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Detection of Muscle Tension Dysphonia Using Eulerian Video Magnification: A Pilot Study
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Detection of Muscle Tension Dysphonia Using Eulerian Video Magnification: A Pilot Study *Jason Adleberg, †Ashley P. O’Connell Ferster, ‡Daniel A. Benito, and §Robert T. Sataloff, *xPhiladelphia, and yHershey, Pennsylvania, and zWashington, District of Columbia
Summary: Objective. To determine whether Eulerian Video Magnification software is useful in diagnosis of muscle tension dysphonia (MTD). Study Design. Prospective. Methods. Adult patients scheduled in a tertiary care laryngology practice for evaluation of dysphonia were recruited between November 2016 and March 2017. Demographic and clinical data were extracted from patient charts. Diagnosis of MTD was confirmed with videostroboscopic and physical exam and by a speech-language pathologist. Eighteen MTD patients were video recorded while at rest and with phonation. Five patients without MTD also were analyzed as controls. Videos were analyzed using Eulerian Video Magnification software (Massachusetts Institute of Technology) to assess change in blood flow at the forehead, infrahyoid muscles, and sternocleidomastoid muscles, while using the values of the background wall as a control value. Results. Patients with MTD demonstrated little change in perfusion to the infrahyoid muscles of the neck while phonating (+1% § 55%). Control subjects demonstrated an increase in perfusion to the infrahyoid muscles while phonating (+102% § 164%), with this change being significant when comparing the two groups (P = 0.04, t = 2.189, df = 21). A change in perfusion of 0% or less to infrahyoid muscles was 75% sensitive and 70% specific for diagnosis of MTD. No differences in perfusion were found between other regions assessed. Patient age and gender did not correlate with any change in perfusion between rest and phonation. Conclusion. Our data suggest that Eulerian Video Magnification can be used in the diagnosis of MTD by focusing on the difference in perfusion to the infrahyoid muscles between rest and phonation. Key Words: Muscle tension dysphonia−Eulerian Video Magnification−Invisible motion−Laryngology−Dysphonia.
INTRODUCTION Muscle tension dysphonia (MTD) is a term used to describe difficulty with phonation due to contraction of the paralaryngeal musculature.1,2 Features of MTD may include palpably increased muscle tension in the paralaryngeal and suprahyoid muscles with phonation, elevation of the larynx in the neck on increasing vocal pitch, an open posterior glottic chink between the arytenoid cartilages on phonation, and variable degrees of mucosal changes, such as vocal nodules or chronic laryngitis.3 Increased tension of extralaryngeal muscles may shift the larynx superiorly or inferiorly, disturbing alignment of cartilaginous structures of the larynx, and may be associated with dysphonia.1 More recent Accepted for publication February 13, 2019. Meeting Information: Accepted for poster presentation at the 2018 Annual Meeting of The American Laryngological Association, National Harbor, MD, April 18−20, 2018. Level of Evidence: 4. Competing Interests: The authors declare that they have no competing interests. From the *Drexel University College of Medicine, Philadelphia, Pennsylvania; yDepartment of Surgery, Division of Otolaryngology − Head & Neck Surgery, Penn State Health: Milton S. Hershey Medical Center, Hershey, Pennsylvania; zDepartment of Surgery, Division of Otolaryngology − Head & Neck Surgery, The George Washington University School of Medicine and Health Sciences, Washington, District of Columbia; and the xDepartment of Otolaryngology − Head & Neck Surgery, Drexel University College of Medicine, Philadelphia, Pennsylvania. Address correspondence and reprint requests to Robert T. Sataloff, Otolaryngology − Head & Neck Surgery, Drexel University College of Medicine, 219 N. Broad Street, 10th Floor, Philadelphia, PA 19107. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.02.006
thinking about MTD has suggested the condition as a disease with multifactorial etiology as opposed to a standalone entity.4−9 Diagnosis of MTD is difficult, and it can be confused with other disorders such as spasmodic dysphonia.10,11 Moreover, many commonly used clinical diagnostic methods, such as history taking and musculoskeletal assessments via palpation, are prone to variability.12 While laryngeal elevation is a common finding in MTD, assessment scales for its measurement have low reliability and validity.13−15 Radiography and surface electromyography (sEMG) have been proposed as more objective measurements of MTD. A study of radiographs by Lowell et al reported elevated hyoid and larynx positions during phonation in MTD patients compared with normal subjects.16 Several studies have used sEMG to record muscle activation using surface electrodes.12,15,17−23 These studies have demonstrated that paralaryngeal muscles are activated during phonation. However, problems with reproducibility of these sEMG experiments have led to inconclusive and mixed results with this approach.12 In an effort to improve objective detection of MTD, we assessed the utility of Eulerian Video Magnification (EVM). EVM is an open-source software program developed at the Massachusetts Institute of Technology which can be used to measure muscle activation.24,25 This technology measures muscle activation in a manner different from sEMG. This software is used on digital video recordings of patients. It focuses on an anatomical region of interest and tracks the
