functions in post-stroke individuals with chronic dysphagiaInternational Journal of Language & Communication Disorders50(3), 389-96.
Reason for exclusion: Case series study design, not RCT.

Crary, M.A., Carnaby, G.D., Lagorio, L.A., & Carvajal, P.J. (2012). Functional and physiological outcomes from an exercise-based dysphagia therapy: a pilot investigation of the McNeill dysphagia therapy program. Archives of Physical Medicine and Rehabilitation93, 1173-8.
Reason for exclusionQuasi-experimental study design, not RCT.

Crary M.A. (1995). A direct intervention program for chronic neurogenic dysphagia secondary to brainstem strokeDysphagia10(1), 6-18.
Reason for exclusion: Not RCT.

Crary M.A., Carnaby G.D., Groher M.E., Helseth E. (2004). Functional benefits of dysphagia therapy using adjunctive sEMG biofeedback. Dysphagia19(3), 160-164.
Reason for exclusion: Not RCT.

Gallas, S., Marie, J.P., Leroi, A.M., & Verin, E. (2010). Sensory transcutaneous electrical stimulation improves post-stroke dysphagic patients. Dysphagia25, 291-7.
Reason for exclusionQuasi-experimental study design, not RCT.

Garon B.R., Engle M., Ormiston C. (1997). A randomized control study to determine the effects of unlimited oral intake of water in patients with identified aspiration. Neurorehabilitation and Neural Repair, 11, 139-148.
Reason for exclusion: Nature of intervention is compensatory

Goulding R., Bakheit AM. (2000). Evaluation of the benefits of monitoring fluid thickness in the dietary management of dysphagic stroke patients. Clinical Rehabilitation, 14, 119-24.
Reason for exclusion: Nature of intervention is compensatory.

Finestone, H.M., Foley, N.C., Woodbury, M.G., Greene-Finestone, L. (2001). Quantifying fluid intake in dysphagic stroke patients: A preliminary comparison of oral and nonoral strategies. Archives of Physical Medicine and Rehabilitation, 82, 1744- 1746.
Reason for exclusion: Not RCT.

Hagg, M. & Larsson, B. (2004). Effects of Motor and Sensory Stimulation in Stroke Patients with Long-Lasting DysphagiaDysphagia19, 219-230.
Reason for exclusion: Not RCT.

Hagg M. & Anniko M. (2008). Lip muscle training in stroke patients with dysphagiaActa Oto-Laryngologica128, 1027-1033.
Reason for exclusion: Not RCT.

Hamidon B.B., Abdullah S.A., Zawawi M. F., Sukumar N., Aminuddin A., Raymond A.A. (2006). A prospective comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding in patients with acute dysphagic strokeThe Medical journal of Malaysia61(1), 59 -66.
Reason for exclusion: Nature of intervention

Huang, J.Y., Zhang, D.Y., Yao, Y., Xia, Q.X., Fan, Q.Q. (2006). Training in swallowing prevents aspiration pneumonia in stroke patients with dysphagiaThe Journal of International Medical Research34, 303-306.
Reason for exclusion: Not RCT.

Kim, S.J. (2010). Music therapy protocol development to enhance swallowing training for stroke patients with dysphagiaJournal of Music TherapyXLVII (2), 102-19.
Reason for exclusion: Case series study design, not RCT.

Lemoncello, R., Sohlberg, M.K., Fickas, S., Albin, R., & Harn, B.E. (2010). Phase I evaluation of the television assisted prompting system to increase completion of home exercises among stroke survivors. Disability and Rehabilitation: Assistive Technology6(5), 440-52.
Reason for exclusion: Case-series study design, not RCT.

Lin, L. C., Wang, S. C., Chen, S. H., Wang, T. G., Chen, M. Y., & Wu, S. C. (2003). Efficacy of swallowing training for residents following strokeJournal of advanced nursing44(5), 469-478.
Reason for exclusion: Not RCT.

Logemann, J.A., Rademaker, A., Pauloski, B.R., Kelly, A., Stangl-McBreen, A., Antinoja, J., Grande, B., Farquharson, J., Kern, M., Easterling, C., & Shaker, R. (2009). A randomize study comparing the Shaker exercise with traditional therapy: a preliminary study. Dysphagia24, 403-11.
Reason for exclusion: Other population than patients with stroke.

Nam, H. S., Beom, J., Oh, B. M., & Han, T. R. (2013). Kinematic effects of hyolaryngeal electrical stimulation therapy on hyoid excursion and laryngeal elevation. Dysphagia, 28(4), 548-556.
Reason for exclusion: Mixed sample with no indication to the percentage of those with stroke vs. brain injury.

Norton B., Homer-Ward M., Donnelly M.T., Long R.G., Holmes G.K. (1996). A randomised prospective comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding after acute dysphagic strokeBritish Medical Journal312(7022), 13-16.
Reason for exclusion: Nature of intervention.

Park R.H.R, Allison M.C., Lang J., Spence E., Morris A.J, Danesh B.J.Z., Russell R.I., Mills P.R. (1992). Randomised comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding in patients with persisting neurological dysphagiaBritish Medical Journal304(6839), 1406-1409.
Reason for exclusion: Nature of intervention

Reddy N.P., Simcox D.L., Gupta V., Motta G.E., Coppenger J., Das A., Buch O. (2000). Biofeedback therapy using accelerometry for treating dysphagic patients with poor laryngeal elevation: Case studies. Journal of Rehabilitation Research and Development, 37(3), 361-372.
Reason for exclusion: Not RCT.

Robbins J.A., Kays S.A., Gangon R.E., Hind J.A., Hewitt A.L., Gentry L.R., Taylor A.J. (2007) The effects of lingual exercise in stroke patients with dysphagiaArchives of Physical Medicine and Rehabilitation, 88, 150-8
Reason for exclusion: Not RCT.

Rosenbek J.C., Robbins J., Willford W.O. et al. (1998) Comparing treatment intensities of tactile-thermal application. Dysphagia13, 1-9.
Reason for exclusion: Both groups received intervention of interest, only the intensity was varied across groups.

Rosenbek J.C., Roecker E.B., Wood J.L. et al. (1996). Thermal application reduces the duration of stage transition in dysphagia after strokeDysphagia11, 225-33.
Reason for exclusion: Both groups received intervention of interest, only the intensity was varied across groups.

Shaker R., Easterling C., Kern M., Nitschke T., Massey B., Daniels S., Grande B., Kazandjian M., & Dikeman K. (2002). Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening. Gastroenterology122 (5), 1314-1321.
Reason for exclusion: Nature of intervention.

Sun, S-F., Hsu, C-W., Lin, H-S., Sun, H-P., Chang, P-H., Hsieh, W-L., & Wang, J-L. (2013). Combined neuromuscular electrical stimulation (NMES) and fiberoptic endoscopic evaluation of swallowing (FEES) and traditional swallowing rehabilitation in the treatment of stroke-related dysphagiaDysphagia28, 557-66.
Reason for exclusionQuasi-experimental study design, not RCT.

Sukthankar S.M., Reddy N.P., Canilang E.P., Stephenson L., Thomas R. (1994). Design and development of portable biofeedback systems for use in oral dysphagia rehabilitation. Medical Engineering & Physics16, 430-435
Reason for exclusion:  Population included other patients than those with stroke.

Takahata, H., Tsutsumi, K., Baba, H., Nagata, I., & Yonekura, M. (2011). Early intervention to promote oral feeding in patients with intracerebral hemorrhage: a retrospective cohort study. BMC neurology11(1), 1.
Reason for exclusion: Not RCT.

The FOOD Trial Collaboration. (2005). Effect of timing and method of enteral tube feeding for dysphagic stroke patients (FOOD): A multicentre randomised controlled trial. Lancet, 365, 764–72.
Reason for exclusion:  Nature of the intervention is compensatory.

