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Analysis of the hyoid motion of tongue cancer patients
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Original Research
Analysis of the hyoid motion of tongue cancer patients Yusuke Takahashi a,∗ , Tsutomu Minamikawa a , Natsuki Yonezawa a , Hirokazu Komatsu b , Kenichi Nibu b , Takahide Komori a a
Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-Cho, Chuo-Ku, Kobe 650-0017, Japan Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-Cho, Chuo-Ku, Kobe 650-0017, Japan b
a r t i c l e
i n f o
Article history: Received 30 May 2016 Received in revised form 3 September 2016 Accepted 15 September 2016 Available online xxx Keywords: Tongue cancer Hyoid motion Videofluoroscopic examination of swallowing
a b s t r a c t Objective: We aimed to analyze movement of the hyoid bone in patients with tongue cancer following radical surgery without pre- or postoperative chemotherapy or radiotherapy. Methods: Ten patients (five males, five females; average age, 56.9 years) with histologically confirmed tongue squamous cell carcinoma underwent pre- and postoperative videofluoroscopic examination of swallowing and radical surgery at the Department of Oral and Maxillofacial Surgery of Kobe University Hospital, Japan. All patients underwent modified radical neck dissection and hemiglossectomy of the mobile tongue with reconstruction using a free radial forearm flap. Hyoid motion was analyzed using the DIPP-Motion PRO2D cineradiography system. According to previous reports, hyoid motion during swallowing is divided into three elements: rearward and upward, forward and upward, and rearward and downward movements. These movements were compared pre- and postoperatively. The endpoints were movement speed, distance, and time. Results: Postoperatively, radical surgery resulted in motor impairment of the hyoid, with decreased movement capacity, including decreased movement distance, time required, speed, and range of motion during swallowing. Conclusions: Hyoid motion analysis could be useful to maintain the quality of life of patients with oral cancer in the future as it could also be used to assess patients after bilateral neck dissection, mandibular resection, and radiotherapy. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction Oral cancer accounts for 1–5% of all malignant tumors. Epidemiologically, tongue cancer accounts for a high proportion of oral cancer cases, similar to gingival cancer. Advanced tongue cancer is likely to metastasize to the cervical lymph nodes, necessitating neck dissection with excision of the primary lesion in several cases that require immediate reconstruction according to the extent of tongue resection. However, when reconstructing the tongue, it is impossible to avoid postoperative impairment of oral functions in the form of mastication, swallowing, and articulation. Various reports regarding functional evaluation after surgery for oral cancer have focused on dysphagia. There are various
夽 Asian AOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author. Fax: +81 078 382 6229. E-mail address: crystal shooting [email protected] (Y. Takahashi).
methods to evaluate dysphagia, including tongue pressure, swallowing pressure, videofluoroscopic examination of swallowing, and endoscopic evaluation of swallowing. Here we focused on postoperative hyoid motion, which can be evaluated objectively. When swallowing, the hyoid bone exhibits upwards and rearwards motion caused by the movement of the suprahyoid muscles and substantially moves forward. Previous reports have clarified that after a bolus passes through the pharynx, the hyoid bone moves rearwards and returns to its original position. En bloc resection of the primary cervical lesion in advanced tongue cancer requires resection of the suprahyoid muscles. Therefore, we aimed to determine how resection of the suprahyoid muscles on one side disrupts the horizontal balance of the hyoid bone and changes movement speed, range, and distance during swallowing. 2. Material and methods 2.1. Patients Patient characteristics are presented in Table 1. The study cohort included ten patients with primary tongue cancer who were
http://dx.doi.org/10.1016/j.ajoms.2016.09.007 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
Please cite this article in press as: Takahashi Y, et al. Analysis of the hyoid motion of tongue cancer patients. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.007
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Table 1 Patient characteristics in the present study. No.
1 2 3 4 5 6 7 8 9 10
Age (years)
77 74 66 57 54 52 38 31 45 75
Sex
M M M M M F F F F F
TN stage
T2N1 T2N1 T2N1 T2N2b T3N1 T2N1 T2N1 T2N1 T2N1 T2N1
Timing of videofluoroscopic examination of swallowing Preoperative (weeks)
Postoperative (months)
2 1 1 1 1 2 2 2 2 2
3 3 3 3 6 4 3 6 4 4
Prognosis
NED NED NED NED NED NED NED NED NED NED
Abbreviation: NED, No Evidence of Disease.
examined at the Department of Oral and Maxillofacial Surgery of Kobe University Hospital, Japan, between April 2012 and December 2014. Patients met the following inclusion criteria: (i) ability to communicate and clear understanding of the treatment regimen, (ii) pre- and postoperative videofluoroscopic examination of swallowing, (iii) hemiglossectomy of the mobile tongue, unilateral neck dissection, and free radial forearm flap reconstruction, (iv) no resection of the lower jawbone during surgery and no postoperative displacement of the occlusion, (v) lip closure possible, (vi) good progress without pre- or postoperative adjuvant chemoradiotherapy, (vii) stable occlusion with natural teeth or dentures, and (viii) no pain during swallowing and stable oral ingestion. All surgeries were performed by the same surgeon. En bloc resection of the primary neck lesion included resection of the suprahyoid (i.e., digastric, geniohyoid, stylohyoid, and mylohyoid) muscles. In our department, patients with advanced oral cancer underwent preand postoperative videofluoroscopic examinations of swallowing and endoscopic evaluation of swallowing for postoperative swallowing rehabilitation. 2.2. Analysis method
rearward and upward movement, forward and upward movement, and movement distance, time, and speed during rearward and downward movement. The Wilcoxon signed-rank test was used to test for significance with the level of significance set at 5%. 3. Results 3.1. Maximum anteroposterior and vertical movement distance of the hyoid bone The mean movement distance of point C on the X-axis, equivalent to the anteroposterior movement of the hyoid bone, was 15.2 mm preoperatively and 9.0 mm postoperatively, reflecting a statistically significant decrease of 41.3%. The mean movement distance of point C on the Y-axis, equivalent to the vertical movement of the hyoid bone, was 13.6 mm preoperatively and 8.4 mm postoperatively, reflecting a statistically significant decrease of 35.9% (Table 2). Table 2 Maximum anteroposterior and vertical movement distance of the hyoid bone. Preoperative