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change in pixel redness over a given amount of time. This slight change in pixel redness, which may not be visible to the human eye, signifies a change in blood perfusion. This subtle change in blood perfusion can then extrapolated to measure muscle activation.26−29 In medicine, EVM has been used to monitor vital signs,30−32 fasciculations in patients with Amyotrophic Lateral Sclerosis,33 and microvascular blood perfusion.34−36 In one study within the Otolaryngology-Head and Neck Surgery literature, EVM was used for noninvasive monitoring of perfusion in free flaps.37 Using EVM, the degree in color change allowed for intraoperative assessment of perfusion, with the hope of using this technology to monitor perfusion in the postoperative setting following anastomosis and inset of free flaps. To the author’s knowledge, EVM has not been used otherwise within the Laryngology or OtolaryngologyHead and Neck Surgery literature. Our study investigated whether EVM may have diagnostic utility for the assessment of MTD. To the knowledge of the authors, correlations between extralaryngeal muscle blood perfusion and a diagnosis of MTD have not been studied. It is known that, with skeletal muscle contraction, both arterial and venous blood flow are increased due to a phenomenon known as exercise hyperemia.26−29 Therefore, we hypothesized that in patients with baseline muscle contraction as noted in MTD, there would be less potential for muscle contraction during phonation. In turn, there would not be a large change in blood flow to extralaryngeal muscles in patients with MTD. Using EVM, we aimed to examine differences in extralaryngeal muscle perfusion during rest and phonation in patients with and without MTD. With this knowledge, EVM has the potential to alter our understanding of the complex body motions involved in phonation. To our knowledge, this is the first study to use EVM within the field of Laryngology. MATERIALS AND METHODS Participants The study was approved by the Institutional Review Board at Drexel University College of Medicine in Philadelphia, Pennsylvania. Adult patients in a tertiary care laryngology practice were recruited for the study between November 2016 and March 2017. All patients were already scheduled for assessment of dysphonia and underwent standard evaluation in the laryngology office, including videostroboscopy and voice team evaluation. Patients with MTD were deemed candidates for inclusion if they demonstrated supraglottic compression, pressed phonation, excessive strap muscle tension, and other signs, such as laryngeal elevation during phonation. The selected patients were those only with findings of MTD and presented with findings typical of MTD. This diagnosis was confirmed independently by a laryngologist and a speech-language pathologist. Patients were excluded from the study if they did not speak English or were under the age of 18 years. Twenty-four patients were recruited for the study. Due to excess movement in videos, six patients were excluded from
the statistical analysis. A total of 18 patients were thus included. Additionally, five patients with no history of or exam findings consistent with a voice disorder, such as MTD, were included in the control population. Demographic and clinical data were extracted from the charts on each patient and control subject. Patients included in the study gave written consent obtained by the authors. Chisquared tests were used to test for the prevalence of different comorbidities in both groups. Recording of Videos Each patient underwent video recording with a Canon Powershot SD1400IS camera, with a 28-mm wide lens and 14.1-megapixel resolution. In order to ensure stability throughout the recordings, a tripod was used. Autofocus was not used to ensure consistent image quality. Videos of a frontal view were recorded using standard studio lighting with a white backdrop in a quiet room. Videos were recorded with the patient at rest and during phonation while saying /i/. Each video was recorded for 10 seconds, and a consistent, stable video segment of exactly 4 seconds was spliced out to ensure a homogenous number and quality of frames in each video for analysis. All videos were de-identified and stored on a secure computer. Eulerian Video Magnification Analysis of video data was conducted following a protocol similar to the original publication describing the process of EVM.24 Change in pixel redness over time was extracted and amplified from the captured video recordings; these changes resembled sine waves in each subject, corresponding to their heart rate (Figure 1). From each sine wave, a Fourier Transform was used to compute the subject’s heart rate and the intensity of perfusion. Four specific regions of interest were selected for each video to focus on change in blood flow: (1) medial forehead, (2) the body of sternocleidomastoid, (3) infrahyoid muscles, and (4) the wall next to the patient (Figure 2). The medial forehead was included as a control, as the forehead musculature is not involved in phonation. The body of the sternocleidomastoid muscle was included due to its proximity to the extralaryngeal musculature in an effort to ensure no perfusion changes in other muscles of the neck during phonation. The wall served as a control to ensure that the software was not confounded by lighting or video recording. The infrahyoid muscles were the most visible muscles involved with phonation that could be recorded while the patient was at rest and phonating. The suprahyoid region was not adequately captured on video with the patient in a seated position. Therefore, it was not included in our analysis. In order to extract perfusion data from a patient video, this technology requires the selection and calibration of several parameters. The amplified frequency range was set from 0.8 Hz to 1.4 Hz, representing a resting heart rate range of 48−84 beats per minute. The alpha level, a magnification parameter, was set to 25. The sampling rate was set to 30
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MTD Detection Using Video Magnification
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FIGURE 1. Analysis of blood perfusion using Eulerian Video Magnification technology. frames per second, chromatic attenuation was set to 4, and the magnification type was set to color magnification instead of motion magnification. These values were chosen from original studies of the software by its authors and kept constant for all participants in the study. As the sampling rate far exceeded the heart rate in each captured video, no concern was warranted that the sampling rate could confound results.