Theurer, J.A., Johnston, J.L., Fisher, J., Darling, S., Stevens, R.C., Taves, D., Teasell, R., Hachinski, V., & Martin, R.E. (2013). Proof-of-principle pilot study of oropharyngeal air-pulse application in individuals with dysphagia after hemispheric strokeArchives of Physical Medicine and Rehabilitation, 94, 1088-94.
Reason for exclusion: Case-series study design, not RCT.

Whelan K. (2001). Inadequate fluid intakes in dysphagic acute strokeClinical Nutrition20(5), 423-428.
Reason for exclusion: Both groups received a form of the treatment.

Wada, S., Tohara, H., Iida, T., Inoue, M., Sato, M., & Ueda, K. (2012). Jaw-opening exercise for insufficient opening of the upper esophageal sphincter. Archives of Physical Medicine and Rehabilitation93, 1995-9.
Reason for exclusion: Other population than patients with stroke.

Repetitive Transcranial Magnetic Stimulation (rTMS)

Evidence Reviewed as of before: 01-04-2012
Author(s)*: Adam Kagan, B.Sc.; Sarah Bouchard-Cyr; Mylène Boudreau; Amélie Brais; Valérie Hotte; Jo-Annie Paré; Anne-Marie Préville; Mylène Proulx
Patient/Family Information Table of contents

Introduction

Transcranial magnetic stimulation is a pain-free, non-invasive technique used to stimulate the central nervous system. The electric currents necessary to stimulate the brain are produced by rapidly changing magnetic fields that are initiated by a brief high-intensity electric current that passes through a wire coil held over the scalp. The subsequent magnetic field is projected perpendicular to the electric current and is able to passes through the layers of human tissue (skin, bone, cortex) with very little impedence. TMS can be delivered via single-pulse, double-pulse, paired-pulse and repetitive pulse (rTMS). rTMS is the method currently under investigation for use as a treatment for stroke mainly due to its ability to modulate excitability in the cerebral cortex over longer time periods (compared to other types of TMS). It can also enhance some cognitive processes, regulate activity in specific brain regions and provide causal information about the roles of different cortical regions in behavioural performance. The use of rTMS can also enhance neuroplasticity during motor training. Theta burst stimulation is a type of rTMS that has been found to effectively induce synaptic long-term potentiation and depression and is also currently under investigation for use as a treatment therapy for stroke. According to some experimental studies, a stroke would cause a relative hyperactivity of the unaffected hemisphere due to the release from reciprocal inhibition by the opposite hemisphere which would explain some of the dysfunctions observed in this population (Brighina et al, 2003). This phenomenon is called “interhemispheric inhibitory interactions”. Thus inhibitory stimulation (low frequency rTMS) to the unaffected hemisphere could work to curb this problem. In addition, other researchers like Talelli et al. (2007) suggest that excitation of the affected hemisphere (with high frequency rTMS) enhances corticospinal output and leads to promising therapeutic results. Nevertheless, there is still a clear lack of knowledge on the exact mechanisms of TMS.

Note: Only the studies that looked at rTMS as a rehabilitation intervention were considered in this module.

Patient/Family Information

Author: Shreya Prasanna, PhD student

What is Repetitive Transcranial Magnetic Stimulation?

After a stroke, changes in the electrical activity of the cells within your brain take place. These changes may explain why you are experiencing functional problems after the stroke (e.g. difficulty moving your arm or leg). Repetitive Transcranial Magnetic Stimulation (rTMS) is a pain-free, non-invasive technique used to stimulate the cells in your brain. This stimulation alters the electrical activity of cells in targeted areas of the brain. Specifically, pulsed magnetic fields are generated by passing current pulses through a conducting coil. The coil is held close to your scalp so that the pulsed magnetic field passes through the skull and stimulates your brain cells. When this stimulation is delivered at regular intervals, it is termed as rTMS. This therapy has been studied by high quality research studies and has been found beneficial for arm function in patients.

Are there different kinds of rTMS?

rTMS can be applied at low, medium and high frequencies depending on which side of your brain is being treated. A low frequency rTMS is often used to stimulate the part of the brain on the same side as your weaker arm/leg. A medium or high frequency rTMS is used to stimulate the part of the brain on the opposite side of your weaker arm/leg.

Does it work for stroke?

Although the exact mechanisms of rTMS are still being studied, there is evidence that the use of rTMS as an adjunct can help improve hand function for some people after stroke, especially those who already have some use of their hand and arm. For example, research studies have reported that patients who receive rTMS have better control of their affected hand and have better ability to try and manipulate fine objects.

What can I expect?

Typically a session of rTMS is non-invasive and painless. A small, plastic-covered coil is placed against your head to deliver the rTMS. The rTMS is provided for several minutes. You will be required to wear earplugs during this session. It is often followed by a session of physical and/or occupational therapy, which involves exercises to promote the use of your weaker arm and hand.

Side effects/risks?

Common side-effects after a session of rTMS can include a minor headache which often resolves after a few hours or with a dose of acetaminophen (i.e. Tylenol®). A very rare side-effect is the risk of seizures. However, your doctor will examine you thoroughly before beginning this treatment in order to examine the possibility for this risk. Some people should not be treated with rTMS. These include people with: a history of seizures, cardiac pacemakers, and metal implants anywhere in the head or mouth.

Who provides the treatment?

A trained medical technician provides the rTMS. The exercise session following that is provided by a physical or occupational therapist. You can speak to your therapist or physician about whether you are a suitable candidate for rTMS and where you can obtain this treatment.

How many treatments?

The exact number of treatment sessions can vary based on your goals, your needs and your tolerance to the intervention. While there is some variability in regards to the frequency/duration of rTMS treatments as reported in research studies, rTMS is often provided for approximately 5-10 sessions, with each session lasting from 10-25 mins. As such, the frequency/duration of your rTMS treatment sessions will be suggested by your therapist or physician.

Is rTMS for me?

rTMS can be beneficial to those individuals who have difficulty in their arm and hand function after stroke. Studies have shown that rTMS may be useful for individuals who have had a stroke very recently, over the past couple of months and those who have experienced a stroke six or more months ago.

Clinician Information

Note: When reviewing the findings, it is important to note that they are always made according to randomized clinical trial (RCT) criteria – specifically as compared to a control group. To clarify, if a treatment is “effective” it implies that it is more effective than the control treatment to which it was compared. Non-randomized studies are no longer included when there is sufficient research to indicate strong evidence (level 1a) for an outcome.

Repetitive transcranial magnetic stimulation (rTMS) is a non-invasive method of stimulating the central nervous system and is currently being considered as a possible treatment for stroke. rTMS is usually delivered via an electronic device that is placed over the scalp and transmits rapidly changing magnetic fields down through a specific section of the brain. While the exact mechanisms of how rTMS works are still under investigation, it is believed that the changing magnetic fields act to modulate the cortical excitability. Low frequency rTMS appears to lower cortical excitability and is thus usually delivered to the unaffected hemisphere (which can become over active post stroke), while high frequency rTMS raises cortical excitability and is often delivered to the affected hemisphere.

To date, 26 studies are included and reviewed in this module. More specifically: 13 high quality RCTs, two fair quality crossover studies, two quasi-experimental studies, two repeated measures studies, one randomly controlled feasibility study, six pre-post studies.

Note: Low-frequency rTMS implies 1-4Hz, high-frequency rTMS implies 5-10Hz. As well, the term ‘affected’ refers to the brain hemisphere affected by stroke (for example ‘affected motor cortex’ refers to the motor cortex on the affected side of the brain).

Note: Please see the Authors results table and publication abstracts for further details of rTMS (e.g. intensity, motor threshold, location).

