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Swallowing Training Combined With Game-Based Biofeedback in Poststroke Dysphagia
PM R XXX (2016) 1-7
www.pmrjournal.org
Original Research
Swallowing Training Combined With Game-Based Biofeedback in Poststroke Dysphagia Chih-Ming Li, MD, PhD, Tyng-Guey Wang, MD, Hsiao-Yu Lee, MS, Hsueh-Pei Wang, MS, Shang-Heng Hsieh, MS, Michelle Chou, BS, Jia-Jin Jason Chen, PhD
Abstract Background: For patients with dysphagia due to stroke, in addition to compensatory strategies, exercises are used to help improve motor function. Biofeedback is used in neuromuscular training and is promising for swallowing training. Objective: To evaluate the functional value of game-based biofeedback in swallowing therapy for patients with poststroke dysphagia. Design: A case-control study. Setting: Academic tertiary hospital. Participants: Subjects with poststroke dysphagia (n ¼ 20) were individually matched to 2 separate groups, a game-based biofeedback group (n ¼ 10) or a control group (n ¼ 10), for age, gender, duration of dysphagia, and dysphagia grades. Interventions: Each participant underwent 1-hour sessions 3 times per week for a total of 16 treatment sessions. Each session included a 30-minute session of traditional swallow treatment and a 30-minute session of laryngeal elevation exercises. In the experimental group, laryngeal elevation exercises were combined with additional game-based biofeedback. Main Outcome Measures: Outcomes assessed before and after interventions included hyoid bone displacement, Functional Oral Intake Scale (FOIS) scores, and nasogastric (NG) tube removal rate. Results: Intergroup analyses showed larger differences in hyoid bone displacement and FOIS scores (before and after treatment) in the experimental group than in the control group, with statistical significance (P ¼ .007 and P ¼ .014, respectively). Intergroup analyses showed that the hyoid bone displacement change and FOIS scores before and after treatment exhibited statistically significant improvement only in the experimental group (P ¼ .002 and P ¼ .004, respectively). In all, 8 of 10 patients (80%) in the experimental group and 2 of 10 patients (20%) in the control group discontinued NG tube insertion after therapy. Participation in the experimental group was associated with an increased probability of tube removal (odds ratio ¼ 6.00; 95% confidence interval ¼ 1.08-33.27, P ¼ .009). Conclusions: Laryngeal elevation training combined with game-based biofeedback augments the change in hyoid bone displacement and FOIS scores, and increases the NG tube removal rate in patients with poststroke dysphagia.
Introduction Dysphagia, which can result from a wide variety of disorders, is seen in 16%-64% of individuals who have sustained a stroke [1-4]. Exercise, in addition to compensatory strategies, can often improve motor function in patients who have acquired dysphagia following a stroke [5,6]. The effortful swallow and the Mendelsohn maneuver are 2 common compensatory strategies for oropharyngeal dysphagia. The effortful swallow increases the oropharyngeal swallow pressure
and augments posterior motion of the tongue base [6]. The Mendelsohn maneuver prolongs and widens the cricopharyngeal opening by extending and sustaining laryngeal elevation during swallowing [6]. However, indiscernible motion or impaired sensation in the oropharynx often hinders patients’ self-awareness during therapeutic procedures. To help patients sense their deglutition, speech therapists have looked for easier methods of providing oral feedback or gestural cues [7,8]. Biofeedback uses specialized equipment to convert subconscious
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Game-Based Swallowing Training
physiologic information into visual or auditory signals, helping patients to sense and manipulate physiological changes to improve their performance [9]. Although biofeedback is commonly used in neuromuscular training, it has not been widely applied to dysphagia treatment. Only a small number of investigations on biofeedback-assisted swallowing training have been conducted, with a focus mainly on laryngeal elevation by electromyography (EMG) or use of accelerometers [8,10-14]. In 1 such experiment, Crary applied biofeedback techniques on swallow training by surface EMG to 6 patients with dysphagia following brainstem strokes, resulting in 5 of the 6 patients regaining total deglutition function between 3 weeks and 7 months of therapy [12]. In another study, Huckabee and Cannito treated 10 patients through surface EMG and stethoscopes. Of the 10 patients, 8 were able to remove their nasogastric (NG) tube and regain deglutition function [8]. In previous studies, the lack of a control group, coupled with inconsistent independent variables such as frequency, intensity, and duration of treatment, affected the interpretation of the results. Recently, the use of virtual reality or game-based biofeedback therapy has expanded to the treatment of motor disorders and other disorders in the cognitive and perceptual realms [15,16]. Virtual reality, when applied during stroke rehabilitation, allows the potential for patients to improve motor function and activities of daily living function [16,17]. Although there is promising evidence regarding the effectiveness of virtual reality biofeedback therapy, there have not been substantial applications of virtual reality or game-based biofeedback to the treatment of patients with dysphagia. For the purpose of this study, biofeedback signals from laryngeal movement were detected by accelerometers and converted into an animation of a frog swallowing a mosquito. Repeated training with this “visualization” of the laryngeal movement may allow a greater possibility of improvement in deglutition functionality. The goal of this study was to determine the effect of incorporating game-based biofeedback into swallowing therapy on patients with poststroke dysphagia. Methods Subjects We enrolled 20 patients in the study. Patients included had a history of hemorrhagic or ischemic stroke, were able to follow multiple-step orders, and had dysphagia classified as level 3 or lower on the Functional Oral Intake Scale (FOIS). Patients with nonstroke neurological disorders (eg, traumatic brain injury, brain tumor, neurodegenerative disorders, Parkinsonism), neck injuries, and surgery-induced
dysphagia were excluded from the enrollment process. Informed consent was obtained from all participants, and the study protocol was approved by the institutional review board of a university teaching hospital. The subjects had all had poststroke dysphagia for 2-72 months and had received traditional speech therapy (except laryngeal elevation exercise) for 1 month before this study. They were individually matched to either the experimental group (treated by traditional swallowing training and game-based biofeedback laryngeal elevation exercises) or to the control group (treated by traditional swallowing training and laryngeal elevation exercises). Four of 10 subjects had chronic dysphagia (>1 year poststroke) in both the experimental and control groups. Each participant underwent 1-hour sessions 3 times per week for a total of 16 treatment sessions. Each session included a 30-minute subsection of traditional swallow treatment and a 30-minute subsection of laryngeal elevation exercises with or without game-based biofeedback. Submental ultrasonography was performed and FOIS scores were evaluated for each participant before and after the 16 treatment sessions to assess the swallowing function.