Calibration for Control Subjects To ensure the accuracy of our approach, videos from subjects without MTD were collected during three sessions over a 2-week period. Values for each patient were compared over multiple dates to ensure consistency. Paired t tests were used to determine whether there was significant variation with values recorded for control subjects. Videos
from each subject with MTD were recorded at one sitting, due to uncertain patient follow-up. Volunteer control subjects were available for repeat testing to ensure accuracy and reliability of the calibration methodology. Analysis of Perfusion Intensity Data Once EVM was applied to the four areas of interest in each video, perfusion frequencies and intensities were extracted and recorded. For each patient, percent change in perfusion was calculated between values at rest versus during phonation. Unpaired t tests were used to measure differences in percent change in perfusion between control and MTD patients. Influence of Age and Gender on Perfusion Intensity and Ratios The influence of age and gender was investigated evaluating percent change in perfusion for all patients. Pearson’s correlation coefficients and unpaired t tests were calculated. Microsoft Excel was used to make all calculations. RESULTS Characteristics of MTD Patients and Normal Speakers Eighteen patients with MTD were included (12 women, 6 men; mean age 44 years, age range 22−87 years). Five control subjects without a history of MTD were recruited (three women, two men; mean age 32 years, age range 29−38 years). Patients from both groups exhibited various comorbidities, although there were no significant differences in prevalence between the two groups (Table 1).
FIGURE 2. *Sites of perfusion measurement for patients with muscle tension dysphonia (MTD) and control subjects; sites include (1) forehead; (2) infrahyoid muscles; (3) sternocleidomastoid; 4) wall (not pictured). *Image modified from "Elementary Anatomy and Physiology: for Colleges, Academies, and Other Schools", by Edward Hitchcock, p 115. Published date 1860.
Influence of Age and Gender on Perfusion Ratios The effects of age and gender were studied to determine whether they influenced perfusion ratios in patients. Age (Table 2) and gender (Table 3) were not correlated with a change in perfusion during phonation. The average ages of the control and MTD groups were 32 and 44 years old, respectively. The percent genders of the control and MTD groups were 40% and 33% male, respectively.
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TABLE 1. Prevalence of Comorbidities and Surgical History of Patients With Muscle Tension Dysphonia (MTD) and Control Subjects Condition
MTD Prevalence (n = 18)
Control Prevalence (n = 5)
P Value*
Chi-Squared
6 (33%) 4 (22%) 1 (6%) 2 (11%) 2 (11%) 3 (17%) 1 (6%)
3 (60%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%)
0.28 0.25 0.58 0.44 0.44 0.33 0.58
1.148 1.271 0.301 0.576 0.576 0.938 0.301
Pulmonary disease Neck surgery Chest/lung surgery Phonosurgery Neurologic disorders Musculoskeletal disorders Cervical spine surgery * Significant P value <0.05.
TABLE 2. Correlation Coefficients (r) of Percent Change in Perfusion Versus Patient Age Site of Perfusion Ratio Measurement
Correlation Coefficient (r) with Age
P Value*
¡0.053 ¡0.007
0.77 0.96
¡0.091 ¡0.298
0.62 0.10
Forehead Sternocleidomastoid muscle Infrahyoid muscles wall
demonstrated significantly different patterns in perfusion. During phonation, perfusion increased by 102% § 164% in control subjects, and increased by 1% § 55% in MTD patients (P = 0.04, t = 2.29, df = 21). Analysis at this site yielded several options for cut-off values which can be used to rule-in or rule-out MTD in our patient set. A change in perfusion of 0% or less was 75% sensitive and 70% specific for diagnosis of MTD. The area under the Receiver Operating Curve was 0.77. No significant differences in percent change in perfusion were seen between phonation and rest at the three other sites observed (Table 5).
* Significant P value <0.05.
Calibration for Control Subjects Data from five control subjects were collected during three sessions over a 2-week period. Using one-sample t tests, values were not found to vary significantly over the 2 week time period (Table 4), except for the wall measurement (P = 0.04, t = 4.84, df = 2) for Patient #3.
EVM Values Percent change in perfusion values was calculated for control and MTD patients. Only the infrahyoid muscles
DISCUSSION This study compared blood perfusion levels of four regions in 18 patients with MTD and five patients, each recorded three times, without MTD. In this pilot study, our data suggest that EVM can be used in the diagnosis of MTD by focusing on the difference in perfusion to the infrahyoid muscles between rest and phonation. Patients with MTD experienced little change in infrahyoid muscle perfusion during phonation, whereas control subjects experienced a two-fold increase in perfusion. We hypothesize that since patients with MTD have a higher baseline state of muscle tension, there is less
TABLE 3. Difference in Percent Change in Perfusion (%) Versus Male and Female Gender
Site of Perfusion Measurement Forehead Sternocleidomastoid muscle Infrahyoid muscles Wall * Significant P value <0.05. † Degrees of freedom (df) for all cases was 30.
Percent Change in Perfusion in Men (%) (n = 11)
Percent Change in Perfusion in Women (%) (n = 21)
P Value*
t Value†
2.2 § 55.3 106.6 § 177.7 100.1 § 174.2 27.6 § 76.4
36.6 § 103.0 66.4 § 110.1 20.2 § 86.9 11.2 § 39.7
0.31 0.43 0.09 0.42
1.032 0.800 1.751 0.817
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* Significant P value <0.05. † Degrees of freedom (df) for all cases was 2.