Results Table

View results table

Outcomes

Acute phase: Low-frequency rTMS over the affected motor cortex vs. control conditions

Activities of daily living
Effective
1b

One high quality RCTs (Khedr et al., 2005) studied the effect of rTMS on activities of daily living (ADLs) in patients with acute stroke. This high quality RCT found a significant difference on the Barthel Index immediately post-intervention and at a 10-day follow up, following 10 sessions of low-frequency rTMS over the motor cortex of the affected hemisphere compared to sham rTMS. Both groups also received usual care. As well, a significantly higher percentage of patients who received low-frequency rTMS compared to sham rTMS scored in the ‘independent’ range (Barthel Index greater or equal to 75) at the 10-day follow-up only.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the motor cortex of the affected hemisphere is more effective than sham rTMS in improving activities of daily living in patients with acute stroke.

Elbow torque
Insufficient evidence
5

One randomized controlled feasibility study (Pomeroy et al., 2007) investigated the effect of rTMS combined with muscle contraction on elbow torque as measured by an isokinetic dynamometer. No significant effect was found for low-frequency rTMS over the motor cortex of the affected hemisphere, combined with either real or placebo muscle contraction when compared to sham rTMS combined with either real or placebo muscle contraction exercises. However, because it was a feasibility study, it was not powered to find significant differences between groups – nor was it a hypothesis testing study.
Note: This study involved some patients with subacute stroke, however the average time after stroke was 27 days, and the majority of patients were in the acute stage.

Conclusion: There is insufficient scientific evidence (level 5) describing the effect of low-frequency rTMS over the motor cortex of the affected hemisphere on elbow torque of the paretic arm in patients with acute stroke, however it should be noted that one randomized controlled feasibility study found no effect.

Purposeful movement
Insufficient evidence
5

One randomized controlled feasibility study (Pomeroy et al., 2007) investigated the effect of rTMS combined with muscle contraction on purposeful movement measured by the Action Research Arm Test. No significant effect was found for a single session of low-frequency rTMS over the motor cortex of the affected hemisphere, combined with either real or placebo muscle contraction, when compared to sham rTMS combined with either real or placebo muscle contraction exercises. However, because it was a feasibility study, it was not powered to find significant differences between groups – nor was it a hypothesis testing study.
Note: This study involved some patients with subacute stroke, however the average time after stroke was 27 days, and the majority of patients were in the acute stage.

Conclusion: There is insufficient scientific evidence (level 5) describing the effect of low-frequency rTMS over the motor cortex of the affected hemisphere on purposeful movement of the paretic arm in patients with acute stroke, however it should be noted that 1 randomized controlled feasibility study found no effect.

Acute phase: Low-frequency rTMS over the oesophageal motor cortex of both hemispheres simultaneously vs. control conditions

Activities of daily living
Effective
1b

The high quality RCT (Khedr et al., 2010) involved patients with lateral medullary infarction (LMI) or other brainstem infarctions. At post-treatment and at 2-month follow-up the study found a significant difference in ADLs (measured by the Barthel Index) for the LMI patients only, in favour of low-frequency rTMS over the oesophageal motor cortex of both hemispheres, compared to sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the oesophageal motor cortex of both hemispheres is more effective than sham rTMS in improving activities of daily living in patients with acute stroke resulting from lateral medullary infarction.

Dysphagia
Effective
1b

One high quality RCT (Khedr et al., 2010) studied the effect of rTMS on dysphagia in patients with acute stroke. This high quality RCT found a significant difference in dysphagia (measured by a standardized swallowing questionnaire) in favour of a group of patients who received 5 sessions of low-frequency rTMS over the oesophageal motor cortex of both hemispheres (simultaneously), compared to a group who received sham rTMS.

Conclusion: There is moderate (level 1b) evidence from 1 high quality RCT that low-frequency rTMS over the oesophageal motor cortex of both hemispheres is more effective than sham rTMS for improving dysphagia in patients with acute stroke.

Grip strength
Not effective
1b

One high quality RCT (Khedr et al., 2010) studied the effect of rTMS on grip strength in patients with acute stroke. This high quality RCT found no significant difference in grip strength at post-treatment between a group of patients who received 5 sessions of low-frequency rTMS over the oesophageal motor cortex of both hemispheres (simultaneously), and a group who received sham rTMS.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that low- frequency rTMS over the motor cortex of both hemispheres is not more effective than sham rTMS in improving grip strength in patients with acute stroke.

Neurological outcomes and recovery
Not effective
1b

One high quality RCTs (Khedr et al., 2010) studied the effect of rTMS on neurological outcomes and recovery in patients with acute stroke. This high quality RCT found no significant difference in neurological outcomes and recovery (measured by the National Institute of Health stroke Scale) between a group of patients who received 5 sessions of low-frequency rTMS over the oesophageal motor cortex of both hemispheres, compared to a group who received sham rTMS.

Conclusion: There is moderate (level 1b) evidence from 1 high quality RCT that low-frequency rTMS over the oesophageal motor cortex of both hemispheres is not more effective than sham rTMS in improving neurological outcomes and recovery in patients with acute stroke.

Acute phase: Low-frequency rTMS over the unaffected motor cortex vs. control conditions

Grip strength
Not effective
1b

One high quality crossover RCT (Lieperta et al., 2007) studied the effect of rTMS on grip strength in patients with acute stroke. This high quality crossover RCT reported no significant change in grip strength following a single session of low-frequency rTMS over the motor cortex of the unaffected hemisphere compared to sham rTMS.

Conclusion : There is moderate evidence (level 1b) from one high quality crossover RCT that low- frequency rTMS over the motor cortex of the unaffected hemisphere is not more effective than sham rTMS in improving grip strength in patients with acute stroke.

Manual dexterity
Effective
1b

One high quality crossover study (Lieperta et al., 2007) studied the effect of rTMS on manual dexterity in patients with acute stroke. The study reported a significant improvement in the Nine Holes Peg Test (NHPT) following a single session of low-frequency rTMS over the motor cortex of the unaffected hemisphere compared to sham rTMS (control).

Conclusion: There is moderate evidence (level 1b) from one high quality crossover RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving manual dexterity in patients with acute stroke.

Subacute phase: Low-frequency rTMS over the unaffected motor cortex vs. control conditions

Activities of daily living
Effective
1b

One high quality RCT (Emara et al., 2010) investigated the effect of rTMS on activities of daily living in patients with subacute stroke. This high quality RCT randomized patients into 3 groups: 1) low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the motor cortex of the affected hemisphere (high-rTMS), or 3) sham rTMS. All 3 groups also received standard rehabilitation. At 10 days, the study found a significant between-group difference in activities of daily living (measured by the Activity Index) in favour of both low-rTMS and high-rTMS compared to sham rTMS. These differences were maintained over 12 weeks of follow-up.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving activities of daily living in patients with subacute stroke.

Cognitive impairment
Not effective
1b

One high quality RCT (Emara et al., 2010) investigated the effect of rTMS on cognitive impairment in patients with subacute stroke. This high quality RCT randomized patients into 3 groups: 1) low-frequency rTMS over the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the affected hemisphere (high-rTMS), or 3) sham rTMS. In addition, all 3 groups received standard rehabilitation. At 10 days, the study found no significant between-group difference in cognitive impairment (measured by the Mini-Mental State Examination).

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is not more effective than sham rTMS for improving cognitive impairment in patients with subacute stroke.

Grip strength
Effective
2b

One repeated measures study (Dafotakis et al., 2008) examined the effect of rTMS on grip strength in patients with subacute stroke. This repeated measures study found that low-frequency rTMS over the  primary motor cortex of the unaffected hemisphere improved the efficiency of grip force scaling and spatio-temporal scaling coupling between grip and lift forces significantly more than sham rTMS (control).