Effortful Swallow and Mendelsohn Maneuver In this study, effortful swallowing combined with the Mendelsohn maneuver was used for laryngeal elevation exercises. For effortful swallow training, patients were asked to follow the instructions, “When you swallow, squeeze as hard as you can with all your throat muscles.” Then patients were asked to continue following the next instructions for Mendelsohn maneuver: “Keep squeezing your throat muscles, and hold your larynx at the highest point. Don’t let it drop, and hold it up for about 1 second” [6].
Submental Ultrasonography Ultrasonography may provide a way to evaluate the effects of direct swallowing therapies. To measure the changes of hyoid bone displacement in dysphasic stroke patients, we implemented the method of submental ultrasonography as developed by Hsiao et al [18]. This study used an ultrasound machine with a curvilinear transducer (BS3C673 Convex Array, 3.5 MHz, BSUS20-32C; Broadsound Corporation, Hsinchu City, Taiwan, Republic of China). Images were recorded at a frequency of 22.5 frames per second. The subjects sat in an upright position with their head fixed and swallowed 3 mL of thickened water. The transducer was placed on the intersection of the midsagittal plane and the submental region to determine hyoid bone displacement (Figure 1a-c).
C.-M. Li et al. / PM R XXX (2016) 1-7
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FOIS score indicated a worse swallowing ability. Patients with a score in the range of 1-3 on the FOIS are dependent on tube feeding, whereas those with a score in the range of 4-6 have oral intake capabilities. Table 1 depicts the definitions of FOIS levels [19]. Game-Based Swallowing Biofeedback System A miniature 3-axis accelerometer was placed on the neck of the subjects just above the thyroid cartilage to measure the acceleration of the larynx when lifted during deglutition. The data output gave visual feedback to the subjects (Figure 2a). The acceleration of the laryngeal elevation was further processed and displayed on the screen to provide real-time biofeedback data (Figure 2b). A 3D animation of a frog catching a mosquito was designed to provide virtual realityebased feedback. Through virtualization, the subjects were tutored to imagine themselves as the frog hunting for a mosquito. A virtual mosquito flew in from the right side of the screen for 15 seconds. During the flight of the mosquito, the subjects had to swallow with effort to hunt the mosquito and hold the swallow for about 1 second. If the acceleration of the laryngeal elevation was higher than the preset acceleration threshold, the frog on the screen would successfully catch the mosquito (Figure 2c). The acceleration threshold was adjustable based on the swallowing ability of the patients to inspire their confidence Statistical Analyses
Figure 1. Placement of ultrasound transducer for biofeedback swallowing training. (a) The transducer was placed on the intersection of the midsagittal plane and the submental region to determine hyoid bone displacement. (b) Open arrow indicates the mandible at coordinate (0,0) at rest. Filled arrow indicates hyoid bone coordinate (X1,Y1) at rest. (c) Open arrow indicates the mandible at coordinate (0,0) at rest. Small filled arrow indicates hyoid bone coordinate (X1,Y1) at rest. Large filled arrow indicates hyoid bone coordinate (X2,Y2) at highest level during deglutition.
Functional Oral Intake Scale The FOIS was designed to measure the swallowing function of stroke patients [19]. A higher FOIS level indicates a better swallowing ability, whereas a lower
Group demographics were viewed using descriptive methods. The Fisher exact test and Mann-Whitney U test were used for comparison of nominal and continuous variables between groups. The Wilcoxon signed-rank test and Mann-Whitney U test were used for the intragroup and intergroup analysis, respectively, of the hyoid bone displacement and FOIS scores. A matched-pair analysis (Mantel-Haenszeleadjusted odds ratio) was conducted on tube removal. SPSS 20.0 software (SPSS Inc., Chicago, IL) was used to carry out data analysis. The level of significance was set at P < .05 for all comparisons. Sample size was calculated by G*Power 3.1.9.2, and the power was 0.98. Table 1 Functional Oral Intake Scale (FOIS) Level Level Level Level Level
1: 2: 3: 4: 5:
Nothing by Mouth Tube dependent with minimal attempts of food or liquid Tube dependent with consistent oral intake of food or liquid Total oral diet of a single consistency Total oral diet with multiple consistencies, but requiring special preparation or compensations Level 6: Total oral diet with multiple consistencies without special preparation, but with specific food limitations Level 7: Total oral diet with no restrictions
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Game-Based Swallowing Training
but in the control group it was not. Before treatment, the intergroup comparisons of hyoid bone displacement proved to be statistically non significant (P ¼ .141); however, the difference in hyoid bone displacement (before and after treatment) in the experimental group was larger than that in the control group with statistical significance (P ¼ .007). Table 4 shows the change in FOIS scores before and after treatment. In the experimental group, the difference between the before and after treatment FOIS scores mean was statistically significant (P ¼ .004), whereas in the control group it was not. Before treatment, intergroup comparisons in FOIS scores were statistically nonsignificant; however, changes in the FOIS scores before and after treatment in the experimental group proved to be larger than those of the control group and showed statistical significance (P ¼ .004). The intergroup comparison showed that the difference in FOIS scores before and after treatment in the experimental group was larger than that in the control group and had statistical significance (P ¼ .014). Before therapy, the NG tube insertion rate was 100% in both the control group and experimental group. After therapy, the experimental group had better improvement. In the experimental group, 8 of 10 patients (80%), including 2 of the 4 patients with chronic dysphagia, discontinued tube insertion, whereas in the control group, 2 of 10 patients (20%; without any patients with chronic dysphagia) removed their tubes after therapy. Table 5 shows that participation in the experimental group was associated with an increased probability of NG tube removal (odds ratio ¼ 6.00; 95% confidence interval ¼ 1.08-33.27, P ¼ .009). Discussion
Figure 2. (a) Sagittal view of the cervical region showing the orientation and polarity of the 3 axes of the accelerometer. (b) The acceleration of the laryngeal lifting was further processed and displayed on the screen to provide real-time biofeedback dataegraphical user interface. (c) Game-based biofeedback display.
