Advanced Biomedical Engineering DOI:10.14326/abe.9.10 9: 10–20, 2020. Original Paper Swallowing Pattern Classication Method Using Multichannel Surface EMG Signals of Suprahyoid and Infrahyoid Muscles * *, # * ** *** Masahiro SUZUKI, Makoto SASAKI, Katsuhiro KAMATA, Atsushi NAKAYAMA, Isamu SHIBAMOTO, † Yasushi TAMADA Abstract The ability to ne-tune the movement of swallowing-related organs and change the swallowing pattern to t the volume of a bolus, texture and the physical properties of the food to be swallowed is referred to as the swallowing reserve. In other words, it is the response capability of food swallowing to avoid choking and aspiration. Herein, we focus on the coordination of the suprahyoid and infrahyoid muscles activities, which are closely related to swallowing movement, as a rst step to develop a method to evaluate swallowing reserve, which declines due to neuromuscular disease, muscle weakness caused by aging, to mention a few. First, using two 22-channel electrodes, we measured the surface electromyography (sEMG) signals of suprahyoid and inf- rahyoid muscles during the following four swallowing conditions: combining two bolus volumes (3 and 15 mL water) and two techniques (normal and effortful swallow). Then, we veried whether the difference in swallow- ing patterns based on swallowing conditions can be classied from sEMG signals using three machine learning methods; namely, the real-time classication, comprehensive classication, and image recognition method. In the real-time classication method, the mean classication accuracy (MCA) for the four swallowing conditions was as low as 81.5%, indicating that the difference between swallowing conditions performed in a period of ap- proximately 1 s cannot be classied sufciently by this method. In the comprehensive classication method that applies a majority decision to all the classication results from the start to the end of swallowing, which can be obtained every 16 ms, MCA was 95.1%. Furthermore, in the image recognition method, the change of a series of sEMG signals in the swallowing movement was converted into swallowing pattern image, and the images were classied using a combination of deep convolutional neural networks and support vector machine (SVM). Compared with the comprehensive classication method, the number of training samples for the image recognition method was only 1/26, but the MCA reached 95.7%. This method, which can noninvasively eval- uate swallowing patterns that change slightly based on swallowing conditions, could be applied to early detec- tion of reduced swallowing function or a state of frailty (dysphagia potential) in aged individuals. Keywords: swallowing, pattern classication, suprahyoid and infrahyoid muscles, surface EMG signals. Adv Biomed Eng. 9: pp. 10–20, 2020. geal phases [1]. Swallowing is mediated by a complex 1. Introduction physiological mechanism involving “voluntary move- Swallowing is a series of movement to transport food ment” and “involuntary reexive movement.” The volun- from the oral cavity to the stomach, and is divided into tary movement mainly refers to the intraoral movement three phases; namely, the oral, pharyngeal, and esopha- to transport the bolus, which is formed by food mastica- tion, to the pharynx via tongue movement (oral phase). Involuntary movement refers to the swallowing re- Received on July 16, 2019; revised on October 21, 2019; accepted ex-mediated movement to pass the bolus through the on December 6, 2019. pharynx (pharyngeal phase). The swallowing reex is a * Graduate School of Science and Engineering, Iwate University, highly reproducible and extremely precise movement Iwate, Japan. pattern programmed by central pattern generator (CPG) ** Department of Engineering for Future Innovation, National Insti- in the medulla oblongata. Therefore, functional oral tute of Technology, Ichinoseki College, Iwate, Japan. *** Graduate School of Rehabilitation Sciences, Seirei Christopher movements and intact swallowing reex are essential for University, Shizuoka, Japan. successful swallowing. † School of Dentistry, Iwate Medical University, Iwate, Japan. Although the swallowing movement pattern induced # E-mail: [email protected] by the swallowing reex is highly reproducible, the Masahiro SUZUKI, et al: Swallowing Pattern Classication Method (11) movement pattern changes depending on differences in ful swallow), as a rst step for evaluating the swallowing the volume of the bolus (amount of food) [2–6] and the reserve. Then, we veried whether the difference in physical properties of the food (such as viscosity and swallowing patterns based on swallowing conditions hardness) [7, 8]. Therefore, the ability to ne-tune the could be classied from sEMG signals using three types movement of