Conclusion: There is limited evidence (level 2b) from 1 repeated measures study that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective in improving some aspects of grip strength related to object lifting.

Manual dexterity
Effective
1b

One high quality crossover study (Mansur et al., 2005) investigated the effects of rTMS on manual dexterity in patients with subacute stroke. This high quality crossover study  randomised patients to receive the following 3 treatments scenarios in random order: (1) low-frequency rTMS over the primary motor cortex of the unaffected hemisphere (2) low-frequency rTMS over the premotor cortex of the unaffected hemisphere, or (3) sham rTMS (control). The study found a significant improvement in the Purdue Pegboard test following ‘scenario 1’ compared to the sham condition, whereas the improvement was not significant for ‘scenario 2’ compared to the sham condition.

Conclusion1: There is moderate evidence (level 1b) from 1 high quality crossover study that low-frequency rTMS over the primary motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving manual dexterity in patients with subacute stroke.

Quality of life
Effective
1b

One high quality RCT (Emara et al., 2010) investigated the effect of rTMS on quality of life in patients with subacute stroke. This high quality RCT randomized patients to 3 groups: 1) low-frequency rTMS over the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the affected hemisphere (high-rTMS), or 3) sham rTMS. All 3 groups also received standard rehabilitation. At 10 days, the study found a significant between-group difference in quality of life (measured by the Modified Rankin Scale) in favour of both low-rTMS and high-rTMS compared to sham rTMS. These differences were maintained over 12 weeks of follow-up.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS in improving quality of life in patients with subacute stroke.

Reaction time of the hand
Effective
1b

One high quality crossover study (Mansur et al., 2005) investigated the effects of rTMS on reaction time of the hand in patients with subacute stroke. In the study, patients received the following 3 treatments scenarios in random order: (1) low-frequency rTMS over the primary motor cortex of the unaffected hemisphere (2) low-frequency rTMS over the premotor cortex of the unaffected hemisphere, or (3) sham rTMS (control). A significant improvement in simple reaction time, and 4-choice reaction time was found following ‘scenario 1’ compared to the sham condition, however there was no significant improvement reported for the finger tapping test. None of these three tests showed any improvement following ‘scenario 2’ compared to the sham condition.

Conclusion: There is moderate evidence (level 1b) from 1 high quality crossover study that low-frequency rTMS to the primary motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving some aspects of reaction time of the hand in patients with subacute stroke.

Subacute phase: Low-frequency rTMS over the right inferior frontal gyrus vs. control conditions

Aphasia
Effective
1b

One high quality RCT (Weiduschat et al., 2010) investigated the effect of rTMS on aphasia in patients with subacute stroke. This high quality RCT randomized patients with subacute stroke to receive low-frequency rTMS over the right triangular part of the inferior frontal gyrus or sham rTMS. At 2 weeks (following 10 sessions) a significant between-group difference in aphasia (measured by the Aachen aphasia Test) was found in favour of rTMS compared to sham rTMS. It should be noted that both groups also received speech and language therapy.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the right triangular part of the inferior frontal gyrus is more effective than sham rTMS for improving aphasia in patients with subacute stroke.

Subacute Phase: Low-frequency rTMS over the parietal lobe of the unaffected hemisphere vs. control conditions

Unilateral spatial neglect
Effective
2b

One quasi-experimental study (Lim et al. 2010) and 1 pre-post study (Brighina et al, 2003) investigated the effect of rTMS on unilateral spatial neglect in patients with subacute stroke.

The quasi-experimental study (Lim et al. 2010) found a significant between-group difference at 2 weeks (immediately post-treatment) in contra-lesional neglect, measured by the Line bisection test (p=.053), with less neglect found for a group that received low-frequency rTMS group over the parietal area of the unaffected hemisphere combined with behavioural therapy, compared to a group that received behavioural therapy alone.

The pre-post study (Brighina et al, 2003) found a significant improvement in the Length judgment of prebisected lines, the Line bisection task and the Clock drawing task following 2 weeks of low-frequency rTMS over the parietal cortex of the unaffected hemisphere in 3 patients with contralateral visuospatial neglect and right brain ischemic stroke.

Conclusion: There is limited evidence (level 2b) from 1 quasi-experimental study that low-frequency rTMS over the parietal lobe of the unaffected hemisphere + behavioral therapy is more effective than behavioural therapy alone for improving certain aspects of unilateral spatial neglect in patients with subacute stroke. In addition 1 pre-post study found improvements in unilateral spatial neglect in patients with subacute stroke following low-frequency rTMS over the parietal cortex of the unaffected hemisphere.

Subacute phase: High-frequency rTMS over the affected motor cortex vs. control conditions

Activities of daily living
Conflicting
4

Two high quality RCTs (Chang et al., 2010, Emara et al., 2010) investigated the effect of rTMS on activities of daily living in patients with subacute stroke.

The first high quality RCT (Chang et al., 2010) found no significant difference at 2 weeks (post-treatment) or at 3 months (follow-up) in activities of daily living (measured by the Barthel Index) between high-frequency rTMS over the motor cortex of the affected hemisphere combined with motor training, compared to sham rTMS combined with motor training.

The second high quality RCT (Emara et al., 2010) randomized patients into 3 groups: 1) low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the motor cortex of the affected hemisphere (high-rTMS), or 3) sham rTMS. All 3 groups also received standard rehabilitation. At 10 days, the study found a significant between-group difference in activities of daily living (measured by the Activity Index) in favour of both low-rTMS and high-rTMS compared to sham rTMS. These differences were maintained over 12 weeks of follow-up.

Conclusion: There is conflicting evidence (level 4) between 2 high quality RCTs regarding the effect of high-frequency rTMS over the motor cortex of the affected hemisphere on activities of daily living in patients with subacute stroke.

Cognitive impairment
Not effective
1b

One high quality RCT (Emara et al., 2010) investigated the effect of rTMS on cognitive impairment in patients with subacute stroke. This high quality RCT randomized patients into 3 groups: 1) low-frequency rTMS over the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the affected hemisphere (high-rTMS), or 3) sham rTMS. In addition, all 3 groups received standard rehabilitation. At 10 days, the study found no significant between-group difference in cognitive impairment (measured by the Mini-Mental State Examination).

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS in improving cognitive impairment in patients with subacute stroke.

Grip strength
Not effective
1b

One high quality RCT (Chang et al., 2010) examined the effect of rTMS on grip strength in patients with subacute stroke. This high quality RCT found no significant difference at 2 weeks (immediately post-treatment) or at 3 months post-stroke in grip strength between a group of patients who received high-frequency rTMS over the motor cortex of the affected hemisphere combined with motor training, compared to sham rTMS combined with motor training. However it should be noted that this study may not have been adequately powered (n=28) and that a within-group pre-post improvement in grip strength was found for the real rTMS group, but not the sham rTMS group at 3 months post-stroke.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving grip strength in patients with subacute stroke. However it should be noted that this study may not have been adequately powered (n=28) and that a within-group pre-post improvement in grip strength was found for real rTMS group, but not sham rTMS group at 3 months post-stroke.

Manual dexterity
Not effective
1b

One high quality RCT (Chang et al., 2010) investigated the effects of rTMS on manual dexterity in patients with subacute stroke. This high quality RCT found no significant difference at 2 weeks (post-treatment) or at 3 months post-stroke in manual dexterity, as measured by the Box and Block Test, between high-frequency rTMS over the motor cortex of the affected hemisphere combined with motor training, compared to sham rTMS combined with motor training.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving manual dexterity in patients with subacute stroke.