2.2.1. Timing of videofluoroscopic examination of swallowing Preoperative testing was conducted approximately 2 weeks before surgery and postoperative testing was conducted within 3–6 months after surgery. 2.2.2. Method of videofluoroscopic examination of swallowing Videofluoroscopic examination of swallowing was performed at the Department of Otolaryngology-Head and Neck Surgery, Kobe University Hospital, Japan with the subject in the standing position. Using rice gruel containing contrast medium (barium sulfate) as the test food, a metal piece with a diameter of 23.5 mm was affixed to the center of the chin, and X-rays were applied to the cervical region from the left side. 2.2.3. Analysis method and measurement items Hyoid motion analysis was performed on the footage of the preand postoperative videofluoroscopic examination of swallowing using the DIPP-Motion PRO2D cineradiography system (DITECT, Co., Ltd., Tokyo, Japan). When measuring the hyoid position and motion, the uppermost anterior end of the 3rd cervical vertebra was set as point A, the lowest anterior end of the 5th cervical vertebra was set as point B, and the most anterior point of the hyoid bone was set as point C. The line joining points A and B were set as the Y-axis, and the line perpendicular to the Y-axis that passed through point B was set as the X-axis. The following three items were measured: (i) maximum movement distance of point C along the X- and Y-axes, (ii) area of the figure formed by the trajectory of motion of point C during swallowing, and (iii)
Postoperative
p
On the X-axis
9.0 mm 15.2 mm (7.5–19.4) (3.5–13.8) Rate of decrease: 41.3%
0.012
On the Y-axis
13.6 mm 8.4 mm (9.5–19.8) (2.5–16.3) Rate of decrease: 35.9%
0.012
3.2. Area enclosed by the trajectory of hyoid motion The figure enclosed by the motion trajectory of point C was equivalent to the range of motion (ROM) of the hyoid bone. Measurement of the area of this figure indicated a significant decrease of 46.5% from 67.1 mm2 preoperatively to 35.9 mm2 postoperatively (Table 3). 3.3. Movement distance, time, and speed for each hyoid motion In agreement with past reports, Fig. 1 shows that the hyoid bone first moved upwards and forwards and then returned to its Table 3 Area enclosed by the trajectory of hyoid motion. Preoperative ROM
Postoperative
35.9 mm2 67.1 mm2 Rate of decrease: 46.5%
p 0.012
Abbreviation: ROM, range of motion.
Please cite this article in press as: Takahashi Y, et al. Analysis of the hyoid motion of tongue cancer patients. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.007
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differences for movement distance and speed during forward and upward movement. The mean movement distance, time required, and speed during rearward and downward movement when forward movement stopped and the hyoid bone returned to its original position were 10.28 mm, 0.48 s, and 20.80 mm/s preoperatively and 6.87 mm, 0.45 s, and 15.08 mm/s postoperatively, respectively. These results show statistically significant differences for movement distance and speed during rearward and downward movement. 4. Discussion
Fig. 1. Movement of the hyoid during swallowing. The hyoid bone, which often exhibits some rearward motion at the start of swallowing (rearward and upward movement), moves slowly upwards. Then, it moves significantly upwards and forwards (forward and upward movement). Finally, it moves rearwards and downwards to return to its original position (rearward and downward movement).
original position during swallowing. More specifically, the hyoid bone, which often exhibits some rearward motion at this time (rearward and upward movement), moved slowly upwards and then moved significantly upwards and forwards (forward and upward movement). Finally, it moved rearwards and downwards to return to its original position (rearward and downward movement) [1]. On the basis of these observations, hyoid motion during swallowing can be classified into three elements: rearward and upward, forward and upward, and rearward and downward movements. The movement distance, time required, and speed were analyzed for each of these three elements (Table 4). The mean movement distance, time required, and speed during rearward and upward movement at the beginning of hyoid motion were 7.73 mm, 0.53 s, and 14.81 mm/s preoperatively and 3.93 mm, 0.38 s, and 12.60 mm/s postoperatively, respectively. These results reflected statistically significant differences for movement distance and time required during rearward and upward movement. The mean movement distance, time required, and speed during forward and upward movement when the hyoid bone suddenly moved forward were 12.53 mm, 0.35 s, and 36.73 mm/s preoperatively and 7.71 mm, 0.42 s, and 19.23 mm/s postoperatively, respectively. These results reflected statistically significant
Table 4 Movement distance, time required, and speed for each hyoid motion.
Rearward and upward Distance (mm) Time (s) Speed (mm/s) Forward and upward Distance Time Speed Rearward and downward Distance Time Speed
Preoperative
Postoperative
p
7.73 0.53 14.81
3.93 0.38 12.60
0.0499 0.0427 0.3289
12.53 0.35 36.73
7.71 0.42 19.23
0.0499 0.3548 0.0122
10.28 0.48 20.80
6.87 0.45 15.08
0.0255 0.5329 0.0178
In the treatment of oral cancer, advances in imaging and reconstruction technologies, microsurgery in particular, have enabled resection of the primary lesion within an appropriate resection range, thereby facilitating the possibility of completely curative treatment even for advanced oral cancer. However, a wider resection range results in a greater extent of postoperative functional disorders. When resecting tumors, facial skin incisions performed to ensure a sufficient surgical field and cases in which complication ablation of the skin is necessarily present significant esthetic issues postoperatively. The main oral functions are mastication, swallowing, and articulation. Thus, the oral cavity is responsible for extremely important functions to maintain life. The continued aging of society has resulted in an increase in the proportion of elderly patients with oral cancer with decreased swallowing reserve [2], necessitating the minimization of postoperative functional disorders as much as possible. Therefore, it is very important to continue research regarding postoperative functional disorders now that the curability of oral cancer has improved. Therefore, the present study focused on hyoid motion during swallowing and subjects were limited to patients with tongue cancer, who account for a large proportion of oral cancer cases. The hyoid bone is positioned between the larynx and oral cavity tissues, including the floor of the mouth, mandible, and tongue, and has no joints. It hangs down while being affixed to the surrounding geniohyoid, mylohyoid, digastric, stylohyoid, sternohyoid, thyrohyoid, omohyoid, and pharyngeal hyoid muscles. The activity of these muscles enables the performing of the subtle motions involved in mastication, swallowing, and speech [1]. 4.1. Patients Analysis of hyoid motion in patients with oral cancer has been conducted at various facilities. A limited number of studies have analyzed hyoid motion following neck dissection for delayedonset cervical lymph node metastasis after surgery for oral cancer [3]. However, the primary lesion sites and methods of resection and reconstruction were not unified, and most reports conducted comparative investigations involving healthy subjects without dysphagia rather than the evaluation of individual patients before and after surgery [4]. In the present study, all cases of advanced tongue cancer underwent surgical treatment using the “pull-through” method, whereby unilateral neck dissection was performed before pulling out the primary lesion to the submandibular region and resecting it en bloc with the neck dissection tissue. Using this surgical technique, suprahyoid muscles such as the digastric and mylohyoid muscles were also resected. In addition, to reduce measurement errors, we decided to measure cases that were resected using the same surgical procedure. Reconstruction was performed using a free radial forearm flap in all patients. Furthermore, we investigated to what extent hemiglossectomy of the mobile tongue and resection of the unilateral suprahyoid and omohyoid muscles affected swallowing dynamics.