swallowing-related organs and change the of machine learning methods; namely, the real-time clas- swallowing pattern to t objects to be swallowed is con- sication, comprehensive classication, and image rec- sidered to be the swallowing reserve, which is the re- ognition methods. sponse capability of food swallowing in order to avoid 2. Method choking and aspiration [9–11]. However, this swallow- ing reserve declines due to neuromuscular disease, mus- 2.1 Participants cle weakness caused by aging, cerebrovascular disease, Eight healthy young men without any history of dyspha- as well as positional changes of the swallowing-related gia (22.4 ± 1.2 years of age, 171.4 ± 6.0 cm in height, organs. Furthermore, in patients with swallowing prob- 62.3 ± 7.4 kg in weight; mean ± SD) participated in the lems secondary to systemic diseases, pharyngeal residue, experiment. Approval for the study was obtained in ad- laryngeal penetration, and bolus aspiration may occur, vance by the Ethical Review Board of Iwate University with an increased risk of developing aspiration pneumo- (Number: 201808). Before starting the tests, we ex- nia [12–14]. Generally, decline of the swallowing re- plained the study objectives, experimental protocol, and serve may cause descent of the hyoid bone and larynx risks to each participant, and received written consent position, associated decrease in the amount of hyoid and from all the participants. larynx elevation in the anterosuperior direction, delay in larynx elevation due to reduced larynx elevation speed, 2.2 Measurement of sEMG signals and delay in stimulation of the swallowing reex [9, 11, The suprahyoid muscles comprise four muscles; namely, 15–17]. However, the specic reference values to detect digastric, stylohyoid, mylohyoid, and geniohyoid mus- reduced swallowing function have not yet been claried. cles, located above the hyoid bone in the neck (Fig. 1). Furthermore, the videouoroscopic examination of swal- The infrahyoid muscles are made up of four muscles; lowing, which is the gold standard of detailed examina- sternohyoid, sternothyroid, thyrohyoid, and omohyoid tion, is essential for the observation and evaluation of muscles, located below the hyoid bone in the neck. these problems. However, this method is not suitable for During swallowing, the suprahyoid muscles pull the hy- routine and regular swallowing function evaluation ow- oid bone anterosuperiorly, followed by the thyrohyoid ing to risks of radiation exposure and aspiration of con- muscle to elevate the larynx. These movements cause trast media. To extend the healthy life expectancy of the epiglottis rotation, thereby helping to prevent aspiration elderly, it is important to detect elderly individuals who while a bolus passes through the pharynx. Therefore, the have reduced swallowing function or are in a state of activities of suprahyoid and infrahyoid muscles are frailty (dysphagia potential) at an early stage [18]. Since closely related to the hyoid and laryngeal movements, these conditions are difcult to perceive by the individu- which play an essential role in the swallowing mecha- als themselves, it is necessary to develop a safe and con- nism. venient evaluation method to monitor daily changes in For measurement of sEMG signals, we designed two swallowing reserve. 22-channel electrodes based on our previous work [22]. This study focuses on the coordination of suprahy- oid and infrahyoid muscles activities as a new approach for evaluating swallowing reserve. These muscles are closely related to the movement of the hyoid and larynx and have the advantage that their activities can be ob- served from the skin surface of the anterior neck [19– 21]. Therefore, if one can detect the differences in swal- lowing patterns depending on the swallowing conditions from these surface electromyography (sEMG) signals, it may be possible to detect early decline of “the ability to change swallowing pattern (swallowing reserve).” Herein, sEMG signals of the suprahyoid and infra- hyoid muscles are measured under four swallowing con- ditions, which combines two bolus volumes (3 and Fig. 1 Structure of suprahyoid muscles and infrahyoid 15 mL of water) and two techniques (normal and effort- muscles. (12) Advanced Biomedical Engineering. Vol. 9, 2020. Table 1 Swallowing conditions combining two bolus vol- umes and two techniques. Bolus volume Technique 3 mL of water 15 mL of water Normal swallow NS3 NS15 Effortful swallow ES3 ES15 struments Corp.). We set the sampling rate to 2,000 Hz. 2.3 Swallowing conditions The swallowing reex is induced by “central input from a higher level such as the cerebral cortex,” which is in- volved in voluntary swallowing, and “peripheral input from the pharynx and larynx,” which is involved in the Fig. 2 Two 22-channel