Results There were no differences in subject factors of both groups such as gender, age, duration of illness, lesion location, and dysphagia grades (FOIS scores) as shown in Table 2. Table 3 shows the change in hyoid bone displacement. In the experimental group, the difference between mean hyoid bone displacement before and after treatment was statistically significant (P ¼ .002),
Our results demonstrate that game-based biofeedback is a viable option for improving patients’ laryngeal elevation. Traditional laryngeal elevation techniques were unable to match the improvement seen in patients’ laryngeal elevation through game-based biofeedback techniques after 16 treatment sessions. According to previous studies [20], the effortful swallow keeps the hyoid bone moving forward and helps it to move higher, thus reducing the risk of choking. The Mendelsohn maneuver increases the hyoid movement and widens the upper esophageal sphincter opening, facilitating bolus passage through the larynx [21-23]. Both maneuvers prolong the upper esophageal sphincter opening time [20,22]. Although the mean hyoid bone displacement increased in both groups after all treatment sessions, only the experimental group experienced statistically significant differences. It was difficult for the subjects to exert the exact and proper force to perform “effortful swallowing” or to keep their larynx elevated for a couple of seconds. In addition, the treatment
C.-M. Li et al. / PM R XXX (2016) 1-7
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Table 2 Characteristics of the study patients Characteristic Gender Male/female Age, y* Poststroke duration* Lesion location Brainstem (n) Cortex/subcortex (n) FOIS scores Median (range) Mean NG intubation (n)
Experimental Group (n ¼ 10)
Control Group (n ¼ 10)
P
Significance
5/5 65.10 (34-87) SD ¼ 19.44 17.80 (2-72) SD ¼ 24.61
6/4 69.70 (51-82) SD ¼ 9.35 13.30 (2-53) SD ¼ 15.87
1.000† .732‡ .847‡ .629‡
NS NS NS NS
8 2
6 4
2.0 (1-3) 1.90 SD ¼ 0.88 10
1 (1-3) 1.50 SD ¼ 0.71 10
.303‡
NS Matched
NS ¼ not significant; SD ¼ standard deviation; FOIS ¼ Functional Oral Intake Scale; NG ¼ nasogastric. * Mean (range). † Fisher exact test. ‡ Mann-Whitney U test.
providers may not have always been able to provide visual cues to serve as feedback information [24]. A study by Wolf et al [25] showed that verbal feedback by the treatment providers tended to lag a few seconds behind the action performed, and was therefore not reliable for real-time feedback. In contrast, biofeedback methods were able to instantaneously convert the physiologic information of a certain muscle into a visual or auditory signal. With the aid of biofeedback technology, patients were able to manipulate the signal by controlling a specific muscle and receiving real-time feedback [8,26]. In this study, an accelerometer was attached above the thyroid cartilage to provide biofeedback information to the subjects, allowing them to view the acceleration of their laryngeal lift. A study by Reddy et al [14] found that the magnitude of laryngeal lift could be increased through biofeedback training performed with an accelerometer. Task-oriented repetition, training frequency, and patient motivation play important roles in stroke rehabilitation. Interesting, challenging, rewarding, and even competitive ways of training might increase patients’ motivation for rehabilitation. Therapy marketed as
Table 3 Hyoid bone displacement change (before and after therapy)
Group
Before Therapy Mean (SD)
After Therapy Mean (SD)
Change Mean (SD)
Intragroup Analyses P Value
Experimental 11.37 (2.31) 14.45 (2.60) 3.08 (2.72) .002* group (n ¼ 10) Control group 12.84 (2.42) 13.35 (2.51) 0.51 (0.78) .106 (n ¼ 10) Intergroup .141 .678 .007* analyses P value Intra- and intergroup analysis was performed by Wilcoxon signed-rank test and Mann-Whitney U test. SD ¼ standard deviation. * P < .01.
playing games instead of performing monotonous exercises may help the patient to succeed in what was originally thought to be impossible [27]. Studies by Manor et al and Macrae et al showed that visual and auditory biofeedback improved swallowing training [28,29]. Burdea suggested that game-based biofeedback treatment through visual and auditory positive feedback would inspire patients [30]. Through real-time verbal positive feedback cues, such as “Good!”, “Very good!”, and “Excellent!”, patients are motivated to try harder and to perform better. Competition and high levels of interaction were emphasized in this study. In the experimental group, hyoid bone displacement increased, possibly due to the patients’ increased awareness and motivation, allowing the patient to modify psycho-physiological responses and to achieve better physiologic functions, both consciously and subconsciously. The amplified positive effect of game-based swallowing biofeedback for the experimental group may have resulted from the adjustable acceleration threshold. Each time that a patient was able to execute laryngeal lifting, we would raise the threshold so that the patient had to exert more force to allow the virtual frog to catch the mosquito. Through this method, the hyoid bone displacement might have increased after repetitions of the biofeedback therapy. Instead of focusing on the physiological change while applying the Mendelsohn maneuver, McCullough and Kim used the Mendelsohn maneuver, assisted by surface EMG biofeedback, for laryngeal elevation training by creating a training program with predefined frequencies, intensities, and durations. In their study, the threshold was also adjustable to suit the patients’ conditions. Studies by McCullough and Kim also showed great improvement in hyoid displacement as a result of biofeedback therapy, similar to our study [22]. In our study, FOIS score improvements and NG tube removal rates were higher in the experimental group
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Table 4 FOIS score change, before and after therapy
Experimental group (n ¼ 10) Control group (n ¼ 10) Intergroup analyses P value
Before Therapy Mean (SD) Median (Range)
After Therapy Mean (SD) Median (Range)
1.90 (0.88) 2 (1-3) 1.50 (0.71) 1 (1-3) .284
5.10 (1.20) 5.5 (3-6) 2.50 (1.78) 2 (1-6) .004†
Change Mean (SD)
Intragroup Analyses P Value
3.20 (1.81)
.004*
1.00 (1.33)
.078
.014*
Intra- and intergroup analysis was performed by Wilcoxon signed-rank test and Mann-Whitney U test. FOIS ¼ Functional Oral Intake Scale; SD ¼ standard deviation. * P < .05. † P < .01.
than in the control group. Crary used a surface EMG biofeedback for swallow training on 25 poststroke patients. Each participant underwent 50-minute training sessions 5 times per week. The median FOIS score increased from 1 to 5.5, with an average increase of 2.96 [13]. Bogaardt et al implemented a modified Mendelsohn maneuver using auxiliary surface EMG biofeedback to treat 11 patients with chronic dysphagia following a stroke. After 7 sessions of therapy, each lasting for 20 minutes, FOIS scores improved from 2.6 to 5.6, with an average increase of 3. Six of the 8 patients were weaned off NG tube feeding and regained total deglutition function, with a NG tube removal rate of 75% [10]. Crary instructed 6 patients with brainstem strokeinduced dysphagia to complete the Mendelsohn maneuver and effortful swallowing with auxiliary surface EMG biofeedback therapy [12]. After daily training for 3 weeks, 5 of 6 patients regained total deglutition function, with a NG tube removal rate of 83%. Huckabee and Cannito used effortful swallowing, the Mendelsohn maneuver, vocal adduction exercises, and head-lifting maneuvers with auxiliary surface EMG and stethoscope biofeedback to treat 10 patients with chronic dysphagia following a brainstem stroke. After a training regimen of 10 hours of therapy offered in 1 week, 8 of the 10 patients were weaned off NG tube feeding and regained total deglutition function, with a NG tube removal rate of 80% [8]. The NG tube removal rate reported in this study closely matched the 80% rate of Huckabee and Cannito; Table 5 Nasogastric (NG) tube insertion NG Tube Insertion (n)
Before/After Therapy
NG Tube Removal Rate (%)
Adjusted OR (95% CI)
P Value
Experimental group (n ¼ 10) Control group (n ¼ 10)
10/2
80
6.00 (1.08-33.27)
.009*
10/8
20
Adjusted odds ratio: Mantel-Haenszel test. CI ¼ confidence interval. * P < .05.