Please cite this article in press as: Takahashi Y, et al. Analysis of the hyoid motion of tongue cancer patients. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.007
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Reconstructive surgery with free radial forearm flaps for cases that underwent hemiglossectomy of the mobile tongue was performed at the Department of Plastic Surgery of Kobe University Hospital. We believed that this was the optimal choice for reconstruction as previous reports have demonstrated that free flaps are more effective than pedicle flaps at maintaining swallowing function [5]. Furthermore, patients who undergo adjuvant chemotherapy or radiotherapy in particular may exhibit muscular fibrosis and atrophy in addition to xerostomia. In our department, we work in cooperation with the Department of Radiation Oncology and Medical Oncology, and recommend postoperative radiation therapy in the following cases: (i) Cancer in the surgical margins of the primary lesion. (ii) Extranodal invasion in the metastatic lymph node. (iii) Multiple metastases to the cervical lymph node (more than four). We also consider the degree of malignancy in the tissue. In the postoperative evaluations, six patients did not have metastatic lymph nodes, and four patients had less than two metastatic lymph nodes. Based on these characteristics, the patients were not judged to be in need of adaptive radiation therapy, but we performed a strict follow-up of these patients. Furthermore, we measured hyoid bone movement during swallowing. Tissue contracture is a known side effect of radiation therapy, so such a thing was excluded in this study to avoid this confounding effect. We decided that cases that required resection of the mandible should be excluded from this study because they were more likely to develop postoperative changes in jaw position and trismus. It has been reported that increased age results in prolonged forward–rearward and vertical movement times of the hyoid bone and lowers the highest point of upward movement [2]. Other reports have indicated that although the hyoid bone rest position is lower in males than in females, there was no difference in the highest point of upward movement between males and females. It was reported that the movement distance in the vertical direction is greater in males [2]. The mean age of the subjects in the present study was 56.9 years (range, 31–77 years), and the male to female ratio was 1:1. To reduce the effects of age and gender on the results, we conducted videofluoroscopic examination of swallowing of the same patients pre- and postoperatively rather than comparing them with healthy individuals. 4.2. Imaging, reference points, and analytical methods A reference line is required to analyze the forward–rearward and vertical motions of the hyoid bone. Several reports have used the 3rd and 5th cervical vertebrae as reference points [1,3,4,6] because the hyoid bone is located between the 3rd and 5th cervical vertebrae at rest and the highest point of upward movement during swallowing is near the top of the 3rd cervical vertebra. This point is advantageous as a reference because there is no hard tissue around the cervical vertebrae, making it easy to follow the point on moving images. A few reports have used the Camper’s plane as a reference [7,8], making it necessary to follow the subnasal point and inferior border of the tragus, of which the Camper’s plane is composed, on moving images. However, overlapping with surrounding hard tissue can make the images unclear, therefore the cervical vertebrae were used as reference points in the present study. If the head is fixed during testing, measurement errors caused by bending of the cervical vertebrae can be avoided. However, because we aimed to capture images during swallowing under the most natural conditions as possible, as was the case with previous studies, we did not fixate the head during testing [2,7]. Good reproducibility was previously reported after test foods were prescribed to the same patient and repeatedly swallowed three times [9]; therefore, subjects swallowed three times in our study, and we used the mean
values for analysis. Ramsey et al. [10] reported that 30 frames/s is appropriate for observation of the hyoid bone and larynx; therefore, the moving imaging speed was fixed at 30 frames/s in the present study.
4.3. Hyoid motion changes Forward–rearward and vertical direction movement distances of the hyoid bone markedly decreased postoperatively in the present study. Comparison of the rates of decrease in forward–rearward and vertical hyoid movement distances indicated that the rate of decrease was significantly greater in the forward–rearward direction, which was consistent with previous reports that demonstrated a decreased amount of upward and forward movement of the hyoid bone in patients with head and neck cancers [11–13]. A report involving hyoid motion analysis in patients with oral cancer who developed late-onset cervical lymph node metastasis after resection of the primary lesion and underwent secondary neck dissection indicated that the degree of upward movement of the hyoid bone did not change despite unilateral resection of the digastric and omohyoid muscles [3]. Previous reports state that among the suprahyoid muscles, resection of the geniohyoid muscle decreases the upward movement of the hyoid bone the most [14] and that the muscles that strongly elevate the hyoid bone during swallowing are the mylohyoid and geniohyoid muscles [1]. Therefore, it appears that the maximum amount of hyoid bone movement decreases in both the forward–rearward and vertical directions and that the rate of decrease is greater in the forward–rearward direction. This may be strongly affected by resection of the suprahyoid muscles, including the mylohyoid and geniohyoid muscles, which work to strongly move the hyoid bone forwards, when the primary lesion is pulled out from the cervical region through the mandible as mentioned above. To examine the area of the shape created by the trajectory of hyoid motion during swallowing in this study, the DIPP-Motion PRO2D cineradiography system was used to extract hyoid bone coordinates within moving images, and corrections were performed such that the post-calculation area had the same size as the actual area. Because all suprahyoid muscles were resected on the affected side, upward and forward movements of the hyoid bone relied upon the movement of muscles on the healthy side. Therefore, a significant decrease was observed in the area postoperatively compared with that observed preoperatively. In addition, because measurements can be performed regardless of where the reference line for analyzing the figures has been set, we hope to determine whether these figures can be used as indices for ROM of the hyoid bone during swallowing in the future. Finally, hyoid movement distance, time required, and speed in three directions during swallowing were analyzed, which revealed statistically significant differences in the movement distance and time required in the rearward and upward directions. Immediately after starting the swallow reflex, the tongue and soft palate voluntarily move to send the food bolus into the pharynx [15,16]. At this time, the hyoid bone moves rearward and upward mainly through the actions of the stylohyoid muscle and the posterior belly of the digastric muscle. Previous analyses of hyoid motion after neck dissection indicated that the extent of upward hyoid bone movement was not affected by unilateral resection of the digastric or omohyoid muscle [3]. All patients in the present study underwent resection of the stylohyoid muscle and posterior body of the digastric muscle. However, significant weakening of rearward elevation strength and reduction of movement distance resulted in the relative decrease of time required, which may explain why there was barely any change in speed.
