Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study

YIJOM-4257; No of Pages 10

Int. J. Oral Maxillofac. Surg. 2019; xxx: xxx–xxx https://doi.org/10.1016/j.ijom.2019.08.001, available online at https://www.sciencedirect.com

Research Paper Craniofacial Anomalies

Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study

T. Joujima1, M. Oda1, M. Sasaguri2, M. Habu2, S. Kataoka3, Y. Miyamura1, N. Wakasugi-Sato1, S. Matsumoto-Takeda1, O. Takahashi2, S. Kokuryo4, T. Sago5, D. Yoshiga4, T. Tanaka1, Y. Morimoto1 1

Division of Oral and Maxillofacial Radiology, Kyushu Dental University, Kitakyushu, Japan; 2 Division of Maxillofacial Surgery, Kyushu Dental University, Kitakyushu, Japan; 3 Division of Anatomy, Kyushu Dental University, Kitakyushu, Japan; 4Division of Oral Medicine, Kyushu Dental University, Kitakyushu, Japan; 5Division of Dental Anaesthesiology, Kyushu Dental University, Kitakyushu, Japan

T. Joujima, M. Oda, M. Sasaguri, M. Habu, S. Kataoka, Y. Miyamura, N. WakasugiSato, S. Matsumoto-Takeda, O. Takahashi, S. Kokuryo, T. Sago, D. Yoshiga, T. Tanaka, Y. Morimoto: Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study. Int. J. Oral Maxillofac. Surg. 2019; xxx: xxx–xxx. ã 2019 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Abstract. The objective was to introduce a new technique for visualizing the threedimensional (3D) movements of velopharyngeal-related muscles using high-speed cine-magnetic resonance imaging (MRI) based on T2-weighted sequences. The evaluation of phonation- and water swallowing-related events was performed in 11 healthy subjects. Specifically, whether cine-MRI could precisely visualize normal velopharyngeal function during these two events was examined. The 3D movements of the soft palate, superior pharyngeal constrictor muscles, and levator veli palatini muscles were visualized in all 11 subjects. A noteworthy finding was that the magnetic resonance signals of the superior constrictor pharyngeal muscles and the levator veli palatini muscles were significantly higher during phonation and during water swallowing than at rest. This initial study suggests that the 3D movements of velopharyngeal-related muscles can be successfully and precisely visualized without side effects. The magnetic resonance signal changes seen in the superior pharyngeal constrictor and levator veli palatini muscles using the technique described here should be useful to develop better methods of evaluation of velopharyngeal function.

Velopharyngeal insufficiency can cause problems such as aspiration dysphonia, obstruction of drinking water, and stridor1. In patients with cleft palate and those 0901-5027/000001+010

who have undergone surgeries for oral cancers, these dysfunctions lead to decreased quality of life (QoL)2,3. Appropriate treatment for velopharyngeal

Key words: cine-MRI; velopharyngeal; dynamic; function. Accepted for publication 7 August 2019

insufficiency is a very important social need. The ability to clinically evaluate velopharyngeal function in patients is becoming increasingly important. However,

ã 2019 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

2

Joujima et al.

it is often difficult to evaluate velopharyngeal function objectively and appropriately, because the movement of the soft palate and superior pharyngeal constrictor muscles is rapid, and only precise visualization of their three-dimensional (3D) actions will provide an accurate evaluation of velopharyngeal function, including phonation-related events. Flexible nasopharyngoscopy has been used for routine clinical evaluation of velopharyngeal function4. However, the key disadvantages of nasopharyngoscopy are the possible occurrence of syncope, mucosal perforation, negative responses to topical anaesthetics, discomfort, vomiting reflex, and nose bleeding4. In addition, nasopharyngoscopy cannot visualize what happens during white-out4. Furthermore, the movements of the levator veli palatini muscles during velopharyngeal function cannot be visualized by flexible nasopharyngoscopy. As a result, real-time 3-T magnetic resonance imaging (MRI) that allows detailed evaluation of velopharyngeal function with appropriate temporal resolution has recently been developed5. However, 3-T MRI systems are not available in the majority of hospitals, and MRI techniques cannot be clinically applied for detailed evaluation of velopharyngeal function in most hospitals. New techniques using 1.5T MRI systems need to be developed to provide precise and objective evaluation of velopharyngeal function. The aim of this study was to investigate the usefulness of a newly developed technique using 1.5-T MRI systems for the evaluation of velopharyngeal function. Subjects and methods Subjects