however, the lack of a control group in their experiment creates difficulty in proving the effect of auxiliary biofeedback. In contrast, our study contained a control group, which confirmed improved swallowing function. Study Limitations The main limitations of our study are the small sample size and the lack of subjective real-time evaluation of deglutition characteristics, as in using a videofluoroscopic swallow study to measure laryngeal elevation. This study was based on applying game-based biofeedback to poststroke dysphagia patients. We plan to enroll more subjects for future studies and treatment sessions, and will follow up the subjects in this study to determine the sustainability of the experimental effects. Game-based biofeedback can also be applied to various other patient groups, such as patients with nasopharyngeal carcinoma, Parkinson disease, brain cancer, or other patients with lesions around the laryngeal region. Since the virtual reality used in this study was immersive and engaging, game-based biofeedback is also suited for children with dysphagia. Conclusion In this study, laryngeal elevation training combined with game-based biofeedback helped patients with poststroke dysphagia to practice laryngeal elevation exercises by receiving interactive biofeedback data. This can augment hyoid bone displacement, and hence improves FOIS scores and NG tube removal rates. Acknowledgments The authors are very grateful to the participants and staff who participated in this project. References 1. Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: Prognosis and prognostic factors at 6 months. Stroke 1999;30:744748.
C.-M. Li et al. / PM R XXX (2016) 1-7 2. Smithard DG, O’Neill PA, Park C, et al. Can bedside assessment reliably exclude aspiration following acute stroke? Age Ageing 1998;27:99-106. 3. Teasell RW, Bach D, McRae M. Prevalence and recovery of aspiration post stroke: A retrospective analysis. Dysphagia 1994; 9:35-39. 4. Veis SL, Logemann JA. Swallowing disorders in persons with cerebrovascular accident. Arch Phys Med Rehabil 1985;66:372-375. 5. Burkhead LM, Sapienza CM, Rosenbek JC. Strength-training exercise in dysphagia rehabilitation: Principles, procedures, and directions for future research. Dysphagia 2007;22:251-265. 6. Logemann JA. Management of the patient with oropharyngeal swallowing disorders. In: Logemann JA, ed. Evaluation and treatment of swallowing disorders. 2nd ed. Austin, TX: pro-ed; 1998, 191-250. 7. Ding R, Larson RC, Logemann JA, Rademaker AW. Surface electromyographic and electroglottographic studies in normal subjects under two swallow conditions: Normal and during the Mendelsohn manuever. Dysphagia 2002;17:1-12. 8. Huckabee ML, Cannito MP. Outcomes of swallowing rehabilitation in chronic brainstem dysphagia: A retrospective evaluation. Dysphagia 1999;14:93-109. 9. McKee MG. Biofeedback: An overview in the context of heartebrain medicine. Cleve Clin J Med 2008;75:S31-S34. 10. Bogaardt HCA, Grolman W, Fokkens WJ. The use of biofeedback in the treatment of chronic dysphagia in stroke patients. Folia Phoniatr Logop 2009;61:200-205. 11. Bryant M. Biofeedback in the treatment of a selected dysphagic patient. Dysphagia 1991;6:140-144. 12. Crary MA. A direct intervention program for chronic neurogenic dysphagia secondary to brainstem stroke. Dysphagia 1995;10:6-18. 13. Crary MA, Carnaby GD, Groher ME, Helseth E. Functional benefits of dysphagia therapy using adjunctive sEMG biofeedback. Dysphagia 2004;19:160-164. 14. Reddy NP, Simcox DL, Gupta V, et al. Biofeedback therapy using accelerometry for treating dysphagic patients with poor laryngeal elevation: Case studies. J Rehabil Res Dev 2000;37:361-372. 15. Romano D. Virtual reality therapy. Dev Med Child Neurol 2005;47: 580. 16. Saposnik G, Teasell R, Mamdani M, et al. Effectiveness of virtual reality using Wii gaming technology in stroke rehabilitation. Stroke 2010;41:1477-1484.
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17. Laver K, George S, Thomas S, Deutsch JE, Crotty M. Virtual reality for stroke rehabilitation: An abridged version of a Cochrane review. Eur J Phys Rehabil Med 2015;51:497-506. 18. Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of ultrasonography in assessing oropharyngeal dysphagia in stroke patients. Ultrasound Med Biol 2012;38:1522-1528. 19. Crary MA, Carnaby GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;86:1516-1520. 20. Hind JA, Nicosia MA, Roecker EB, Carnes ML, Robbins J. Comparison of effortful and noneffortful swallows in healthy middle aged and older adults. Arch Phys Med Rehabil 2001;82:1661-1665. ˚ , Hedstro 21. Bode ´n K, Hallgren A ¨m H. Effects of three different swallow maneuvers analyzed by videomanometry. Acta Radiol 2006;47:628-633. 22. McCullough GH, Kim Y. Effects of the Mendelsohn maneuver on extent of hyoid movement and UES opening post-stroke. Dysphagia 2013;28:511-519. 23. Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Physiol 1991;260:450-456. 24. Daniels SK, Huckabee ML. Rehabilitation of oropharyngeal dysphagia. In: Daniels SK, Huckabee ML, eds. Dysphagia following stroke. San Diego, CA: Plural; 2014, 301-342. 25. Wolf SL. Biofeedback. In: Downey JA, Myers SJ, Gonzalez EG, Liberman JS, eds. The physiological basis of rehabilitation medicine. 2nd ed. Stoneham, MA: Butterworth-Heinemann; 1994, 563-572. 26. McKee MG. Contributions of psychophysiologic monitoring to diagnosis and treatment of chronic head pain: A case study. Headache Q 1991;11:327-330. 27. Bach-y-Rita P, Wood S, Leder R, et al. Computer-assisted motivating rehabilitation (CAMR) for institutional, home, and educational late stroke programs. Top Stroke Rehabil 2002;8:1-10. 28. Manor Y, Mootanah R, Freud D, Nir G, Cohen JT. Video-assisted swallowing therapy for patients with Parkinson’s disease. Parkinsonism Relat Disord 2013;19:207-211. 29. Macrae P, Anderson C, Taylor-Kamara1 I, Humbert I. The effects of feedback on volitional manipulation of airway protection during swallowing. J Mot Behav 2014;46:133-139. 30. Burdea GC. Virtual rehabilitationdbenefits and challenges. Methods Inf Med 2003;42:519-523.