Please cite this article in press as: Takahashi Y, et al. Analysis of the hyoid motion of tongue cancer patients. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.007
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Statistically significant differences were noted for movement distance and speed during forward and upward movements, which rapidly act to move the hyoid bone forward. As mentioned above, the mylohyoid and geniohyoid muscles, which act to strongly elevate the hyoid bone during swallowing, were resected, possibly resulting in a shortened movement distance and decreased movement speed postoperatively. We assumed that the time required was not greatly affected because this motion occurred as a reflex movement [15,16]. Statistically significant differences were observed with regard to movement distance and speed in rearward and downward movements. After forward movement, the movement that returns the hyoid bone to its rest position is reported to be mainly performed by disuse of the suprahyoid muscles and elasticity of the soft tissue rather than activity of the infrahyoid muscles [14,17]. This means that the rearward and downward movements occur after the forward and upward movements and that the shortened postoperative distance in this forward and upward movement resulted in a shorter return distance to the rest position. It is likely that the time required did not change, and the movement speed was slower because the hyoid bone did not return to its rest position by muscle activity. 5. Conclusions Hemiglossectomy of the mobile tongue, unilateral neck dissection, and free radial forearm flap reconstruction are typical surgical procedures for treating advanced tongue cancer. In the present study, we analyzed hyoid motion in patients who underwent these procedures. The results indicated that this regimen resulted in motor impairment of the hyoid bone with decreased movement capacity and ROM of the hyoid bone during swallowing. No clear dysphagia occurred in response to hyoid bone motor impairment caused by the surgical procedures investigated in this study. However, this hyoid motion analysis may be used to maintain the quality of life of oral cancer patients in the future as it could also be used to assess patients after bilateral neck dissection, mandibular resection, and radiotherapy. Human rights statements and informed consent Not applicable. Animal rights statements Not applicable.
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Conflict of interest statements None. Acknowledgments The authors would like to extend their deepest gratitude to Professors Kenichi Nibu, Miki Saito, Hirokazu Komatsu, and Hitomi Shinomiya of the Department of Otolaryngology-Head and Neck Surgery, Kobe University Hospital, for their cooperation in this research and its presentation. References [1] Nakahara M. A cinefluorographic study of hyoid and laryngeal movements during deglutition. Nippon Jibiinkoka Gakkai Kaiho 1987;90:669–79. [2] Kaneko I. A cinefluorographic study of hyoid bone movement during deglutition. Nippon Jibiinkoka Gakkai Kaiho 1992;95:974–87. [3] Matsunaga K, Oobu K, Kamiishi H. The clinical study on pre and postoperative swallowing function inunilateral radical neck dissection cases – the effect of radical neck dissection and postoperative radiation. J Jpn Soc Stomatognath Funct 2003;10:53–9. [4] Fujimoto Y, Hasegawa Y, Matsuura H, Nakayama B. A quantitative study of videofluorography using a personal computer analysis of postoperative dysphagia of oral and oropharyngeal cancer patients. Jpn J Head Neck Cancer 1996;22:72–7. [5] Nigauri T, Kamata S, Kawabata K. Postoperative function of the oropharyngeal cancer patients – lateral wall and soft palate reconstruction. J Jpn Soc Head Neck Surg 1997;7:113–6. [6] Fujiwara K, Kawamoto K, Nakayama B. Swallowing analysis using DIPP-Motion Pro 2D. Pract Otorhinolaryngol 2010;103:1057–61. [7] Ueda N, Nohara K, Kotani Y, Tanaka N, Okuno K, Sakai T. Effects of the bolus volume on hyoid movements in normal individuals. J Oral Rehabil 2013;40:491–9. [8] Nakane A, Tohara H, Ouchi Y, Goto S, Uematsu H. Videofluoroscopic kinesiologic analysis of swallowing: defining a standard plane. J Med Dent Sci 2006;53:7–15. [9] Yokoyama M, Michiwaki Y, Takahashi K. Analysis of swallowing function using videofluorographic images basic study for the time analysis. J Jpn Stomatol Soc 2000;49:16–24. [10] Ramsey GH, Watson JS, Gramiak R, Weinberg SA. Cinefluorographic analysis of the mechanism of swallowing. Radiology 1955;64:498–518. [11] Zu Y, Yang Z, Perlman AL. Hyoid displacement in post-treatment cancer patients: preliminary findings. J Speech Lang Hear Res 2011;54:813–20. [12] Kendall KA, McKenzie SW, Leonard RJ, Jones C. Structural mobility in deglutition after single modality treatment of head and neck carcinomas with radiotherapy. Head Neck 1998;20:720–5. [13] Magara J, Hayashi H, Kanda C, Hori K, Taniguchi H, Ono K, et al. Spatial and temporal relationship between swallow-related hyoid movement and bolus propulsion during swallowing. J Jpn Soc Stomatognath Funct 2015;20:22–32. [14] Shin T. Closure of the larynx during the swallowing. J Jpn Bronchoesophagol Soc 1975;26:131–42. [15] Hirano M. Pharyngeal stage of swallowing: its physiology and pathologies. Jpn Bronchoesophagol Soc 1980;31:1–9. [16] Yoshida T. Electromyographic and X-ray investigations of normal deglutition. Jibi To Rinsho 1979;25:824–72. [17] Saigusa H. Anatomy of the suprahyoid muscles. Otorhinolaryngology 2010;53:246–53.