Eleven volunteers (nine men, two women; mean age 26.5 years, range 23–30 years) with no history or presence of aspiration dysphonia, no obstruction of drinking water, and no stridor were recruited. All subjects were Japanese and native Japanese speakers. Approval for the study was obtained from the Institutional Review Board at Kyushu Dental University (No. 16-52). Informed consent was obtained from all volunteers prior to MRI.

Imaging parameters for high-speed continuous MRI based on T2-weighted sequences

All images were acquired using a 1.5-T full-body MRI system (Excelart Vantage powered by Atlas; Toshiba, Tokyo, Japan)

with a circular polarized neck coil to visualize the movement of the soft palate, superior pharyngeal constrictor muscles, and levator veli palatini muscles in the velopharyngeal region. Cine-MRI based on T2-weighted sequences was performed for each subject. Prior to the cine-MRI sequence, static T1- and T2-weighted images in the axial, coronal, and sagittal planes were also acquired for each subject to be used as a locator for the extent and angulation on cine-MRI and for precise anatomical analysis. In addition, abnormalities in the acquired regions were evaluated. Subjects were examined in the supine position using a circular polarized neck coil centred on the velopharyngeal area. RF-spoiled steady-state free precession field-echo images with radial encoding were continuously acquired with the parameters listed in Table 1. The parameters of cine-MRI based on T2-weighted sequences were: repetition time (TR), 3.2 ms; echo time (TE), 1.6 ms; flip angle (FA), 45 ; field of view (FOV), 250  225 mm2; and slice thickness, 8 mm. The sequences for the static T1- and T2weighted images are also shown in Table 1. Individual images were obtained from 10 radial spokes distributed equally to sample the MRI data space. A corresponding image acquisition time of about 36 ms results in an actual temporal resolution of 28 fps, with image interpolation or data sharing in a sliding-window reconstruction. Cine-MRI movies based on T2-weighted sequences of the subject pronouncing one word, ‘‘papa’’, were recorded using midsagittal orientations to evaluate functions in the velopharyngeal region. On phonation of the word ‘‘papa’’, nasal airflow increases significantly, and the area under the pressure curve decreases significantly more in patients with velopharyngeal inadequacy than in healthy volunteers6. ‘‘Papa’’ is a word that is easy to remember for volunteers. In addition, cine-MRI movies of the subject swallowing 5 ml of saline solution were also

recorded, in accordance with the method described by Tanaka et al.7. The subjects were removed from the scanner and given 5 ml of water to keep in the oral cavity until the signal was given by the clinician for them to swallow. The midsagittal plane covering the velopharyngeal area including the oral cavity, nasopharynx, and pharynx was seen on MRI (Fig. 1). The axial plane was placed at the level of the soft palate to visualize the closure of the nasopharynx (Fig. 1). The oblique coronal imaging was performed along the plane of the levator veli palatini muscles to visualize their movement (Fig. 1)8,9. Subjects were instructed in phonation of the word ‘‘papa’’ and in water swallowing by a clinician standing next to them throughout the MRI procedure. Phonation and swallowing were conducted in separate sessions. The clinician then gave a signal to the subject to start saying the word or to swallow the water, corresponding with the start of cine-MRI, and the subject immediately started phonation or swallowing. The respective function was performed once for each cine-MRI based on T2-weighted sequences, which lasted about 10 s. As all relevant anatomical structures move during phonation or water swallowing, movies of individual phonation or water swallowing were sequentially recorded in midsagittal, axial, and oblique coronal sections. The section in which the respective function and the rest period were best illustrated was chosen for image evaluation. The angulated planes, more in oblique coronal than axial imaging, were performed in an individually configured fashion. Image evaluation