Disclosure C.-M.L. Department of Biomedical Engineering, National Cheng Kung University, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
S.-H.H. Department of Biomedical Engineering, National Cheng Kung University, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
T.-G.W. Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei City, Taiwan, Republic of China Disclosure: nothing to disclose
M.C. Department of Electrical and Computer Engineering, University of Texas at Austin, Austin, TX, USA Disclosure: nothing to disclose
H.-Y.L. Department of Digital Media Design and Management, Far East University, Xinshi District, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
J.-J.J.C. Department of Biomedical Engineering, National Cheng Kung University, No.1, University Road, Tainan City 70101, Taiwan, Republic of China. Address correspondence to: J.-J.J.C.; e-mail: [email protected] Disclosure: nothing to disclose
H.-P.W. Department of Speech and Hearing Disorder and Sciences, National Taipei University of Nursing and Health Sciences, Taipei City, Taiwan, Republic of China Disclosure: nothing to disclose
Supported by grant no. 10146 from Central & Southern Medical Alliance, Taiwan Ministry of Health and Welfare. Submitted for publication August 23, 2015; accepted January 6, 2016.
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Original Research
Swallowing Training Combined With Game-Based Biofeedback in Poststroke Dysphagia Chih-Ming Li, MD, PhD, Tyng-Guey Wang, MD, Hsiao-Yu Lee, MS, Hsueh-Pei Wang, MS, Shang-Heng Hsieh, MS, Michelle Chou, BS, Jia-Jin Jason Chen, PhD
Abstract Background: For patients with dysphagia due to stroke, in addition to compensatory strategies, exercises are used to help improve motor function. Biofeedback is used in neuromuscular training and is promising for swallowing training. Objective: To evaluate the functional value of game-based biofeedback in swallowing therapy for patients with poststroke dysphagia. Design: A case-control study. Setting: Academic tertiary hospital. Participants: Subjects with poststroke dysphagia (n ¼ 20) were individually matched to 2 separate groups, a game-based biofeedback group (n ¼ 10) or a control group (n ¼ 10), for age, gender, duration of dysphagia, and dysphagia grades. Interventions: Each participant underwent 1-hour sessions 3 times per week for a total of 16 treatment sessions. Each session included a 30-minute session of traditional swallow treatment and a 30-minute session of laryngeal elevation exercises. In the experimental group, laryngeal elevation exercises were combined with additional game-based biofeedback. Main Outcome Measures: Outcomes assessed before and after interventions included hyoid bone displacement, Functional Oral Intake Scale (FOIS) scores, and nasogastric (NG) tube removal rate. Results: Intergroup analyses showed larger differences in hyoid bone displacement and FOIS scores (before and after treatment) in the experimental group than in the control group, with statistical significance (P ¼ .007 and P ¼ .014, respectively). Intergroup analyses showed that the hyoid bone displacement change and FOIS scores before and after treatment exhibited statistically significant improvement only in the experimental group (P ¼ .002 and P ¼ .004, respectively). In all, 8 of 10 patients (80%) in the experimental group and 2 of 10 patients (20%) in the control group discontinued NG tube insertion after therapy. Participation in the experimental group was associated with an increased probability of tube removal (odds ratio ¼ 6.00; 95% confidence interval ¼ 1.08-33.27, P ¼ .009). Conclusions: Laryngeal elevation training combined with game-based biofeedback augments the change in hyoid bone displacement and FOIS scores, and increases the NG tube removal rate in patients with poststroke dysphagia.
Introduction Dysphagia, which can result from a wide variety of disorders, is seen in 16%-64% of individuals who have sustained a stroke [1-4]. Exercise, in addition to compensatory strategies, can often improve motor function in patients who have acquired dysphagia following a stroke [5,6]. The effortful swallow and the Mendelsohn maneuver are 2 common compensatory strategies for oropharyngeal dysphagia. The effortful swallow increases the oropharyngeal swallow pressure
and augments posterior motion of the tongue base [6]. The Mendelsohn maneuver prolongs and widens the cricopharyngeal opening by extending and sustaining laryngeal elevation during swallowing [6]. However, indiscernible motion or impaired sensation in the oropharynx often hinders patients’ self-awareness during therapeutic procedures. To help patients sense their deglutition, speech therapists have looked for easier methods of providing oral feedback or gestural cues [7,8]. Biofeedback uses specialized equipment to convert subconscious
1934-1482/$ - see front matter ª 2016 by the American Academy of Physical Medicine and Rehabilitation http://dx.doi.org/10.1016/j.pmrj.2016.01.003
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Game-Based Swallowing Training
physiologic information into visual or auditory signals, helping patients to sense and manipulate physiological changes to improve their performance [9]. Although biofeedback is commonly used in neuromuscular training, it has not been widely applied to dysphagia treatment. Only a small number of investigations on biofeedback-assisted swallowing training have been conducted, with a focus mainly on laryngeal elevation by electromyography (EMG) or use of accelerometers [8,10-14]. In 1 such experiment, Crary applied biofeedback techniques on swallow training by surface EMG to 6 patients with dysphagia following brainstem strokes, resulting in 5 of the 6 patients regaining total deglutition function between 3 weeks and 7 months of therapy [12]. In another study, Huckabee and Cannito treated 10 patients through surface EMG and stethoscopes. Of the 10 patients, 8 were able to remove their nasogastric (NG) tube and regain deglutition function [8]. In previous studies, the lack of a control group, coupled with inconsistent independent variables such as frequency, intensity, and duration of treatment, affected the interpretation of the results. Recently, the use of virtual reality or game-based biofeedback therapy has expanded to the treatment of motor disorders and other disorders in the cognitive and perceptual realms [15,16]. Virtual reality, when applied during stroke rehabilitation, allows the potential for patients to improve motor function and activities of daily living function [16,17]. Although there is promising evidence regarding the effectiveness of virtual reality biofeedback therapy, there have not been substantial applications of virtual reality or game-based biofeedback to the treatment of patients with dysphagia. For the purpose of this study, biofeedback signals from laryngeal movement were detected by accelerometers and converted into an animation of a frog swallowing a mosquito. Repeated training with this “visualization” of the laryngeal movement may allow a greater possibility of improvement in deglutition functionality. The goal of this study was to determine the effect of incorporating game-based biofeedback into swallowing therapy on patients with poststroke dysphagia. Methods Subjects We enrolled 20 patients in the study. Patients included had a history of hemorrhagic or ischemic stroke, were able to follow multiple-step orders, and had dysphagia classified as level 3 or lower on the Functional Oral Intake Scale (FOIS). Patients with nonstroke neurological disorders (eg, traumatic brain injury, brain tumor, neurodegenerative disorders, Parkinsonism), neck injuries, and surgery-induced
dysphagia were excluded from the enrollment process. Informed consent was obtained from all participants, and the study protocol was approved by the institutional review board of a university teaching hospital. The subjects had all had poststroke dysphagia for 2-72 months and had received traditional speech therapy (except laryngeal elevation exercise) for 1 month before this study. They were individually matched to either the experimental group (treated by traditional swallowing training and game-based biofeedback laryngeal elevation exercises) or to the control group (treated by traditional swallowing training and laryngeal elevation exercises). Four of 10 subjects had chronic dysphagia (>1 year poststroke) in both the experimental and control groups. Each participant underwent 1-hour sessions 3 times per week for a total of 16 treatment sessions. Each session included a 30-minute subsection of traditional swallow treatment and a 30-minute subsection of laryngeal elevation exercises with or without game-based biofeedback. Submental ultrasonography was performed and FOIS scores were evaluated for each participant before and after the 16 treatment sessions to assess the swallowing function.