Please cite this article in press as: Takahashi Y, et al. Analysis of the hyoid motion of tongue cancer patients. J Oral Maxillofac Surg Med Pathol (2016), http://dx.doi.org/10.1016/j.ajoms.2016.09.007
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Original Research
Analysis of the hyoid motion of tongue cancer patients Yusuke Takahashi a,∗ , Tsutomu Minamikawa a , Natsuki Yonezawa a , Hirokazu Komatsu b , Kenichi Nibu b , Takahide Komori a a
Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-Cho, Chuo-Ku, Kobe 650-0017, Japan Department of Otolaryngology-Head and Neck Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-Cho, Chuo-Ku, Kobe 650-0017, Japan b
a r t i c l e
i n f o
Article history: Received 30 May 2016 Received in revised form 3 September 2016 Accepted 15 September 2016 Available online xxx Keywords: Tongue cancer Hyoid motion Videofluoroscopic examination of swallowing
a b s t r a c t Objective: We aimed to analyze movement of the hyoid bone in patients with tongue cancer following radical surgery without pre- or postoperative chemotherapy or radiotherapy. Methods: Ten patients (five males, five females; average age, 56.9 years) with histologically confirmed tongue squamous cell carcinoma underwent pre- and postoperative videofluoroscopic examination of swallowing and radical surgery at the Department of Oral and Maxillofacial Surgery of Kobe University Hospital, Japan. All patients underwent modified radical neck dissection and hemiglossectomy of the mobile tongue with reconstruction using a free radial forearm flap. Hyoid motion was analyzed using the DIPP-Motion PRO2D cineradiography system. According to previous reports, hyoid motion during swallowing is divided into three elements: rearward and upward, forward and upward, and rearward and downward movements. These movements were compared pre- and postoperatively. The endpoints were movement speed, distance, and time. Results: Postoperatively, radical surgery resulted in motor impairment of the hyoid, with decreased movement capacity, including decreased movement distance, time required, speed, and range of motion during swallowing. Conclusions: Hyoid motion analysis could be useful to maintain the quality of life of patients with oral cancer in the future as it could also be used to assess patients after bilateral neck dissection, mandibular resection, and radiotherapy. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction Oral cancer accounts for 1–5% of all malignant tumors. Epidemiologically, tongue cancer accounts for a high proportion of oral cancer cases, similar to gingival cancer. Advanced tongue cancer is likely to metastasize to the cervical lymph nodes, necessitating neck dissection with excision of the primary lesion in several cases that require immediate reconstruction according to the extent of tongue resection. However, when reconstructing the tongue, it is impossible to avoid postoperative impairment of oral functions in the form of mastication, swallowing, and articulation. Various reports regarding functional evaluation after surgery for oral cancer have focused on dysphagia. There are various
夽 Asian AOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author. Fax: +81 078 382 6229. E-mail address: crystal shooting [email protected] (Y. Takahashi).
methods to evaluate dysphagia, including tongue pressure, swallowing pressure, videofluoroscopic examination of swallowing, and endoscopic evaluation of swallowing. Here we focused on postoperative hyoid motion, which can be evaluated objectively. When swallowing, the hyoid bone exhibits upwards and rearwards motion caused by the movement of the suprahyoid muscles and substantially moves forward. Previous reports have clarified that after a bolus passes through the pharynx, the hyoid bone moves rearwards and returns to its original position. En bloc resection of the primary cervical lesion in advanced tongue cancer requires resection of the suprahyoid muscles. Therefore, we aimed to determine how resection of the suprahyoid muscles on one side disrupts the horizontal balance of the hyoid bone and changes movement speed, range, and distance during swallowing. 2. Material and methods 2.1. Patients Patient characteristics are presented in Table 1. The study cohort included ten patients with primary tongue cancer who were
http://dx.doi.org/10.1016/j.ajoms.2016.09.007 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
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Table 1 Patient characteristics in the present study. No.
1 2 3 4 5 6 7 8 9 10
Age (years)
77 74 66 57 54 52 38 31 45 75
Sex
M M M M M F F F F F
TN stage
T2N1 T2N1 T2N1 T2N2b T3N1 T2N1 T2N1 T2N1 T2N1 T2N1
Timing of videofluoroscopic examination of swallowing Preoperative (weeks)
Postoperative (months)
2 1 1 1 1 2 2 2 2 2
3 3 3 3 6 4 3 6 4 4
Prognosis
NED NED NED NED NED NED NED NED NED NED
Abbreviation: NED, No Evidence of Disease.