77.5 § 123.5 18.4 § 37.7 ¡25.0 § 46.5 ¡5.4 § 59.1 4.4 § 67.5
0.34 0.44 0.40 0.88 0.91
1.24 0.95 1.06 0.17 0.12
89.6 § 62.3 105.1 § 193 32.3 § 59.4 141.6 § 191.0 224.2 § 317.4
0.06 0.39 0.39 0.26 0.28
3.89 1.08 1.08 1.55 1.46
92.8 § 68.1 116.6 § 162.5 ¡16.6 § 31.8 107.7 § 211.8 210.7 § 290.1
0.07 0.28 0.41 0.42 0.27
3.57 1.46 1.03 1.00 1.51
11.9 § 33.7 ¡32.4 § 57.8 38.1 § 22.9 75 § 108.9 44.4 § 91.7
0.57 0.39 0.04 0.29 0.44
0.67 1.08 4.84 1.42 0.95
MTD Detection Using Video Magnification
Control 1 Control 2 Control 3 Control 4 Control 5
SternocleidoP Value t Value Mastoid Muscle P Value t Value Infrahyoid Muscles P Value* t Value† Forehead Control patient No.
Percent (%) Change in Perfusion (average percent over three sessions)
TABLE 4. Percent Change in Perfusion (%) for Control Subjects at Three Sessions Over a 2-Week Time Period
Wall
P Value t Value
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change in muscle contraction during phonation in MTD patients. Since there is less change in muscle contraction, this results in less change in perfusion. This decreased change of perfusion was demonstrated with EVM technology. A change in perfusion of 0% or less was 75% sensitive and 70% specific for diagnosis of MTD. Percent change in perfusion was smaller in MTD patients than in control patients, with this difference being statistically significant (P = 0.04). Due to the small number of patients in this pilot study, it is possible that this statistical significance was due to chance. However, our findings are supported by what would be expected based on our understanding of skeletal muscle physiology.26−29 Given that EVM is a new technology, best practices have yet to be established for its clinical use. Successful use of the technology requires both consistent technique for capture of video subjects and appropriate analysis of results obtained. A relatively strict, controlled environment with consistent lighting and steady filming is necessary. Any excess movement of the video recording is detected by the sensitive EVM software, making the use of a stabilizing unit such as a camera tripod essential. Slight patient movement also can distort results, as we found in our study. Appropriate selection of patients is also critical, as recordings from several of our patients had to be discarded due to resting tremor. Tremor distorted elements of the video and rendered EVM analysis invalid. As EVM analyzes the change in pixel redness of a subject, variable lighting and filming conditions can introduce noisy data. We believe that while our control subjects did not show significant variation in blood perfusion over multiple recording sessions, the variation found could be reduced further with an even more rigorous recording setup. Moreover, analysis of blood perfusion is sensitive to differences in skin tone between patients.34 This factor does not occur with Doppler Ultrasound, which has also been used previously with skeletal muscle perfusion for diagnosis of disease states.38−40 This study is subject to a few additional limitations. First, there was a small sample of control subjects used in our analysis. This small size likely led to larger degrees of variability in data obtained within the control patients’ group. Accordingly, a larger sample of control patients would allow for higher reliability of results. Recruitment of control patients (ie, patients without voice disorders) was limited, as patients were recruited from a tertiary care laryngology clinic with a vast majority of referred patients presenting with a voice disorder. Future studies would benefit from recruitment of patients from nonlaryngology clinics in order to increase the number of control patients. In addition, our analysis did not examine perfusion to the suprahyoid musculature. Since our camera faced seated subjects at a perpendicular angle, we were unable to adequately capture the muscles of the suprahyoid region on video. In order to obtain video of this region, it would require the patient to be in an uncomfortable and unnatural position with extreme neck extension. This position would not be reasonably applied in a clinical setting due to patient
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TABLE 5. Percent Change in Perfusion (%) for Control and Muscle Tension Dysphonia (MTD) Patients
Region of interest
Percent Change in Perfusion, Control (%) (n = 5)
Percent Change in Perfusion, MTD (%) (n = 18)
P Value*
t Value†
14 § 69 119 § 168 102 § 164 28 § 68
31 § 103 59 § 103 1 § 55 6 § 39
0.58 0.26 0.04* 0.30
0.562 1.157 2.189 1.062
Forehead Sternocleidomastoid Infrahyoid Wall * Significant P value <0.05. † Degrees of freedom (df) for all cases was 21.
discomfort. This position may have also caused other neck musculature to become contracted during phonation and at rest, which could have been a confounder to our analysis if this was applied. Finally, our approach was unable to separate the individual contributions of the omohyoid, sternohyoid, sternothyroid, and thyrohyoid muscles. We believe that higher video resolution capture may facilitate the ability to do so. Further study of EVM is warranted for patients with MTD, not only preceding but also following voice therapy. Clinicians could potentially use this software to aid in narrowing their differential diagnosis as well as to track patient progress during voice therapy. Depending on patient progress as detected by perfusion via EVM, clinicians could alter treatment regimens in order to improve patient outcomes. Future studies may also include the use of this technology to help differentiate patients with MTD due to muscle-based hyperfunction from those patients with emotional-based hyperfunction, which could also help to direct therapy. CONCLUSION This study investigated the utility of EVM in detecting differences in perfusion to the extralaryngeal and, specifically, infrahyoid muscles. Patients with MTD demonstrated little change in perfusion to the infrahyoid muscles while phonating, but there was an increase in perfusion to the same location in control subjects. This difference in percent change in perfusion between control and MTD patients makes EVM a potential tool for diagnosing MTD and for monitoring efficacy of treatment, however, the utility of EVM for these purposes certainly warrants additional study. Acknowledgments We would like to thank Drexel University for their support of this research. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.02.006.