Effortful Swallow and Mendelsohn Maneuver In this study, effortful swallowing combined with the Mendelsohn maneuver was used for laryngeal elevation exercises. For effortful swallow training, patients were asked to follow the instructions, “When you swallow, squeeze as hard as you can with all your throat muscles.” Then patients were asked to continue following the next instructions for Mendelsohn maneuver: “Keep squeezing your throat muscles, and hold your larynx at the highest point. Don’t let it drop, and hold it up for about 1 second” [6].
Submental Ultrasonography Ultrasonography may provide a way to evaluate the effects of direct swallowing therapies. To measure the changes of hyoid bone displacement in dysphasic stroke patients, we implemented the method of submental ultrasonography as developed by Hsiao et al [18]. This study used an ultrasound machine with a curvilinear transducer (BS3C673 Convex Array, 3.5 MHz, BSUS20-32C; Broadsound Corporation, Hsinchu City, Taiwan, Republic of China). Images were recorded at a frequency of 22.5 frames per second. The subjects sat in an upright position with their head fixed and swallowed 3 mL of thickened water. The transducer was placed on the intersection of the midsagittal plane and the submental region to determine hyoid bone displacement (Figure 1a-c).
C.-M. Li et al. / PM R XXX (2016) 1-7
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FOIS score indicated a worse swallowing ability. Patients with a score in the range of 1-3 on the FOIS are dependent on tube feeding, whereas those with a score in the range of 4-6 have oral intake capabilities. Table 1 depicts the definitions of FOIS levels [19]. Game-Based Swallowing Biofeedback System A miniature 3-axis accelerometer was placed on the neck of the subjects just above the thyroid cartilage to measure the acceleration of the larynx when lifted during deglutition. The data output gave visual feedback to the subjects (Figure 2a). The acceleration of the laryngeal elevation was further processed and displayed on the screen to provide real-time biofeedback data (Figure 2b). A 3D animation of a frog catching a mosquito was designed to provide virtual realityebased feedback. Through virtualization, the subjects were tutored to imagine themselves as the frog hunting for a mosquito. A virtual mosquito flew in from the right side of the screen for 15 seconds. During the flight of the mosquito, the subjects had to swallow with effort to hunt the mosquito and hold the swallow for about 1 second. If the acceleration of the laryngeal elevation was higher than the preset acceleration threshold, the frog on the screen would successfully catch the mosquito (Figure 2c). The acceleration threshold was adjustable based on the swallowing ability of the patients to inspire their confidence Statistical Analyses
Figure 1. Placement of ultrasound transducer for biofeedback swallowing training. (a) The transducer was placed on the intersection of the midsagittal plane and the submental region to determine hyoid bone displacement. (b) Open arrow indicates the mandible at coordinate (0,0) at rest. Filled arrow indicates hyoid bone coordinate (X1,Y1) at rest. (c) Open arrow indicates the mandible at coordinate (0,0) at rest. Small filled arrow indicates hyoid bone coordinate (X1,Y1) at rest. Large filled arrow indicates hyoid bone coordinate (X2,Y2) at highest level during deglutition.
Functional Oral Intake Scale The FOIS was designed to measure the swallowing function of stroke patients [19]. A higher FOIS level indicates a better swallowing ability, whereas a lower
Group demographics were viewed using descriptive methods. The Fisher exact test and Mann-Whitney U test were used for comparison of nominal and continuous variables between groups. The Wilcoxon signed-rank test and Mann-Whitney U test were used for the intragroup and intergroup analysis, respectively, of the hyoid bone displacement and FOIS scores. A matched-pair analysis (Mantel-Haenszeleadjusted odds ratio) was conducted on tube removal. SPSS 20.0 software (SPSS Inc., Chicago, IL) was used to carry out data analysis. The level of significance was set at P < .05 for all comparisons. Sample size was calculated by G*Power 3.1.9.2, and the power was 0.98. Table 1 Functional Oral Intake Scale (FOIS) Level Level Level Level Level
1: 2: 3: 4: 5:
Nothing by Mouth Tube dependent with minimal attempts of food or liquid Tube dependent with consistent oral intake of food or liquid Total oral diet of a single consistency Total oral diet with multiple consistencies, but requiring special preparation or compensations Level 6: Total oral diet with multiple consistencies without special preparation, but with specific food limitations Level 7: Total oral diet with no restrictions
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Game-Based Swallowing Training
but in the control group it was not. Before treatment, the intergroup comparisons of hyoid bone displacement proved to be statistically non significant (P ¼ .141); however, the difference in hyoid bone displacement (before and after treatment) in the experimental group was larger than that in the control group with statistical significance (P ¼ .007). Table 4 shows the change in FOIS scores before and after treatment. In the experimental group, the difference between the before and after treatment FOIS scores mean was statistically significant (P ¼ .004), whereas in the control group it was not. Before treatment, intergroup comparisons in FOIS scores were statistically nonsignificant; however, changes in the FOIS scores before and after treatment in the experimental group proved to be larger than those of the control group and showed statistical significance (P ¼ .004). The intergroup comparison showed that the difference in FOIS scores before and after treatment in the experimental group was larger than that in the control group and had statistical significance (P ¼ .014). Before therapy, the NG tube insertion rate was 100% in both the control group and experimental group. After therapy, the experimental group had better improvement. In the experimental group, 8 of 10 patients (80%), including 2 of the 4 patients with chronic dysphagia, discontinued tube insertion, whereas in the control group, 2 of 10 patients (20%; without any patients with chronic dysphagia) removed their tubes after therapy. Table 5 shows that participation in the experimental group was associated with an increased probability of NG tube removal (odds ratio ¼ 6.00; 95% confidence interval ¼ 1.08-33.27, P ¼ .009). Discussion
Figure 2. (a) Sagittal view of the cervical region showing the orientation and polarity of the 3 axes of the accelerometer. (b) The acceleration of the laryngeal lifting was further processed and displayed on the screen to provide real-time biofeedback dataegraphical user interface. (c) Game-based biofeedback display.