examined at the Department of Oral and Maxillofacial Surgery of Kobe University Hospital, Japan, between April 2012 and December 2014. Patients met the following inclusion criteria: (i) ability to communicate and clear understanding of the treatment regimen, (ii) pre- and postoperative videofluoroscopic examination of swallowing, (iii) hemiglossectomy of the mobile tongue, unilateral neck dissection, and free radial forearm flap reconstruction, (iv) no resection of the lower jawbone during surgery and no postoperative displacement of the occlusion, (v) lip closure possible, (vi) good progress without pre- or postoperative adjuvant chemoradiotherapy, (vii) stable occlusion with natural teeth or dentures, and (viii) no pain during swallowing and stable oral ingestion. All surgeries were performed by the same surgeon. En bloc resection of the primary neck lesion included resection of the suprahyoid (i.e., digastric, geniohyoid, stylohyoid, and mylohyoid) muscles. In our department, patients with advanced oral cancer underwent preand postoperative videofluoroscopic examinations of swallowing and endoscopic evaluation of swallowing for postoperative swallowing rehabilitation. 2.2. Analysis method
rearward and upward movement, forward and upward movement, and movement distance, time, and speed during rearward and downward movement. The Wilcoxon signed-rank test was used to test for significance with the level of significance set at 5%. 3. Results 3.1. Maximum anteroposterior and vertical movement distance of the hyoid bone The mean movement distance of point C on the X-axis, equivalent to the anteroposterior movement of the hyoid bone, was 15.2 mm preoperatively and 9.0 mm postoperatively, reflecting a statistically significant decrease of 41.3%. The mean movement distance of point C on the Y-axis, equivalent to the vertical movement of the hyoid bone, was 13.6 mm preoperatively and 8.4 mm postoperatively, reflecting a statistically significant decrease of 35.9% (Table 2). Table 2 Maximum anteroposterior and vertical movement distance of the hyoid bone. Preoperative
2.2.1. Timing of videofluoroscopic examination of swallowing Preoperative testing was conducted approximately 2 weeks before surgery and postoperative testing was conducted within 3–6 months after surgery. 2.2.2. Method of videofluoroscopic examination of swallowing Videofluoroscopic examination of swallowing was performed at the Department of Otolaryngology-Head and Neck Surgery, Kobe University Hospital, Japan with the subject in the standing position. Using rice gruel containing contrast medium (barium sulfate) as the test food, a metal piece with a diameter of 23.5 mm was affixed to the center of the chin, and X-rays were applied to the cervical region from the left side. 2.2.3. Analysis method and measurement items Hyoid motion analysis was performed on the footage of the preand postoperative videofluoroscopic examination of swallowing using the DIPP-Motion PRO2D cineradiography system (DITECT, Co., Ltd., Tokyo, Japan). When measuring the hyoid position and motion, the uppermost anterior end of the 3rd cervical vertebra was set as point A, the lowest anterior end of the 5th cervical vertebra was set as point B, and the most anterior point of the hyoid bone was set as point C. The line joining points A and B were set as the Y-axis, and the line perpendicular to the Y-axis that passed through point B was set as the X-axis. The following three items were measured: (i) maximum movement distance of point C along the X- and Y-axes, (ii) area of the figure formed by the trajectory of motion of point C during swallowing, and (iii)
Postoperative
p
On the X-axis
9.0 mm 15.2 mm (7.5–19.4) (3.5–13.8) Rate of decrease: 41.3%
0.012
On the Y-axis
13.6 mm 8.4 mm (9.5–19.8) (2.5–16.3) Rate of decrease: 35.9%
0.012
3.2. Area enclosed by the trajectory of hyoid motion The figure enclosed by the motion trajectory of point C was equivalent to the range of motion (ROM) of the hyoid bone. Measurement of the area of this figure indicated a significant decrease of 46.5% from 67.1 mm2 preoperatively to 35.9 mm2 postoperatively (Table 3). 3.3. Movement distance, time, and speed for each hyoid motion In agreement with past reports, Fig. 1 shows that the hyoid bone first moved upwards and forwards and then returned to its Table 3 Area enclosed by the trajectory of hyoid motion. Preoperative ROM
Postoperative
35.9 mm2 67.1 mm2 Rate of decrease: 46.5%
p 0.012
Abbreviation: ROM, range of motion.
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differences for movement distance and speed during forward and upward movement. The mean movement distance, time required, and speed during rearward and downward movement when forward movement stopped and the hyoid bone returned to its original position were 10.28 mm, 0.48 s, and 20.80 mm/s preoperatively and 6.87 mm, 0.45 s, and 15.08 mm/s postoperatively, respectively. These results show statistically significant differences for movement distance and speed during rearward and downward movement. 4. Discussion
Fig. 1. Movement of the hyoid during swallowing. The hyoid bone, which often exhibits some rearward motion at the start of swallowing (rearward and upward movement), moves slowly upwards. Then, it moves significantly upwards and forwards (forward and upward movement). Finally, it moves rearwards and downwards to return to its original position (rearward and downward movement).
original position during swallowing. More specifically, the hyoid bone, which often exhibits some rearward motion at this time (rearward and upward movement), moved slowly upwards and then moved significantly upwards and forwards (forward and upward movement). Finally, it moved rearwards and downwards to return to its original position (rearward and downward movement) [1]. On the basis of these observations, hyoid motion during swallowing can be classified into three elements: rearward and upward, forward and upward, and rearward and downward movements. The movement distance, time required, and speed were analyzed for each of these three elements (Table 4). The mean movement distance, time required, and speed during rearward and upward movement at the beginning of hyoid motion were 7.73 mm, 0.53 s, and 14.81 mm/s preoperatively and 3.93 mm, 0.38 s, and 12.60 mm/s postoperatively, respectively. These results reflected statistically significant differences for movement distance and time required during rearward and upward movement. The mean movement distance, time required, and speed during forward and upward movement when the hyoid bone suddenly moved forward were 12.53 mm, 0.35 s, and 36.73 mm/s preoperatively and 7.71 mm, 0.42 s, and 19.23 mm/s postoperatively, respectively. These results reflected statistically significant
Table 4 Movement distance, time required, and speed for each hyoid motion.
Rearward and upward Distance (mm) Time (s) Speed (mm/s) Forward and upward Distance Time Speed Rearward and downward Distance Time Speed
Preoperative
Postoperative
p
7.73 0.53 14.81
3.93 0.38 12.60
0.0499 0.0427 0.3289
12.53 0.35 36.73
7.71 0.42 19.23
0.0499 0.3548 0.0122
10.28 0.48 20.80
6.87 0.45 15.08
0.0255 0.5329 0.0178
In the treatment of oral cancer, advances in imaging and reconstruction technologies, microsurgery in particular, have enabled resection of the primary lesion within an appropriate resection range, thereby facilitating the possibility of completely curative treatment even for advanced oral cancer. However, a wider resection range results in a greater extent of postoperative functional disorders. When resecting tumors, facial skin incisions performed to ensure a sufficient surgical field and cases in which complication ablation of the skin is necessarily present significant esthetic issues postoperatively. The main oral functions are mastication, swallowing, and articulation. Thus, the oral cavity is responsible for extremely important functions to maintain life. The continued aging of society has resulted in an increase in the proportion of elderly patients with oral cancer with decreased swallowing reserve [2], necessitating the minimization of postoperative functional disorders as much as possible. Therefore, it is very important to continue research regarding postoperative functional disorders now that the curability of oral cancer has improved. Therefore, the present study focused on hyoid motion during swallowing and subjects were limited to patients with tongue cancer, who account for a large proportion of oral cancer cases. The hyoid bone is positioned between the larynx and oral cavity tissues, including the floor of the mouth, mandible, and tongue, and has no joints. It hangs down while being affixed to the surrounding geniohyoid, mylohyoid, digastric, stylohyoid, sternohyoid, thyrohyoid, omohyoid, and pharyngeal hyoid muscles. The activity of these muscles enables the performing of the subtle motions involved in mastication, swallowing, and speech [1]. 4.1. Patients Analysis of hyoid motion in patients with oral cancer has been conducted at various facilities. A limited number of studies have analyzed hyoid motion following neck dissection for delayedonset cervical lymph node metastasis after surgery for oral cancer [3]. However, the primary lesion sites and methods of resection and reconstruction were not unified, and most reports conducted comparative investigations involving healthy subjects without dysphagia rather than the evaluation of individual patients before and after surgery [4]. In the present study, all cases of advanced tongue cancer underwent surgical treatment using the “pull-through” method, whereby unilateral neck dissection was performed before pulling out the primary lesion to the submandibular region and resecting it en bloc with the neck dissection tissue. Using this surgical technique, suprahyoid muscles such as the digastric and mylohyoid muscles were also resected. In addition, to reduce measurement errors, we decided to measure cases that were resected using the same surgical procedure. Reconstruction was performed using a free radial forearm flap in all patients. Furthermore, we investigated to what extent hemiglossectomy of the mobile tongue and resection of the unilateral suprahyoid and omohyoid muscles affected swallowing dynamics.