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Detection of Muscle Tension Dysphonia Using Eulerian Video Magnification: A Pilot Study *Jason Adleberg, †Ashley P. O’Connell Ferster, ‡Daniel A. Benito, and §Robert T. Sataloff, *xPhiladelphia, and yHershey, Pennsylvania, and zWashington, District of Columbia
Summary: Objective. To determine whether Eulerian Video Magnification software is useful in diagnosis of muscle tension dysphonia (MTD). Study Design. Prospective. Methods. Adult patients scheduled in a tertiary care laryngology practice for evaluation of dysphonia were recruited between November 2016 and March 2017. Demographic and clinical data were extracted from patient charts. Diagnosis of MTD was confirmed with videostroboscopic and physical exam and by a speech-language pathologist. Eighteen MTD patients were video recorded while at rest and with phonation. Five patients without MTD also were analyzed as controls. Videos were analyzed using Eulerian Video Magnification software (Massachusetts Institute of Technology) to assess change in blood flow at the forehead, infrahyoid muscles, and sternocleidomastoid muscles, while using the values of the background wall as a control value. Results. Patients with MTD demonstrated little change in perfusion to the infrahyoid muscles of the neck while phonating (+1% § 55%). Control subjects demonstrated an increase in perfusion to the infrahyoid muscles while phonating (+102% § 164%), with this change being significant when comparing the two groups (P = 0.04, t = 2.189, df = 21). A change in perfusion of 0% or less to infrahyoid muscles was 75% sensitive and 70% specific for diagnosis of MTD. No differences in perfusion were found between other regions assessed. Patient age and gender did not correlate with any change in perfusion between rest and phonation. Conclusion. Our data suggest that Eulerian Video Magnification can be used in the diagnosis of MTD by focusing on the difference in perfusion to the infrahyoid muscles between rest and phonation. Key Words: Muscle tension dysphonia−Eulerian Video Magnification−Invisible motion−Laryngology−Dysphonia.
INTRODUCTION Muscle tension dysphonia (MTD) is a term used to describe difficulty with phonation due to contraction of the paralaryngeal musculature.1,2 Features of MTD may include palpably increased muscle tension in the paralaryngeal and suprahyoid muscles with phonation, elevation of the larynx in the neck on increasing vocal pitch, an open posterior glottic chink between the arytenoid cartilages on phonation, and variable degrees of mucosal changes, such as vocal nodules or chronic laryngitis.3 Increased tension of extralaryngeal muscles may shift the larynx superiorly or inferiorly, disturbing alignment of cartilaginous structures of the larynx, and may be associated with dysphonia.1 More recent Accepted for publication February 13, 2019. Meeting Information: Accepted for poster presentation at the 2018 Annual Meeting of The American Laryngological Association, National Harbor, MD, April 18−20, 2018. Level of Evidence: 4. Competing Interests: The authors declare that they have no competing interests. From the *Drexel University College of Medicine, Philadelphia, Pennsylvania; yDepartment of Surgery, Division of Otolaryngology − Head & Neck Surgery, Penn State Health: Milton S. Hershey Medical Center, Hershey, Pennsylvania; zDepartment of Surgery, Division of Otolaryngology − Head & Neck Surgery, The George Washington University School of Medicine and Health Sciences, Washington, District of Columbia; and the xDepartment of Otolaryngology − Head & Neck Surgery, Drexel University College of Medicine, Philadelphia, Pennsylvania. Address correspondence and reprint requests to Robert T. Sataloff, Otolaryngology − Head & Neck Surgery, Drexel University College of Medicine, 219 N. Broad Street, 10th Floor, Philadelphia, PA 19107. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.02.006
thinking about MTD has suggested the condition as a disease with multifactorial etiology as opposed to a standalone entity.4−9 Diagnosis of MTD is difficult, and it can be confused with other disorders such as spasmodic dysphonia.10,11 Moreover, many commonly used clinical diagnostic methods, such as history taking and musculoskeletal assessments via palpation, are prone to variability.12 While laryngeal elevation is a common finding in MTD, assessment scales for its measurement have low reliability and validity.13−15 Radiography and surface electromyography (sEMG) have been proposed as more objective measurements of MTD. A study of radiographs by Lowell et al reported elevated hyoid and larynx positions during phonation in MTD patients compared with normal subjects.16 Several studies have used sEMG to record muscle activation using surface electrodes.12,15,17−23 These studies have demonstrated that paralaryngeal muscles are activated during phonation. However, problems with reproducibility of these sEMG experiments have led to inconclusive and mixed results with this approach.12 In an effort to improve objective detection of MTD, we assessed the utility of Eulerian Video Magnification (EVM). EVM is an open-source software program developed at the Massachusetts Institute of Technology which can be used to measure muscle activation.24,25 This technology measures muscle activation in a manner different from sEMG. This software is used on digital video recordings of patients. It focuses on an anatomical region of interest and tracks the