Results There were no differences in subject factors of both groups such as gender, age, duration of illness, lesion location, and dysphagia grades (FOIS scores) as shown in Table 2. Table 3 shows the change in hyoid bone displacement. In the experimental group, the difference between mean hyoid bone displacement before and after treatment was statistically significant (P ¼ .002),
Our results demonstrate that game-based biofeedback is a viable option for improving patients’ laryngeal elevation. Traditional laryngeal elevation techniques were unable to match the improvement seen in patients’ laryngeal elevation through game-based biofeedback techniques after 16 treatment sessions. According to previous studies [20], the effortful swallow keeps the hyoid bone moving forward and helps it to move higher, thus reducing the risk of choking. The Mendelsohn maneuver increases the hyoid movement and widens the upper esophageal sphincter opening, facilitating bolus passage through the larynx [21-23]. Both maneuvers prolong the upper esophageal sphincter opening time [20,22]. Although the mean hyoid bone displacement increased in both groups after all treatment sessions, only the experimental group experienced statistically significant differences. It was difficult for the subjects to exert the exact and proper force to perform “effortful swallowing” or to keep their larynx elevated for a couple of seconds. In addition, the treatment
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Table 2 Characteristics of the study patients Characteristic Gender Male/female Age, y* Poststroke duration* Lesion location Brainstem (n) Cortex/subcortex (n) FOIS scores Median (range) Mean NG intubation (n)
Experimental Group (n ¼ 10)
Control Group (n ¼ 10)
P
Significance
5/5 65.10 (34-87) SD ¼ 19.44 17.80 (2-72) SD ¼ 24.61
6/4 69.70 (51-82) SD ¼ 9.35 13.30 (2-53) SD ¼ 15.87
1.000† .732‡ .847‡ .629‡
NS NS NS NS
8 2
6 4
2.0 (1-3) 1.90 SD ¼ 0.88 10
1 (1-3) 1.50 SD ¼ 0.71 10
.303‡
NS Matched
NS ¼ not significant; SD ¼ standard deviation; FOIS ¼ Functional Oral Intake Scale; NG ¼ nasogastric. * Mean (range). † Fisher exact test. ‡ Mann-Whitney U test.
providers may not have always been able to provide visual cues to serve as feedback information [24]. A study by Wolf et al [25] showed that verbal feedback by the treatment providers tended to lag a few seconds behind the action performed, and was therefore not reliable for real-time feedback. In contrast, biofeedback methods were able to instantaneously convert the physiologic information of a certain muscle into a visual or auditory signal. With the aid of biofeedback technology, patients were able to manipulate the signal by controlling a specific muscle and receiving real-time feedback [8,26]. In this study, an accelerometer was attached above the thyroid cartilage to provide biofeedback information to the subjects, allowing them to view the acceleration of their laryngeal lift. A study by Reddy et al [14] found that the magnitude of laryngeal lift could be increased through biofeedback training performed with an accelerometer. Task-oriented repetition, training frequency, and patient motivation play important roles in stroke rehabilitation. Interesting, challenging, rewarding, and even competitive ways of training might increase patients’ motivation for rehabilitation. Therapy marketed as
Table 3 Hyoid bone displacement change (before and after therapy)
Group
Before Therapy Mean (SD)
After Therapy Mean (SD)
Change Mean (SD)
Intragroup Analyses P Value
Experimental 11.37 (2.31) 14.45 (2.60) 3.08 (2.72) .002* group (n ¼ 10) Control group 12.84 (2.42) 13.35 (2.51) 0.51 (0.78) .106 (n ¼ 10) Intergroup .141 .678 .007* analyses P value Intra- and intergroup analysis was performed by Wilcoxon signed-rank test and Mann-Whitney U test. SD ¼ standard deviation. * P < .01.
playing games instead of performing monotonous exercises may help the patient to succeed in what was originally thought to be impossible [27]. Studies by Manor et al and Macrae et al showed that visual and auditory biofeedback improved swallowing training [28,29]. Burdea suggested that game-based biofeedback treatment through visual and auditory positive feedback would inspire patients [30]. Through real-time verbal positive feedback cues, such as “Good!”, “Very good!”, and “Excellent!”, patients are motivated to try harder and to perform better. Competition and high levels of interaction were emphasized in this study. In the experimental group, hyoid bone displacement increased, possibly due to the patients’ increased awareness and motivation, allowing the patient to modify psycho-physiological responses and to achieve better physiologic functions, both consciously and subconsciously. The amplified positive effect of game-based swallowing biofeedback for the experimental group may have resulted from the adjustable acceleration threshold. Each time that a patient was able to execute laryngeal lifting, we would raise the threshold so that the patient had to exert more force to allow the virtual frog to catch the mosquito. Through this method, the hyoid bone displacement might have increased after repetitions of the biofeedback therapy. Instead of focusing on the physiological change while applying the Mendelsohn maneuver, McCullough and Kim used the Mendelsohn maneuver, assisted by surface EMG biofeedback, for laryngeal elevation training by creating a training program with predefined frequencies, intensities, and durations. In their study, the threshold was also adjustable to suit the patients’ conditions. Studies by McCullough and Kim also showed great improvement in hyoid displacement as a result of biofeedback therapy, similar to our study [22]. In our study, FOIS score improvements and NG tube removal rates were higher in the experimental group
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Game-Based Swallowing Training
Table 4 FOIS score change, before and after therapy
Experimental group (n ¼ 10) Control group (n ¼ 10) Intergroup analyses P value
Before Therapy Mean (SD) Median (Range)
After Therapy Mean (SD) Median (Range)
1.90 (0.88) 2 (1-3) 1.50 (0.71) 1 (1-3) .284
5.10 (1.20) 5.5 (3-6) 2.50 (1.78) 2 (1-6) .004†
Change Mean (SD)
Intragroup Analyses P Value
3.20 (1.81)
.004*
1.00 (1.33)
.078
.014*
Intra- and intergroup analysis was performed by Wilcoxon signed-rank test and Mann-Whitney U test. FOIS ¼ Functional Oral Intake Scale; SD ¼ standard deviation. * P < .05. † P < .01.