Mobility
Not effective
1b

One high quality RCT (Chang et al., 2010) investigated the effect of rTMS on lower extremity motor function in patients with subacute stroke. There were no significant differences found at either post-treatment (2 weeks), or at follow-up (3 months post stroke) on the Functional Ambulation Category between a group of patients who received high-frequency rTMS over the motor cortex of the affected hemisphere combined with motor training, compared to sham rTMS combined with motor training.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT, that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving mobility in patients with subacute stroke.

Motor function (lower extremity)
Not effective
1b

One high quality RCT (Chang et al., 2010) investigated the effect of rTMS on lower extremity motor function in patients with subacute stroke. There were no significant differences found at either post-treatment (2 weeks), or at follow-up (3 months post stroke) on the leg score of the Motricity Index (MI-A) or the Fugl-Meyer Assessment –lower limb score between a group of patients who received high-frequency rTMS over the primary motor cortex of the affected hemisphere combined with motor training, compared to sham rTMS combined with motor training.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT, that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving lower extremity motor function in patients with subacute stroke.

Motor function (upper extremity)
Effective
1b

One high quality RCT (Chang et al., 2010) investigated the effects of rTMS on upper extremity motor function in patients with subacute stroke. This high quality RCT found a significant difference at 2 weeks (post-treatment) in motor function (measured by the arm section of the Motricity Index) in favour of high-frequency rTMS over the motor cortex of the affected hemisphere combined with motor training (hi-rTMS), compared to sham rTMS combined with motor training. Additionally a significant group X time interaction was found at 3-months post-stroke suggesting that hi-rTMS may have resulted in additional improvements that lasted at 3 months after onset of stroke.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT, that high-frequency rTMS over the motor cortex of the affected hemisphere is more effective than sham rTMS for improving upper extremity motor function in the short-term in patients with subacute stroke. While a significant group by time interaction indicated that real rTMS may have resulted in additional improvements that lasted 3 months after onset of stroke, the between-group difference at 3 months was not significant.

Quality of life
Effective
1b

One high quality RCT (Emara et al., 2010) investigated the effect of rTMS on quality of life in patients with subacute stroke. This high quality RCT randomized patients to 3 groups: 1) low-frequency rTMS over the unaffected hemisphere (low-rTMS), 2) high-frequency rTMS over the affected hemisphere (high-rTMS), or 3) sham rTMS. All 3 groups also received standard rehabilitation. At 10 days, the study found a significant between-group difference in quality of life (measured by the Modified Rankin Scale) in favour of both low-rTMS and high-rTMS compared to sham rTMS. These differences were maintained over 12 weeks of follow-up.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that high-frequency rTMS over the motor cortex of the affected hemisphere is more effective than sham rTMS in improving quality of life in patients with subacute stroke.

Chronic phase: Bilateral rTMS (Low-frequency rTMS over the unaffected motor cortex combined with high frequency rTMS over the affected motor cortex) vs. control conditions

Pinch acceleration
Effective
1b

One high quality RCT (Takeuchi et al., 2009) investigated the effect of rTMS on pinch acceleration in patients with chronic stroke. This high quality RCT randomized patients into 3 groups: 1) low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS) 2) high-frequency rTMS over the motor cortex of the affected hemisphere (high-rTMS), or 3) bilateral rTMS (bi-rTMS), which consisted of low-rTMS combined with hi-rTMS. All 3 groups also received motor training. At post-treatment (1 session) a significant between-group difference in pinch acceleration (measured by a monoaxial accelerometer) was found in favour of both bi-rTMS and low-rTMS compared to high-rTMS and these differences were maintained at 7-day follow-up.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that bilateral rTMS, involving low-frequency rTMS over the unaffected motor cortex (low-rTMS) combined with high-frequency rTMS over the affected motor cortex (high-rTMS) is more effective than high-rTMS alone for improving pinch acceleration in patients with chronic stroke.

Pinch force
Effective
1b

One high quality RCT (Takeuchi et al., 2009) investigated the effect of rTMS on pinch force in patients with chronic stroke. This high quality RCT randomized patients into 3 groups: 1) low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS) 2) high-frequency rTMS over the motor cortex (high-rTMS) of the affected hemisphere, or 3) bilateral rTMS (bi-rTMS), which consisted of low-rTMS combined with hi-rTMS. All 3 groups also received motor training. At post-treatment (1 session) and 7-day follow-up, a significant between-group difference was found in pinch force (measured by a pinch gauge), in favour of bi-rTMS compared to both high- and low-rTMS.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that bilateral rTMS, involving low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS) combined with high-frequency rTMS over the motor cortex of the affected hemisphere (high-rTMS) is more effective for improving pinch force compared to either low-rTMS or high-rTMS alone, in patients with chronic stroke.

Chronic phase: Excitatory theta burst stimulation over the motor cortex of the affected hemisphere and Inhibitory theta burst stimulation over the motor cortex of the unaffected hemisphere vs. control conditions

Grip strength
Not effective
2a

One fair quality cross-over study (Talelli et al., 2007) investigated the impact of rTMS on grip strength in patients with chronic stroke. The study reported no significant effects on grip strength following either excitatory theta burst stimulation (iTBS) over the motor cortex of the affected hemisphere, inhibitory theta burst stimulation (cTBS) over the motor cortex of the unaffected hemisphere or sham stimulation.
Note:  iTBS involved 20 trains of 10 theta bursts with 8-sec intervals (600 bursts) whereas cTBS involved 100 continuous trains of theta burst stimulation.
Note: This study involved only 6 patients and thus may not have been adequately powered to provide significant results.

Conclusion: There is limited evidence (level 2a) from 1 fair quality crossover study that excitatory theta burst stimulation over the motor cortex of the affected hemisphere or inhibitory theta burst stimulation over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving grip strength in patients with chronic stroke.

Reaction time of the hand
Effective
2a

One fair quality crossover study (Talelli et al., 2007) investigated the impact of rTMS on reaction time and speed of the paretic hand of 6 patients with chronic stroke. This fair quality cross-over study found significant improvement in simple reaction time with the application of excitatory stimulation (iTBS) over the affected cortex compared to inhibitory stimulation (cTBS) over the unaffected hemisphere immediately after stimulation, and compared to sham stimulation up to 30 minutes after stimulation. No significant improvement was found for choice reaction time for any of the 3 conditions.
Note: iTBS involved 20 trains of 10 the same theta bursts with 8-sec intervals (600 bursts) whereas cTBS involved 100 continuous trains of theta burst stimulation.

Conclusion: There is limited evidence (level 2a) from one fair quality crossover study, that excitatory theta burst stimulation over the motor cortex affected hemisphere is more effective than inhibitory theta burst stimulation over the primary cortex of the unaffected hemisphere (immediately after stimulation only)  or sham rTMS (up to 30 minutes after stimulation) for improving simple reaction time in patients with chronic stroke.

Chronic phase: Low-frequency rTMS over the both sides of the brain vs. control conditions

Activities of daily living
Insufficient evidence
5

One pre-post study (Mally & Dinya, 2008) investigated the effect of rTMS on activities of daily living (ADLs) in patients with chronic stroke. This pre-post study divided participants into 4 groups. Group A consisted of patients who had movement in the paretic arm that could be evoked by a TMS pulse to either hemisphere of the brain. Group B consisted of patients who had no paretic arm movement evoked from either side of the brain; the pathway to the healthy arm was stimulated from where visible movement could be evoked. Patients in Group C had paretic arm movement that could only be evoked from the contralateral side of the brain, while patients in group D had paretic arm movement that could only be evoked from the ipsilateral side of the brain. Only patients in group B improved in functional activities (dressing, catching and walking as measured by a 4 point scale) following 1-week of low-frequency rTMS (where the region of the brain stimulated during treatment corresponded with the group to which the patient belonged).

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of low-frequency rTMS over the both sides of the brain on activities of daily living in patients with chronic stroke. However it should be noted that one pre-post study found a significant improvement in ADLs following low-frequency rTMS over the both sides of the brain in patients who had no initial paretic arm movement evoked from either side of the brain.