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change in pixel redness over a given amount of time. This slight change in pixel redness, which may not be visible to the human eye, signifies a change in blood perfusion. This subtle change in blood perfusion can then extrapolated to measure muscle activation.26−29 In medicine, EVM has been used to monitor vital signs,30−32 fasciculations in patients with Amyotrophic Lateral Sclerosis,33 and microvascular blood perfusion.34−36 In one study within the Otolaryngology-Head and Neck Surgery literature, EVM was used for noninvasive monitoring of perfusion in free flaps.37 Using EVM, the degree in color change allowed for intraoperative assessment of perfusion, with the hope of using this technology to monitor perfusion in the postoperative setting following anastomosis and inset of free flaps. To the author’s knowledge, EVM has not been used otherwise within the Laryngology or OtolaryngologyHead and Neck Surgery literature. Our study investigated whether EVM may have diagnostic utility for the assessment of MTD. To the knowledge of the authors, correlations between extralaryngeal muscle blood perfusion and a diagnosis of MTD have not been studied. It is known that, with skeletal muscle contraction, both arterial and venous blood flow are increased due to a phenomenon known as exercise hyperemia.26−29 Therefore, we hypothesized that in patients with baseline muscle contraction as noted in MTD, there would be less potential for muscle contraction during phonation. In turn, there would not be a large change in blood flow to extralaryngeal muscles in patients with MTD. Using EVM, we aimed to examine differences in extralaryngeal muscle perfusion during rest and phonation in patients with and without MTD. With this knowledge, EVM has the potential to alter our understanding of the complex body motions involved in phonation. To our knowledge, this is the first study to use EVM within the field of Laryngology. MATERIALS AND METHODS Participants The study was approved by the Institutional Review Board at Drexel University College of Medicine in Philadelphia, Pennsylvania. Adult patients in a tertiary care laryngology practice were recruited for the study between November 2016 and March 2017. All patients were already scheduled for assessment of dysphonia and underwent standard evaluation in the laryngology office, including videostroboscopy and voice team evaluation. Patients with MTD were deemed candidates for inclusion if they demonstrated supraglottic compression, pressed phonation, excessive strap muscle tension, and other signs, such as laryngeal elevation during phonation. The selected patients were those only with findings of MTD and presented with findings typical of MTD. This diagnosis was confirmed independently by a laryngologist and a speech-language pathologist. Patients were excluded from the study if they did not speak English or were under the age of 18 years. Twenty-four patients were recruited for the study. Due to excess movement in videos, six patients were excluded from
the statistical analysis. A total of 18 patients were thus included. Additionally, five patients with no history of or exam findings consistent with a voice disorder, such as MTD, were included in the control population. Demographic and clinical data were extracted from the charts on each patient and control subject. Patients included in the study gave written consent obtained by the authors. Chisquared tests were used to test for the prevalence of different comorbidities in both groups. Recording of Videos Each patient underwent video recording with a Canon Powershot SD1400IS camera, with a 28-mm wide lens and 14.1-megapixel resolution. In order to ensure stability throughout the recordings, a tripod was used. Autofocus was not used to ensure consistent image quality. Videos of a frontal view were recorded using standard studio lighting with a white backdrop in a quiet room. Videos were recorded with the patient at rest and during phonation while saying /i/. Each video was recorded for 10 seconds, and a consistent, stable video segment of exactly 4 seconds was spliced out to ensure a homogenous number and quality of frames in each video for analysis. All videos were de-identified and stored on a secure computer. Eulerian Video Magnification Analysis of video data was conducted following a protocol similar to the original publication describing the process of EVM.24 Change in pixel redness over time was extracted and amplified from the captured video recordings; these changes resembled sine waves in each subject, corresponding to their heart rate (Figure 1). From each sine wave, a Fourier Transform was used to compute the subject’s heart rate and the intensity of perfusion. Four specific regions of interest were selected for each video to focus on change in blood flow: (1) medial forehead, (2) the body of sternocleidomastoid, (3) infrahyoid muscles, and (4) the wall next to the patient (Figure 2). The medial forehead was included as a control, as the forehead musculature is not involved in phonation. The body of the sternocleidomastoid muscle was included due to its proximity to the extralaryngeal musculature in an effort to ensure no perfusion changes in other muscles of the neck during phonation. The wall served as a control to ensure that the software was not confounded by lighting or video recording. The infrahyoid muscles were the most visible muscles involved with phonation that could be recorded while the patient was at rest and phonating. The suprahyoid region was not adequately captured on video with the patient in a seated position. Therefore, it was not included in our analysis. In order to extract perfusion data from a patient video, this technology requires the selection and calibration of several parameters. The amplified frequency range was set from 0.8 Hz to 1.4 Hz, representing a resting heart rate range of 48−84 beats per minute. The alpha level, a magnification parameter, was set to 25. The sampling rate was set to 30
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FIGURE 1. Analysis of blood perfusion using Eulerian Video Magnification technology. frames per second, chromatic attenuation was set to 4, and the magnification type was set to color magnification instead of motion magnification. These values were chosen from original studies of the software by its authors and kept constant for all participants in the study. As the sampling rate far exceeded the heart rate in each captured video, no concern was warranted that the sampling rate could confound results.