than in the control group. Crary used a surface EMG biofeedback for swallow training on 25 poststroke patients. Each participant underwent 50-minute training sessions 5 times per week. The median FOIS score increased from 1 to 5.5, with an average increase of 2.96 [13]. Bogaardt et al implemented a modified Mendelsohn maneuver using auxiliary surface EMG biofeedback to treat 11 patients with chronic dysphagia following a stroke. After 7 sessions of therapy, each lasting for 20 minutes, FOIS scores improved from 2.6 to 5.6, with an average increase of 3. Six of the 8 patients were weaned off NG tube feeding and regained total deglutition function, with a NG tube removal rate of 75% [10]. Crary instructed 6 patients with brainstem strokeinduced dysphagia to complete the Mendelsohn maneuver and effortful swallowing with auxiliary surface EMG biofeedback therapy [12]. After daily training for 3 weeks, 5 of 6 patients regained total deglutition function, with a NG tube removal rate of 83%. Huckabee and Cannito used effortful swallowing, the Mendelsohn maneuver, vocal adduction exercises, and head-lifting maneuvers with auxiliary surface EMG and stethoscope biofeedback to treat 10 patients with chronic dysphagia following a brainstem stroke. After a training regimen of 10 hours of therapy offered in 1 week, 8 of the 10 patients were weaned off NG tube feeding and regained total deglutition function, with a NG tube removal rate of 80% [8]. The NG tube removal rate reported in this study closely matched the 80% rate of Huckabee and Cannito; Table 5 Nasogastric (NG) tube insertion NG Tube Insertion (n)
Before/After Therapy
NG Tube Removal Rate (%)
Adjusted OR (95% CI)
P Value
Experimental group (n ¼ 10) Control group (n ¼ 10)
10/2
80
6.00 (1.08-33.27)
.009*
10/8
20
Adjusted odds ratio: Mantel-Haenszel test. CI ¼ confidence interval. * P < .05.
however, the lack of a control group in their experiment creates difficulty in proving the effect of auxiliary biofeedback. In contrast, our study contained a control group, which confirmed improved swallowing function. Study Limitations The main limitations of our study are the small sample size and the lack of subjective real-time evaluation of deglutition characteristics, as in using a videofluoroscopic swallow study to measure laryngeal elevation. This study was based on applying game-based biofeedback to poststroke dysphagia patients. We plan to enroll more subjects for future studies and treatment sessions, and will follow up the subjects in this study to determine the sustainability of the experimental effects. Game-based biofeedback can also be applied to various other patient groups, such as patients with nasopharyngeal carcinoma, Parkinson disease, brain cancer, or other patients with lesions around the laryngeal region. Since the virtual reality used in this study was immersive and engaging, game-based biofeedback is also suited for children with dysphagia. Conclusion In this study, laryngeal elevation training combined with game-based biofeedback helped patients with poststroke dysphagia to practice laryngeal elevation exercises by receiving interactive biofeedback data. This can augment hyoid bone displacement, and hence improves FOIS scores and NG tube removal rates. Acknowledgments The authors are very grateful to the participants and staff who participated in this project. References 1. Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: Prognosis and prognostic factors at 6 months. Stroke 1999;30:744748.
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17. Laver K, George S, Thomas S, Deutsch JE, Crotty M. Virtual reality for stroke rehabilitation: An abridged version of a Cochrane review. Eur J Phys Rehabil Med 2015;51:497-506. 18. Hsiao MY, Chang YC, Chen WS, Chang HY, Wang TG. Application of ultrasonography in assessing oropharyngeal dysphagia in stroke patients. Ultrasound Med Biol 2012;38:1522-1528. 19. Crary MA, Carnaby GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil 2005;86:1516-1520. 20. Hind JA, Nicosia MA, Roecker EB, Carnes ML, Robbins J. Comparison of effortful and noneffortful swallows in healthy middle aged and older adults. Arch Phys Med Rehabil 2001;82:1661-1665. ˚ , Hedstro 21. Bode ´n K, Hallgren A ¨m H. Effects of three different swallow maneuvers analyzed by videomanometry. Acta Radiol 2006;47:628-633. 22. McCullough GH, Kim Y. Effects of the Mendelsohn maneuver on extent of hyoid movement and UES opening post-stroke. Dysphagia 2013;28:511-519. 23. Kahrilas PJ, Logemann JA, Krugler C, Flanagan E. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Physiol 1991;260:450-456. 24. Daniels SK, Huckabee ML. Rehabilitation of oropharyngeal dysphagia. In: Daniels SK, Huckabee ML, eds. Dysphagia following stroke. San Diego, CA: Plural; 2014, 301-342. 25. Wolf SL. Biofeedback. In: Downey JA, Myers SJ, Gonzalez EG, Liberman JS, eds. The physiological basis of rehabilitation medicine. 2nd ed. Stoneham, MA: Butterworth-Heinemann; 1994, 563-572. 26. McKee MG. Contributions of psychophysiologic monitoring to diagnosis and treatment of chronic head pain: A case study. Headache Q 1991;11:327-330. 27. Bach-y-Rita P, Wood S, Leder R, et al. Computer-assisted motivating rehabilitation (CAMR) for institutional, home, and educational late stroke programs. Top Stroke Rehabil 2002;8:1-10. 28. Manor Y, Mootanah R, Freud D, Nir G, Cohen JT. Video-assisted swallowing therapy for patients with Parkinson’s disease. Parkinsonism Relat Disord 2013;19:207-211. 29. Macrae P, Anderson C, Taylor-Kamara1 I, Humbert I. The effects of feedback on volitional manipulation of airway protection during swallowing. J Mot Behav 2014;46:133-139. 30. Burdea GC. Virtual rehabilitationdbenefits and challenges. Methods Inf Med 2003;42:519-523.
Disclosure C.-M.L. Department of Biomedical Engineering, National Cheng Kung University, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
S.-H.H. Department of Biomedical Engineering, National Cheng Kung University, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
T.-G.W. Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei City, Taiwan, Republic of China Disclosure: nothing to disclose
M.C. Department of Electrical and Computer Engineering, University of Texas at Austin, Austin, TX, USA Disclosure: nothing to disclose
H.-Y.L. Department of Digital Media Design and Management, Far East University, Xinshi District, Tainan City, Taiwan, Republic of China Disclosure: nothing to disclose
J.-J.J.C. Department of Biomedical Engineering, National Cheng Kung University, No.1, University Road, Tainan City 70101, Taiwan, Republic of China. Address correspondence to: J.-J.J.C.; e-mail: [email protected] Disclosure: nothing to disclose
H.-P.W. Department of Speech and Hearing Disorder and Sciences, National Taipei University of Nursing and Health Sciences, Taipei City, Taiwan, Republic of China Disclosure: nothing to disclose
Supported by grant no. 10146 from Central & Southern Medical Alliance, Taiwan Ministry of Health and Welfare. Submitted for publication August 23, 2015; accepted January 6, 2016.