Lower extremity movement (either hemisphere)
Insufficient evidence
5

One pre-post study (Mally & Dinya, 2008) investigated the effect of rTMS on lower extremity movement in patients with chronic stroke. Participants were divided into 4 groups. Group A consisted of patients who had a movement in the paretic arm that could be evoked by a TMS pulse (low-frequency) to either hemisphere of the brain. Group B consisted of patients who had no paretic arm movement evoked from either side of the brain; the pathway to the healthy arm was stimulated from where visible movement could be evoked. Patients in Group C had paretic arm movement that could only be evoked from the contralateral side of the brain, while patients in group D had paretic arm movement that could only be evoked from the ipsilateral side of the brain. Patients in group B and C improved significantly in lower extremity movement (as measured by several 4 point scales) following a 1-week program of low-frequency rTMS (the region of the brain stimulated during treatment corresponded with the group to which the patient belonged).

Conclusion: While there is insufficient scientific evidence (level 5) that rTMS improves lower extremity movement in patients with chronic stroke, 1 pre-post study found that patients who received low-frequency rTMS to the motor cortex of either the unaffected or the affected hemisphere showed some improvements.

Spasticity of the hand
Insufficient evidence
5

One pre-post study (Mally & Dinya, 2008) investigated the effect of rTMS on hand spasticity in patients with chronic stroke. This pre-post study divided patients with chronic stroke into 4 groups. Group A consisted of patients who had a movement in the paretic arm that could be evoked by a TMS pulse (low-frequency) to either hemisphere of the brain. Group B consisted of patients who had no paretic arm movement evoked from either side of the brain; the pathway to the healthy arm was stimulated from where visible movement could be evoked. Patients in Group C had paretic arm movement that could only be evoked from the contralateral side of the brain, while patients in group D had paretic arm movement that could only be evoked from the ipsilateral side of the brain. Patients in group A, B and C improved significantly in finger spasticity (as measured by a 4-point scale), with group B improving the most, following a 1-week program of low-frequency rTMS where the region of the brain stimulated during treatment corresponded with the group to which the patient belonged.

Conclusion: There is insufficient scientific evidence (level 5) showing an effect of low-frequency rTMS over the both sides of the brain on spasticity in patients with chronic stroke, however 1 pre-post study found significant within-group improvements in spasticity when rTMS was applies to either the affected or unaffected hemisphere, especially when applied to the affected hemisphere of patients with no movement evoked potential of the paretic arm from TMS to the affected hemisphere.

Upper extremity movement (either hemisphere)
Insufficient evidence
5

One pre-post study (Mally & Dinya, 2008) investigated the effect of rTMS on overall upper extremity movement in patients with chronic stroke. Participants were divided into 4 groups. Group A consisted of patients who had a movement in the paretic arm that could be evoked by a TMS pulse (low-frequency) to either hemisphere of the brain. Group B consisted of patients who had no paretic arm movement evoked from either side of the brain; the pathway to the healthy arm was stimulated from where visible movement could be evoked. Patients in Group C had paretic arm movement that could only be evoked from the contralateral side of the brain, while patients in group D had paretic arm movement that could only be evoked from the ipsilateral side of the brain. Patients in group B and C improved significantly in upper extremity movement (as measured by several 4 point scales) following a 1-week program of low-frequency rTMS (the region of the brain stimulated during treatment corresponded with the group to which the patient belonged).

Conclusion: While there is insufficient scientific evidence (level 5) that rTMS improves overall upper extremity movement in patients with chronic stroke, 1 pre-post study found that patients who received low-frequency rTMS to the unaffected hemisphere, especially those who had no evoked movement from either hemisphere before treatment, showed some improvements.

Chronic phase: Low-frequency rTMS over the left prefrontal cortex vs. control conditions

Activities of daily
Not effective
1b

One high quality RCT (Kim et al., 2010) investigated the effect of rTMS on activities of daily living (ADLs) in patients with chronic stroke. This high quality RCT found no significant difference in ADLs (measured by the Barthel Index) at 2 weeks (immediately post-treatment) between low-frequency rTMS over the left prefrontal cortex, high-frequency rTMS over the left prefrontal cortex and sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the left prefrontal cortex  is not more effective than sham rTMS in improving activities of living in patients with chronic stroke.

Cognitive impairment
Not effective
1b

One high quality RCT (Kim et al., 2010) investigated the effects of rTMS on cognitive impairment in patients with chronic stroke. This high quality RCT found no significant difference in cognitive impairment (measured by the Mini-Mental State Examination) at 2 weeks (immediately post-treatment) between low-frequency rTMS over the left prefrontal cortex, high-frequency rTMS over the left prefrontal cortex and sham rTMS.

Conclusion: There is moderate evidence (level 1b) that low-frequency rTMS over the left prefrontal cortex, is not more effective than sham rTMS in improving cognitive impairment in patients with chronic stroke.

Mood
Not effective
1b

One high quality RCT (Kim et al., 2010) investigated the effect of rTMS on mood in patients with chronic stroke. This high quality RCT found a significant difference in mood (measured by the Beck Depression Scale) at post-treatment (2 weeks) in favour of high-frequency rTMS over the left prefrontal cortex compared to low-frequency rTMS over the left prefrontal cortex or sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the left prefrontal cortex or sham rTMS is less effective than high-frequency rTMS over the left prefrontal cortex in improving mood in patients with chronic stroke.

Chronic phase: Low-frequency rTMS over the right Broca's area

Aphasia
Insufficient evidence
5

One pre-post study (Naeser et al., 2005) investigated the effect of rTMS on patients with chronic stroke and chronic aphasia. The study found some short-term improvements in naming (as measured by the Snodgrass and Vanderwart) as well as some longer lasting improvement in naming (as measured by the Boston Naming test and the Boston Diagnostic aphasia Exam) following 2 weeks of low-frequency rTMS over the anterior portion of the right Broca’s area.

Conclusion: While there is insufficient scientific evidence (level 5) that rTMS has an effect on aphasia in patients with chronic stroke, one pre-post study showed some improvements in naming ability following low-frequency rTMS to the right Broca’s area.

Chronic phase: Low-frequency rTMS over the unaffected motor cortex vs. control conditions

Manual dexterity
Effective
1b

One high quality RCT (Fregni et al., 2006) investigated the effect of rTMS on manual dexterity in patients with chronic stroke. This high quality RCT reported significant improvement on the Purdue Pegboard test and Jebsen-Taylor Hand Function Test for subjects who received 5 sessions over 5 days of low-frequency rTMS over the motor cortex of the unaffected hemisphere, compared to those who received sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere  is more effective than sham rTMS for improving manual dexterity in patients with chronic stroke.

Mood
Insufficient evidence
5

One repeated measures study (Boggio et al., 2006) investigated the effect of rTMS on mood in patients with chronic stroke. This repeated measures study showed no improvement in mood (measured by a visual analogue scale) following low-frequency rTMS over the motor cortex of the unaffected hemisphere.

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of low-frequency rTMS over the contralateral hemisphere on mood in patients with chronic stroke, however it should be noted that 1 repeated measures study found no improvements following treatment.

Motor function (upper extremity)
Insufficient evidence
5

One pre-post study (Kakuda et al., 2011) investigated the effects of rTMS on motor function in patients with chronic stroke. Patients were divided based on Brunnstrom stage of recovery for hand-fingers into 3 groups: stage III, stage IV, & stage V. At 15 days, the study found an improvement in all groups on the Fugl-Meyer Assessment – upper extremity (FMA-UE) and Wolf Motor Function Test – upper extremity following low-frequency rTMS over the motor cortex of the unaffected hemisphere combined with occupational therapy. Patients in stage IV improved significantly more than the other 2 stages on the FMA, and patients in stage III improved significantly less than the other 2 stages on the WMFT. The authors concluded that rTMS appears to improve motor function, and that outcomes are influenced by baseline severity of upper limb hemi-paresis.
Note: This study did not compare the intervention to a control group; therefore results of this study were not used to inform levels of evidence. The study was included in this review, however, to note the effect of different baseline severity on outcome.