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Reconstructive surgery with free radial forearm flaps for cases that underwent hemiglossectomy of the mobile tongue was performed at the Department of Plastic Surgery of Kobe University Hospital. We believed that this was the optimal choice for reconstruction as previous reports have demonstrated that free flaps are more effective than pedicle flaps at maintaining swallowing function [5]. Furthermore, patients who undergo adjuvant chemotherapy or radiotherapy in particular may exhibit muscular fibrosis and atrophy in addition to xerostomia. In our department, we work in cooperation with the Department of Radiation Oncology and Medical Oncology, and recommend postoperative radiation therapy in the following cases: (i) Cancer in the surgical margins of the primary lesion. (ii) Extranodal invasion in the metastatic lymph node. (iii) Multiple metastases to the cervical lymph node (more than four). We also consider the degree of malignancy in the tissue. In the postoperative evaluations, six patients did not have metastatic lymph nodes, and four patients had less than two metastatic lymph nodes. Based on these characteristics, the patients were not judged to be in need of adaptive radiation therapy, but we performed a strict follow-up of these patients. Furthermore, we measured hyoid bone movement during swallowing. Tissue contracture is a known side effect of radiation therapy, so such a thing was excluded in this study to avoid this confounding effect. We decided that cases that required resection of the mandible should be excluded from this study because they were more likely to develop postoperative changes in jaw position and trismus. It has been reported that increased age results in prolonged forward–rearward and vertical movement times of the hyoid bone and lowers the highest point of upward movement [2]. Other reports have indicated that although the hyoid bone rest position is lower in males than in females, there was no difference in the highest point of upward movement between males and females. It was reported that the movement distance in the vertical direction is greater in males [2]. The mean age of the subjects in the present study was 56.9 years (range, 31–77 years), and the male to female ratio was 1:1. To reduce the effects of age and gender on the results, we conducted videofluoroscopic examination of swallowing of the same patients pre- and postoperatively rather than comparing them with healthy individuals. 4.2. Imaging, reference points, and analytical methods A reference line is required to analyze the forward–rearward and vertical motions of the hyoid bone. Several reports have used the 3rd and 5th cervical vertebrae as reference points [1,3,4,6] because the hyoid bone is located between the 3rd and 5th cervical vertebrae at rest and the highest point of upward movement during swallowing is near the top of the 3rd cervical vertebra. This point is advantageous as a reference because there is no hard tissue around the cervical vertebrae, making it easy to follow the point on moving images. A few reports have used the Camper’s plane as a reference [7,8], making it necessary to follow the subnasal point and inferior border of the tragus, of which the Camper’s plane is composed, on moving images. However, overlapping with surrounding hard tissue can make the images unclear, therefore the cervical vertebrae were used as reference points in the present study. If the head is fixed during testing, measurement errors caused by bending of the cervical vertebrae can be avoided. However, because we aimed to capture images during swallowing under the most natural conditions as possible, as was the case with previous studies, we did not fixate the head during testing [2,7]. Good reproducibility was previously reported after test foods were prescribed to the same patient and repeatedly swallowed three times [9]; therefore, subjects swallowed three times in our study, and we used the mean
values for analysis. Ramsey et al. [10] reported that 30 frames/s is appropriate for observation of the hyoid bone and larynx; therefore, the moving imaging speed was fixed at 30 frames/s in the present study.
4.3. Hyoid motion changes Forward–rearward and vertical direction movement distances of the hyoid bone markedly decreased postoperatively in the present study. Comparison of the rates of decrease in forward–rearward and vertical hyoid movement distances indicated that the rate of decrease was significantly greater in the forward–rearward direction, which was consistent with previous reports that demonstrated a decreased amount of upward and forward movement of the hyoid bone in patients with head and neck cancers [11–13]. A report involving hyoid motion analysis in patients with oral cancer who developed late-onset cervical lymph node metastasis after resection of the primary lesion and underwent secondary neck dissection indicated that the degree of upward movement of the hyoid bone did not change despite unilateral resection of the digastric and omohyoid muscles [3]. Previous reports state that among the suprahyoid muscles, resection of the geniohyoid muscle decreases the upward movement of the hyoid bone the most [14] and that the muscles that strongly elevate the hyoid bone during swallowing are the mylohyoid and geniohyoid muscles [1]. Therefore, it appears that the maximum amount of hyoid bone movement decreases in both the forward–rearward and vertical directions and that the rate of decrease is greater in the forward–rearward direction. This may be strongly affected by resection of the suprahyoid muscles, including the mylohyoid and geniohyoid muscles, which work to strongly move the hyoid bone forwards, when the primary lesion is pulled out from the cervical region through the mandible as mentioned above. To examine the area of the shape created by the trajectory of hyoid motion during swallowing in this study, the DIPP-Motion PRO2D cineradiography system was used to extract hyoid bone coordinates within moving images, and corrections were performed such that the post-calculation area had the same size as the actual area. Because all suprahyoid muscles were resected on the affected side, upward and forward movements of the hyoid bone relied upon the movement of muscles on the healthy side. Therefore, a significant decrease was observed in the area postoperatively compared with that observed preoperatively. In addition, because measurements can be performed regardless of where the reference line for analyzing the figures has been set, we hope to determine whether these figures can be used as indices for ROM of the hyoid bone during swallowing in the future. Finally, hyoid movement distance, time required, and speed in three directions during swallowing were analyzed, which revealed statistically significant differences in the movement distance and time required in the rearward and upward directions. Immediately after starting the swallow reflex, the tongue and soft palate voluntarily move to send the food bolus into the pharynx [15,16]. At this time, the hyoid bone moves rearward and upward mainly through the actions of the stylohyoid muscle and the posterior belly of the digastric muscle. Previous analyses of hyoid motion after neck dissection indicated that the extent of upward hyoid bone movement was not affected by unilateral resection of the digastric or omohyoid muscle [3]. All patients in the present study underwent resection of the stylohyoid muscle and posterior body of the digastric muscle. However, significant weakening of rearward elevation strength and reduction of movement distance resulted in the relative decrease of time required, which may explain why there was barely any change in speed.