All images were independently assessed by two expert radiologists (T.T. and M.O.) recognized by the Japanese Society for Oral and Maxillofacial Radiology. If there was a discrepancy between the radiologists’ scores, consensus was reached by discussion. In addition, all of the images

Table 1. Imaging parameters. Sequences

TR (ms) TE (ms) Flip angle ( ) FOV (mm) Section thickness (mm) Intersection gap (mm) Matrix (pixel)

Cine-MRI

T1-weighted images

T2-weighted images

3.2 1.6 45 250  225 8 – 120  96

820 15 90 220  220 6 1 320  224

4100 100 90 220  220 6 1 256  224

MRI, magnetic resonance imaging; TR, repetition time; TE, echo time; FOV, field of view.

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

Evaluation of velopharyngeal function by cine-MRI

3

Fig. 1. Locations of the midsagittal, axial, and oblique coronal dynamic imaging planes. (A) Midsagittal cine-MRI based on the T2-weighted sequence movie plane is located on the locator images to cover the velopharyngeal area including the oral cavity, nasopharynx, and pharynx. (B) The axial plane is placed at the level of the soft palate using the midsagittal image. (C) The oblique coronal imaging plane to visualize the levator veli palatini muscles is obtained by aiming at the origin on the midsagittal image (C-1; arrow) and insertion on the lateral sagittal image visualizing the pterygoid process (C-2; arrow).

were assessed again by the same radiologists twice after 1 week. These raters had no prior knowledge of the volunteers’ identities, since all images were read in a blinded and randomized manner. The images from cine-MRI based on T2weighted sequences were evaluated using the methods described below7. The following velopharyngeal functions in phonation of the one word ‘‘papa’’ or in water swallowing were assessed: (1) contact between the soft palate and the posterior pharyngeal wall; (2) movements of the soft palate, levator veli palatini muscles, and superior constrictor pharyngeal muscles. The ability to detect and characterize distinct velopharyngeal functions was rated on a fivepoint scale for each subject, as follows: 1, not detectable; 2, poor detectability; 3, detectable; 4, good detectability; or 5, excellent detectability.

Quantitative analysis

Alterations in the signal intensity for the levator veli palatini muscles and superior constrictor pharyngeal muscles were also measured between rest and phonation or water swallowing. The alterations in signal intensity of the muscles were measured using the method of Choi et al.10, with modifications. In brief, on the cineMRI at rest, the bilateral regions of interest (ROIs) were placed on the levator veli palatini muscles or superior pharyngeal constrictor muscles, and signal intensities of the ROIs were measured at the corresponding locations during phonation or water swallowing (Fig. 2). The signal intensities of the masseter muscles were then measured in the rest and working phases as the control for the cine-MRI. The rate of change in the signal intensity between rest and working was calculated as SIworking/SIrest for the respective muscles.

Sample size calculation

The sample size was calculated using G*Power version 3.1.9.2 (HeinrichHeine-Universita¨t Du¨sseldorf, Du¨sseldorf, Germany) and with reference to previous studies11–15. Input parameters and sample sizes were as follows: tails, two; effect size (difference), 0.8; alpha error, 0.05; power (1 beta error), 0.6; sample size, 10.

Statistical analysis

All statistical analyses were performed using SPSS version 23 statistical software (SPSS Inc., Chicago, IL, USA). Differences in the rate of change of the signal intensity for the velopharyngeal-related and non-related muscles given as SIworking/SIrest between rest and activity during phonation or during water swallowing were analyzed using the paired t-test. Differences in the signal intensity of the velopharyngeal-related muscles between rest and activity during phonation or during water swallowing were analyzed using the paired t-test. The level of significance was set at P < 0.05. Inter- and intra-observer agreement and reliability were assessed for the image score evaluation using kappa (k) statistics and the percentage agreement. Results Representative cine-MRI based on T2weighted sequences for phonation