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of rTMS on upper extremity motor function in patients with chronic stroke.  However, 1 pre-post study found some improvement in motor function following low-frequency rTMS over the motor cortex of the unaffected hemisphere.

Pinch acceleration
Effective
1a

Two high quality RCTs (Takeuchi et al., 2005Takeuchi et al., 2009) investigated the effect of rTMS on pinch acceleration in patients with chronic stroke.

The first high quality RCT (Takeuchi et al., 2005) reported significantly greater pinch acceleration (measured by a monoaxial accelerometer) at post-treatment (single session) in favour of low-frequency rTMS over the motor cortex of the unaffected hemisphere compared to sham rTMS. However the between-group difference did not remain at 30 minutes post-intervention. Both groups also received motor training.

The second high quality RCT (Takeuchi et al., 2009) randomized patients into 3 groups: 1) low-frequency rTMS over the motor cortex of the unaffected hemisphere (low-rTMS) 2) high-frequency rTMS over the motor cortex of the affected hemisphere (high-rTMS), or 3) bilateral rTMS (bi-rTMS), which consisted of low-rTMS combined with hi-rTMS. All 3 groups also received motor training. At post-treatment (1 session) a significant between-group difference in pinch acceleration (measured by a monoaxial accelerometer) was found in favour of both bi-rTMS and low-rTMS compared to high-rTMS and these differences were maintained at 7-day follow-up.

Conclusion: There is strong evidence (level 1a) from 2 high quality RCTs that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than control conditions (sham rTMS, high-frequency rTMS) for improving pinch acceleration in patients with chronic stroke. It should be noted that one study demonstrated immediate effects only.

Pinch force
Not effective
1b

One high quality RCT (Takeuchi et al., 2005) investigated the effect of rTMS on pinch force in patients with chronic stroke. This high quality RCT found no significant difference in pinch force (measured by a pinch gauge) at post-treatment between 1 session of low-frequency rTMS over the unaffected motor cortex compare to sham rTMS. Both groups also received motor training.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is not more effective than sham rTMS in improving pinch force in patients with chronic stroke.

Range of motion of the hand
Insufficient evidence
5

One repeated measures study (Boggio et al., 2006) investigated the effect of rTMS on hand range of motion in patients with chronic stroke. This repeated measures study found a marked improvement in fingers and thumb range of motion (measured by angle of extension) following a single session of low-frequency rTMS over the motor cortex of the unaffected hemisphere and these improvements were maintained at the 4-month follow-up. No changes were found following sham rTMS.
Note: This study only involved 1 patient and did not do multiple baseline assessments beforehand; therefore results of this study were not used to inform levels of evidence.

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of rTMS on hand range of motion. However, 1 repeated measures study found some improvement motion following low-frequency rTMS.
Note:
This repeated measures study was deemed unqualified to inform levels of evidence.

Reaction time of the hand
Effective
1b

One high quality RCT (Fregni et al., 2006) investigated the impact of rTMS on reaction time and speed of the paretic hand in patients with chronic stroke. This high quality RCT reported significant improvement in simple reaction time and choice reaction time for subjects who received 5 sessions over 5 days of low-frequency rTMS over the motor cortex of the unaffected hemisphere compared to those who received sham rTMS.

Conclusion: There is moderate evidence (Level 1b) from 1 high quality RCT that suggests that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS  for improving reaction time of the paretic hand in patients with chronic stroke.

Spasticity of the hand
Insufficient evidence
5

One repeated measures study (Boggio et al., 2006) investigated the effect of rTMS on hand spasticity in patients with chronic stroke. This repeated measures study reported no effect of low-frequency rTMS over the motor cortex of the unaffected hemisphere on spasticity (measured by the Modified Ashworth Scale) in a 74-year-old woman with chronic stroke.
Note: This study only involved 1 patient and did not to multiple baseline assessments beforehand; therefore results of this study were not used to inform levels of evidence.

Conclusion: There is insufficient scientific evidence (level 5) showing an effect of low-frequency rTMS over the motor cortex of the unaffected hemisphere on spasticity in patients with chronic stroke, however 1 low quality repeated measures study found no improvement in spasticity following low-frequency rTMS to the unaffected hemisphere.

Chronic phase: Low-frequency rTMS over the unaffected parietal lobe vs. control conditions

Cognitive impairment
Insufficient evidence
5

One pre-post study (Shindo et al., 2006) investigated the effects of rTMS on cognitive impairment in patients with chronic stroke. This pre-post study found no change in cognitive impairment or dementia (measure by the Mini-Mental State Examination and the Revised Hasegawa Dementia Scale) following 2 weeks of low-frequency rTMS over the parietal cortex of the unaffected hemisphere.

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of low-frequency rTMS over the parietal cortex of the unaffected hemisphere on cognitive impairment in patients with chronic stroke. However, it should be noted that one pre-post study found no effect of treatment on cognitive impairment or dementia.

Chronic phase: High-frequency rTMS over the affected motor cortex vs. control conditions

Activities of daily living
Not effective
2b

One quasi-experimental study (Izumi et al., 2008) investigated the effect of rTMS on activities of daily living (ADLs) in patients with chronic stroke. This quasi-experimental study found no significant difference at 4 weeks (immediately post-treatment) in activities of daily living (measured by the Barthel Index) between high-frequency rTMS over the motor cortex of the affected hemisphere during maximum finger or thumb extension and sham rTMS.

Conclusion: There is limited evidence (level 2b) from one quasi-experimental study that high-frequency rTMS over motor cortex of the affective hemisphere is not more effective than sham rTMS for improving activities of daily living in patients with chronic stroke.

Hand function
Not effective
2b

One quasi-experimental study (Izumi et al., 2008) investigated the effect of rTMS on overall hand function in patients with chronic stroke. This study found no significant difference at 4 weeks (immediately post-treatment) in overall hand function, as measured by Brunnstrom’s protocol, the Manual Function Test, and the hand items of the stroke Impairment Assessment Set, between high-frequency rTMS over the motor cortex of the affected hemisphere during maximum finger or thumb extension compared to sham rTMS (control). However a trend towards significance was found for the Manual Function Test in favour of the real rTMS group.
Note: This study only involved 9 subjects and thus may not have been powered to find significant results.

Conclusion: There is limited evidence (level 2b) from 1 quasi-experimental study showing that high-frequency rTMS over the motor cortex of the affected hemisphere, during maximum finger or thumb extension is not more effective than sham rTMS for improving overall hand function in patients with chronic stroke. It should be noted that this study may not have been powered to find significant results.

Manual dexterity
Effective
1b

One high quality cross-over study (Kim et al., 2006) investigated the effect of rTMS on manual dexterity in patients with chronic stroke. This high quality cross-over study showed significant improvement in movement accuracy and movement time of paretic fingers (as measured by a sequential motor task) with the application of 1 session of high-frequency rTMS over the motor cortex of the affected hemisphere compared to sham rTMS combined with the same movement tasks.
Note: The positive change in movement accuracy was related to increased cortical excitability following the real rTMS condition.

Conclusion: There is moderate evidence (level 1b), from 1 high quality crossover study that high-frequency rTMS over the motor cortex of the affected hemisphere is effective than sham rTMS for improving manual dexterity in patients with chronic stroke.