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Statistically significant differences were noted for movement distance and speed during forward and upward movements, which rapidly act to move the hyoid bone forward. As mentioned above, the mylohyoid and geniohyoid muscles, which act to strongly elevate the hyoid bone during swallowing, were resected, possibly resulting in a shortened movement distance and decreased movement speed postoperatively. We assumed that the time required was not greatly affected because this motion occurred as a reflex movement [15,16]. Statistically significant differences were observed with regard to movement distance and speed in rearward and downward movements. After forward movement, the movement that returns the hyoid bone to its rest position is reported to be mainly performed by disuse of the suprahyoid muscles and elasticity of the soft tissue rather than activity of the infrahyoid muscles [14,17]. This means that the rearward and downward movements occur after the forward and upward movements and that the shortened postoperative distance in this forward and upward movement resulted in a shorter return distance to the rest position. It is likely that the time required did not change, and the movement speed was slower because the hyoid bone did not return to its rest position by muscle activity. 5. Conclusions Hemiglossectomy of the mobile tongue, unilateral neck dissection, and free radial forearm flap reconstruction are typical surgical procedures for treating advanced tongue cancer. In the present study, we analyzed hyoid motion in patients who underwent these procedures. The results indicated that this regimen resulted in motor impairment of the hyoid bone with decreased movement capacity and ROM of the hyoid bone during swallowing. No clear dysphagia occurred in response to hyoid bone motor impairment caused by the surgical procedures investigated in this study. However, this hyoid motion analysis may be used to maintain the quality of life of oral cancer patients in the future as it could also be used to assess patients after bilateral neck dissection, mandibular resection, and radiotherapy. Human rights statements and informed consent Not applicable. Animal rights statements Not applicable.
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Conflict of interest statements None. Acknowledgments The authors would like to extend their deepest gratitude to Professors Kenichi Nibu, Miki Saito, Hirokazu Komatsu, and Hitomi Shinomiya of the Department of Otolaryngology-Head and Neck Surgery, Kobe University Hospital, for their cooperation in this research and its presentation. References [1] Nakahara M. A cinefluorographic study of hyoid and laryngeal movements during deglutition. Nippon Jibiinkoka Gakkai Kaiho 1987;90:669–79. [2] Kaneko I. A cinefluorographic study of hyoid bone movement during deglutition. Nippon Jibiinkoka Gakkai Kaiho 1992;95:974–87. [3] Matsunaga K, Oobu K, Kamiishi H. The clinical study on pre and postoperative swallowing function inunilateral radical neck dissection cases – the effect of radical neck dissection and postoperative radiation. J Jpn Soc Stomatognath Funct 2003;10:53–9. [4] Fujimoto Y, Hasegawa Y, Matsuura H, Nakayama B. A quantitative study of videofluorography using a personal computer analysis of postoperative dysphagia of oral and oropharyngeal cancer patients. Jpn J Head Neck Cancer 1996;22:72–7. [5] Nigauri T, Kamata S, Kawabata K. Postoperative function of the oropharyngeal cancer patients – lateral wall and soft palate reconstruction. J Jpn Soc Head Neck Surg 1997;7:113–6. [6] Fujiwara K, Kawamoto K, Nakayama B. Swallowing analysis using DIPP-Motion Pro 2D. Pract Otorhinolaryngol 2010;103:1057–61. [7] Ueda N, Nohara K, Kotani Y, Tanaka N, Okuno K, Sakai T. Effects of the bolus volume on hyoid movements in normal individuals. J Oral Rehabil 2013;40:491–9. [8] Nakane A, Tohara H, Ouchi Y, Goto S, Uematsu H. Videofluoroscopic kinesiologic analysis of swallowing: defining a standard plane. J Med Dent Sci 2006;53:7–15. [9] Yokoyama M, Michiwaki Y, Takahashi K. Analysis of swallowing function using videofluorographic images basic study for the time analysis. J Jpn Stomatol Soc 2000;49:16–24. [10] Ramsey GH, Watson JS, Gramiak R, Weinberg SA. Cinefluorographic analysis of the mechanism of swallowing. Radiology 1955;64:498–518. [11] Zu Y, Yang Z, Perlman AL. Hyoid displacement in post-treatment cancer patients: preliminary findings. J Speech Lang Hear Res 2011;54:813–20. [12] Kendall KA, McKenzie SW, Leonard RJ, Jones C. Structural mobility in deglutition after single modality treatment of head and neck carcinomas with radiotherapy. Head Neck 1998;20:720–5. [13] Magara J, Hayashi H, Kanda C, Hori K, Taniguchi H, Ono K, et al. Spatial and temporal relationship between swallow-related hyoid movement and bolus propulsion during swallowing. J Jpn Soc Stomatognath Funct 2015;20:22–32. [14] Shin T. Closure of the larynx during the swallowing. J Jpn Bronchoesophagol Soc 1975;26:131–42. [15] Hirano M. Pharyngeal stage of swallowing: its physiology and pathologies. Jpn Bronchoesophagol Soc 1980;31:1–9. [16] Yoshida T. Electromyographic and X-ray investigations of normal deglutition. Jibi To Rinsho 1979;25:824–72. [17] Saigusa H. Anatomy of the suprahyoid muscles. Otorhinolaryngology 2010;53:246–53.
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