Calibration for Control Subjects To ensure the accuracy of our approach, videos from subjects without MTD were collected during three sessions over a 2-week period. Values for each patient were compared over multiple dates to ensure consistency. Paired t tests were used to determine whether there was significant variation with values recorded for control subjects. Videos
from each subject with MTD were recorded at one sitting, due to uncertain patient follow-up. Volunteer control subjects were available for repeat testing to ensure accuracy and reliability of the calibration methodology. Analysis of Perfusion Intensity Data Once EVM was applied to the four areas of interest in each video, perfusion frequencies and intensities were extracted and recorded. For each patient, percent change in perfusion was calculated between values at rest versus during phonation. Unpaired t tests were used to measure differences in percent change in perfusion between control and MTD patients. Influence of Age and Gender on Perfusion Intensity and Ratios The influence of age and gender was investigated evaluating percent change in perfusion for all patients. Pearson’s correlation coefficients and unpaired t tests were calculated. Microsoft Excel was used to make all calculations. RESULTS Characteristics of MTD Patients and Normal Speakers Eighteen patients with MTD were included (12 women, 6 men; mean age 44 years, age range 22−87 years). Five control subjects without a history of MTD were recruited (three women, two men; mean age 32 years, age range 29−38 years). Patients from both groups exhibited various comorbidities, although there were no significant differences in prevalence between the two groups (Table 1).
FIGURE 2. *Sites of perfusion measurement for patients with muscle tension dysphonia (MTD) and control subjects; sites include (1) forehead; (2) infrahyoid muscles; (3) sternocleidomastoid; 4) wall (not pictured). *Image modified from "Elementary Anatomy and Physiology: for Colleges, Academies, and Other Schools", by Edward Hitchcock, p 115. Published date 1860.
Influence of Age and Gender on Perfusion Ratios The effects of age and gender were studied to determine whether they influenced perfusion ratios in patients. Age (Table 2) and gender (Table 3) were not correlated with a change in perfusion during phonation. The average ages of the control and MTD groups were 32 and 44 years old, respectively. The percent genders of the control and MTD groups were 40% and 33% male, respectively.
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TABLE 1. Prevalence of Comorbidities and Surgical History of Patients With Muscle Tension Dysphonia (MTD) and Control Subjects Condition
MTD Prevalence (n = 18)
Control Prevalence (n = 5)
P Value*
Chi-Squared
6 (33%) 4 (22%) 1 (6%) 2 (11%) 2 (11%) 3 (17%) 1 (6%)
3 (60%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%)
0.28 0.25 0.58 0.44 0.44 0.33 0.58
1.148 1.271 0.301 0.576 0.576 0.938 0.301
Pulmonary disease Neck surgery Chest/lung surgery Phonosurgery Neurologic disorders Musculoskeletal disorders Cervical spine surgery * Significant P value <0.05.
TABLE 2. Correlation Coefficients (r) of Percent Change in Perfusion Versus Patient Age Site of Perfusion Ratio Measurement
Correlation Coefficient (r) with Age
P Value*
¡0.053 ¡0.007
0.77 0.96
¡0.091 ¡0.298
0.62 0.10
Forehead Sternocleidomastoid muscle Infrahyoid muscles wall
demonstrated significantly different patterns in perfusion. During phonation, perfusion increased by 102% § 164% in control subjects, and increased by 1% § 55% in MTD patients (P = 0.04, t = 2.29, df = 21). Analysis at this site yielded several options for cut-off values which can be used to rule-in or rule-out MTD in our patient set. A change in perfusion of 0% or less was 75% sensitive and 70% specific for diagnosis of MTD. The area under the Receiver Operating Curve was 0.77. No significant differences in percent change in perfusion were seen between phonation and rest at the three other sites observed (Table 5).
* Significant P value <0.05.
Calibration for Control Subjects Data from five control subjects were collected during three sessions over a 2-week period. Using one-sample t tests, values were not found to vary significantly over the 2 week time period (Table 4), except for the wall measurement (P = 0.04, t = 4.84, df = 2) for Patient #3.
EVM Values Percent change in perfusion values was calculated for control and MTD patients. Only the infrahyoid muscles
DISCUSSION This study compared blood perfusion levels of four regions in 18 patients with MTD and five patients, each recorded three times, without MTD. In this pilot study, our data suggest that EVM can be used in the diagnosis of MTD by focusing on the difference in perfusion to the infrahyoid muscles between rest and phonation. Patients with MTD experienced little change in infrahyoid muscle perfusion during phonation, whereas control subjects experienced a two-fold increase in perfusion. We hypothesize that since patients with MTD have a higher baseline state of muscle tension, there is less
TABLE 3. Difference in Percent Change in Perfusion (%) Versus Male and Female Gender
Site of Perfusion Measurement Forehead Sternocleidomastoid muscle Infrahyoid muscles Wall * Significant P value <0.05. † Degrees of freedom (df) for all cases was 30.
Percent Change in Perfusion in Men (%) (n = 11)
Percent Change in Perfusion in Women (%) (n = 21)
P Value*
t Value†
2.2 § 55.3 106.6 § 177.7 100.1 § 174.2 27.6 § 76.4
36.6 § 103.0 66.4 § 110.1 20.2 § 86.9 11.2 § 39.7
0.31 0.43 0.09 0.42
1.032 0.800 1.751 0.817
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* Significant P value <0.05. † Degrees of freedom (df) for all cases was 2.