Range of motion of the hand
Insufficient evidence
5

One randomized cross-over study (Koganemaru et al., 2010) investigated the effect of rTMS on hand range of motion in patients with chronic stroke. This randomized crossover study randomized patients to receive, in random order: 1) high-frequency rTMS over the affected hemisphere (rTMS), 2) extensor motor training (EMT) and 3) both interventions combined (rTMS+EMT). At post-treatment (1 session), no within-group improvements were found for any of the 3 groups. However, when rTMS+EMT was continued for a further 8 weeks, a within-group improvement in hand range of motion (measurement tool not described) was found.
Note: This study did not compare rTMS to a control group; therefore results of this study were not used to inform levels of evidence.

Conclusion: There is insufficient scientific evidence (level 5) regarding the effect of rTMS on hand range of motion. However, 1 randomized crossover trial found some improvement motion following high-frequency rTMS.
Note:
This randomized crossover trial was deemed unqualified to inform levels of evidence.

Spasticity of the hand
Not effective
2b

One fair quality randomized cross-over study (Koganemaru et al., 2010) and one quasi-experimental study (Izumi et al., 2008) investigated the effect of rTMS on hand spasticity in patients with chronic stroke.

In the fair quality randomized crossover trial (Koganemaru et al., 2010), patients received (in random order) a single session of: 1) high-frequency rTMS over the motor cortex of the affected hemisphere (rTMS), 2) extensor motor training (EMT) and 3) both interventions combined (rTMS+EMT). No between-group comparisons were reported in this study*. However it should be noted that at post-treatment a significant improvement in hand spasticity (Modified Ashworth Scale) was found for the rTMS+EMT group only. In addition, patients continued receiving rTMS+EMT for 8 weeks. At the end of 8 weeks significant improvements were found for spasticity.
* Between-group comparisons were not reported; therefore results of this study were not used to inform levels of evidence.

The quasi-experimental study (Izumi et al., 2008) found no significant difference at 4 weeks (post-treatment) in paretic hand spasticity (measured by the Modified Ashworth Scale) between high-frequency rTMS over the motor cortex of the affected hemisphere during maximum finger or thumb extension vs. sham rTMS. However a tendency towards significance was found for wrist spasticity in favour of the real rTMS group.
Note: This study only involved 9 subjects and thus may not have been adequately powered to find significant results.

Conclusion: There is limited evidence (level 2b) from 1 quasi-experimental study that high-frequency rTMS over the motor cortex of the affected hemisphere, during maximum finger or thumb extension is not more effective than sham rTMS for improving spasticity in patients with chronic stroke. However, it should be noted that one randomized crossover study found a significant within-group improvement following high-rTMS over the motor cortex of the affected hemispherecombined with extensor motor training.

Stroke outcomes
Not effective
2b

One quasi-experimental study (Izumi et al., 2008) investigated the effects of rTMS on stroke severity and overall function in patients with chronic stroke. The study found no significant difference at 4 weeks (immediately post-treatment) in overall stroke impairment (measured by the stroke Impairment Assessment Set) between high-frequency rTMS over the motor cortex of the affected hemisphere during maximum finger or thumb extension vs. sham rTMS (control).
Note: This study only involved 9 subjects and thus may not have been powered to find significant results.

Conclusion: There is limited evidence (level 2b) from one quasi-experimental study showing that high-frequency rTMS over the motor cortex of the affected hemisphere is not more effective than sham rTMS for improving overall stroke impairment in patients with chronic stroke.

Chronic phase: High-frequency rTMS over the left prefrontal cortex vs. control conditions

Activities of daily
Not effective
1b

One high quality RCT (Kim et al., 2010) investigated the effect of rTMS on activities of daily living (ADLs) in patients with chronic stroke. This high quality RCT found no significant difference in ADLs (measured by the Barthel Index) at 2 weeks (immediately post-treatment) between high-frequency rTMS over the left prefrontal cortex, low-frequency rTMS over the left prefrontal cortex and sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that both low-frequency rTMS over the left prefrontal cortex and high-frequency rTMS over the left prefrontal cortex are not more effective than sham rTMS in improving activities of daily living in patients with chronic stroke.

Cognitive impairment
Not effective
1b

One high quality RCT (Kim et al., 2010) investigated the effects of rTMS on cognitive impairment in patients with chronic stroke. This high quality RCT found no significant difference in cognitive impairment (measure by the Mini-Mental State Examination) at 2 weeks (immediately post-treatment) between high-frequency rTMS over the left prefrontal cortex, low-frequency rTMS over the left prefrontal cortex and sham rTMS.

Conclusion: There is moderate evidence (level 1b) that both low-frequency rTMS over the left prefrontal cortex, and high-frequency rTMS over the left prefrontal cortex are not more effective than sham rTMS in improving cognitive impairment in patients with chronic stroke.

Mood
Effective
1b

One high quality RCT (Kim et al., 2010) investigated the effect of rTMS on mood in patients with chronic stroke. This high quality RCT found a significant difference in mood (measured by the Beck Depression Scale) at post-treatment (2 weeks) in favour of high-frequency rTMS over the left prefrontal cortex compared to low-frequency rTMS over the left prefrontal cortex or sham rTMS.

Conclusion: There is moderate evidence (level 1b) from 1 high quality RCT that high-frequency rTMS over the left prefrontal cortex is more effective than low-frequency rTMS over the left prefrontal cortex or sham rTMS in improving mood in patients with chronic stroke.

Chronic phase: High-frequency rTMS over the unaffected motor cortex vs. control conditions

Safety of rTMS
Insufficient evidence
5

One pre-post study (Carey et al., 2007) investigated the safety of rTMS on patients with chronic stroke. The study found no significant impairment of overall function after high-frequency rTMS over the motor cortex of the unaffected hemisphere as measured by the Wechsler Adult Intelligence Scale-third edition, Beck Depression Inventory-Second edition or the NIH stroke Scale at post treatment or follow-up. Interviews with the patients on treatment day showed some tiredness, headache, anxiety and nausea. There was a significant impairment shown by the HVLT-R (Hopkins Verbal Learning Test-Revised) for word memory at post-test, but the score returned to normal at follow-up over the next 5 days. As well, there was no significant impairment of the fingers motor control of the normal and paretic hand with the finger-tracking performance test at post-test and follow-up.

Conclusion: While there is insufficient scientific evidence (level 5) describing whether or not rTMS is safe for patient with chronic stroke, one pre-post study concluded that high-frequency rTMS over the unaffected hemisphere does not cause any profound negative impact on daily function. Although some minor impairments were found immediately post treatment in this study, the problems faded at subsequent follow-up tests.

Pediatric - chronic phase: Low-frequency rTMS over the unaffected motor cortex vs. control conditions

Grip strength
Effective
1b

One high quality RCT (Kirton et al., 2008) studied the effects of rTMS on grip strength in children with chronic stroke. The study reported a significant between-group difference at 1-day follow-up and 7-day follow-up for grip strength (measured by a dynamometer) in favour of 8 days of low-frequency rTMS over the motor cortex of the unaffected hemisphere vs. sham rTMS.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving grip strength in children with chronic stroke.

Upper extremity motor function
Effective
1b

One high quality RCT (Kirton et al., 2008) studied the effects of rTMS on upper extremity motor function in children with chronic stroke. The results showed a significant improvement at a 1-day follow-up in upper extremity motor function (measured by the Melbourne Assessment of Upper Extremity Function) in favour of 8 days of low-frequency rTMS over the motor cortex of the unaffected hemisphere vs. sham rTMS, however the difference was no longer significant at a 1-week follow-up.

Conclusion: There is moderate evidence (level 1b) from one high quality RCT that low-frequency rTMS over the motor cortex of the unaffected hemisphere is more effective than sham rTMS for improving upper extremity motor function at 1-day follow-up in children with chronic stroke. However, this difference was no longer significant at 1-week follow-up.

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