77.5 § 123.5 18.4 § 37.7 ¡25.0 § 46.5 ¡5.4 § 59.1 4.4 § 67.5
0.34 0.44 0.40 0.88 0.91
1.24 0.95 1.06 0.17 0.12
89.6 § 62.3 105.1 § 193 32.3 § 59.4 141.6 § 191.0 224.2 § 317.4
0.06 0.39 0.39 0.26 0.28
3.89 1.08 1.08 1.55 1.46
92.8 § 68.1 116.6 § 162.5 ¡16.6 § 31.8 107.7 § 211.8 210.7 § 290.1
0.07 0.28 0.41 0.42 0.27
3.57 1.46 1.03 1.00 1.51
11.9 § 33.7 ¡32.4 § 57.8 38.1 § 22.9 75 § 108.9 44.4 § 91.7
0.57 0.39 0.04 0.29 0.44
0.67 1.08 4.84 1.42 0.95
MTD Detection Using Video Magnification
Control 1 Control 2 Control 3 Control 4 Control 5
SternocleidoP Value t Value Mastoid Muscle P Value t Value Infrahyoid Muscles P Value* t Value† Forehead Control patient No.
Percent (%) Change in Perfusion (average percent over three sessions)
TABLE 4. Percent Change in Perfusion (%) for Control Subjects at Three Sessions Over a 2-Week Time Period
Wall
P Value t Value
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change in muscle contraction during phonation in MTD patients. Since there is less change in muscle contraction, this results in less change in perfusion. This decreased change of perfusion was demonstrated with EVM technology. A change in perfusion of 0% or less was 75% sensitive and 70% specific for diagnosis of MTD. Percent change in perfusion was smaller in MTD patients than in control patients, with this difference being statistically significant (P = 0.04). Due to the small number of patients in this pilot study, it is possible that this statistical significance was due to chance. However, our findings are supported by what would be expected based on our understanding of skeletal muscle physiology.26−29 Given that EVM is a new technology, best practices have yet to be established for its clinical use. Successful use of the technology requires both consistent technique for capture of video subjects and appropriate analysis of results obtained. A relatively strict, controlled environment with consistent lighting and steady filming is necessary. Any excess movement of the video recording is detected by the sensitive EVM software, making the use of a stabilizing unit such as a camera tripod essential. Slight patient movement also can distort results, as we found in our study. Appropriate selection of patients is also critical, as recordings from several of our patients had to be discarded due to resting tremor. Tremor distorted elements of the video and rendered EVM analysis invalid. As EVM analyzes the change in pixel redness of a subject, variable lighting and filming conditions can introduce noisy data. We believe that while our control subjects did not show significant variation in blood perfusion over multiple recording sessions, the variation found could be reduced further with an even more rigorous recording setup. Moreover, analysis of blood perfusion is sensitive to differences in skin tone between patients.34 This factor does not occur with Doppler Ultrasound, which has also been used previously with skeletal muscle perfusion for diagnosis of disease states.38−40 This study is subject to a few additional limitations. First, there was a small sample of control subjects used in our analysis. This small size likely led to larger degrees of variability in data obtained within the control patients’ group. Accordingly, a larger sample of control patients would allow for higher reliability of results. Recruitment of control patients (ie, patients without voice disorders) was limited, as patients were recruited from a tertiary care laryngology clinic with a vast majority of referred patients presenting with a voice disorder. Future studies would benefit from recruitment of patients from nonlaryngology clinics in order to increase the number of control patients. In addition, our analysis did not examine perfusion to the suprahyoid musculature. Since our camera faced seated subjects at a perpendicular angle, we were unable to adequately capture the muscles of the suprahyoid region on video. In order to obtain video of this region, it would require the patient to be in an uncomfortable and unnatural position with extreme neck extension. This position would not be reasonably applied in a clinical setting due to patient
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TABLE 5. Percent Change in Perfusion (%) for Control and Muscle Tension Dysphonia (MTD) Patients
Region of interest
Percent Change in Perfusion, Control (%) (n = 5)
Percent Change in Perfusion, MTD (%) (n = 18)
P Value*
t Value†
14 § 69 119 § 168 102 § 164 28 § 68
31 § 103 59 § 103 1 § 55 6 § 39
0.58 0.26 0.04* 0.30
0.562 1.157 2.189 1.062
Forehead Sternocleidomastoid Infrahyoid Wall * Significant P value <0.05. † Degrees of freedom (df) for all cases was 21.
discomfort. This position may have also caused other neck musculature to become contracted during phonation and at rest, which could have been a confounder to our analysis if this was applied. Finally, our approach was unable to separate the individual contributions of the omohyoid, sternohyoid, sternothyroid, and thyrohyoid muscles. We believe that higher video resolution capture may facilitate the ability to do so. Further study of EVM is warranted for patients with MTD, not only preceding but also following voice therapy. Clinicians could potentially use this software to aid in narrowing their differential diagnosis as well as to track patient progress during voice therapy. Depending on patient progress as detected by perfusion via EVM, clinicians could alter treatment regimens in order to improve patient outcomes. Future studies may also include the use of this technology to help differentiate patients with MTD due to muscle-based hyperfunction from those patients with emotional-based hyperfunction, which could also help to direct therapy. CONCLUSION This study investigated the utility of EVM in detecting differences in perfusion to the extralaryngeal and, specifically, infrahyoid muscles. Patients with MTD demonstrated little change in perfusion to the infrahyoid muscles while phonating, but there was an increase in perfusion to the same location in control subjects. This difference in percent change in perfusion between control and MTD patients makes EVM a potential tool for diagnosing MTD and for monitoring efficacy of treatment, however, the utility of EVM for these purposes certainly warrants additional study. Acknowledgments We would like to thank Drexel University for their support of this research. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.02.006.
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