For each subject, the total acquisition time of cine-MRI for phonation of the word ‘‘papa’’ in the midsagittal, axial, and oblique coronal imaging planes was approximately 3 minutes. Representative cine-MRI findings based on T2-weighted sequences during phonation are described below (Fig. 3; Supplementary Material Video 1). Cine-MRI showed that when velopharyngeal closure occurred appropriately, the soft palate and levator veli palatini muscles moved backward and contacted the posterior

wall of the oropharynx as frontal side closure. At the same time, the superior pharyngeal constrictor muscles projected frontally and bilaterally as the posterior, right, and left side closures. Unexpectedly, the signals of the levator veli palatini muscles and the superior pharyngeal constrictor muscles changed markedly during phonation in the sequences obtained, and they were higher than those measured during rest (before and during phonation). The rate of change in signal intensity between before and during phonation was 1.36  0.34 for the levator veli palatini muscles in the oblique coronal images and 1.98  0.45 for the superior constrictor pharyngeal muscles in the axial images (mean  standard deviation values) (Table 2). In contrast, the ratio of the signal intensities for the masseter muscles was 0.96  0.08 in the oblique coronal images and 0.99  0.05 in the axial images, showing almost no change from before to during phonation (Table 2). A significant difference in the signal intensity between rest and activity of the levator veli palatini muscles was found in the oblique coronal images (paired t-test, P < 0.001). Similarly, a significant difference in signal intensity was found between rest and activity of the superior pharyngeal constrictor muscles in the axial images (paired t-test, P < 0.001). Conversely, no significant difference in signal intensity of the masseter muscles was found between rest and activity in the oblique coronal images (paired t-test, P = 0.12) or axial images (paired t-test, P = 0.38). A significant difference in the signal intensity ratio (SIworking/SIrest) was clearly found between the levator veli palatini and masseter muscles (paired t-test, P = 0.004) (Table 2). In addition, a significant difference in the signal intensity ratio (SIworking/ SIrest) was found between the superior pharyngeal constrictor and masseter muscles (paired t-test, P < 0.001) (Table 2). The mean score of the two raters for the detectability of all phonations was

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

4

Joujima et al.

Fig. 2. Measurement diagrams superimposed on the magnetic reaonance images of signal intensity in the quantitative analysis. The signal intensities are calculated on the cine-MRI during rest (A), phonation (B), and swallowing (C). The signal intensities of the superior pharyngeal constrictor muscles (yellow), levator veli palatini muscles (purple), and masseter muscles (green) are measured on the axial images (A-1, B-1, C-1) and oblique coronal images (A-2, B-2, C-2).

4.52  0.62. With regard to individual functions, the mean score of the two raters was 4.82  0.28 for velopharyngeal closure, 3.84  0.74 for movements of the soft palate, 4.66  0.45 for movements of the levator veli palatini muscles, and 4.77  0.36 for movements of the superior pharyngeal constrictor muscles (Table 3). The kappa statistic indicated good diagnostic agreement between the radiologists (k = 0.670, percentage agreement 83.0%)

and good intra-observer reliability (k = 0.868, percentage agreement 93.2%). Representative cine-MRI based on T2weighted sequences for water swallowing

For each subject, the total acquisition time of cine-MRI for water swallowing in the midsagittal, axial, and oblique coronal imaging planes was approximately 3 min-

utes. Representative cine-MRI findings based on T2-weighted sequences during swallowing are described water below (Fig. 4; Supplementary Material Video 2). Cine-MRI showed that when the velopharyngeal closure occurred appropriately, the soft palate and the levator veli palatini muscles moved backward and contacted the posterior wall of the oropharynx as frontal side closure. At the

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

Evaluation of velopharyngeal function by cine-MRI

5

Fig. 3. Representative cine-MRI (A, midsagittal; B, axial; C, oblique coronal) during rest (1) and phonation of the word ‘‘papa’’ (2). During phonation, velopharyngeal closure is appropriately visualized and is associated with the soft palate and the levator veli palatini muscles moving backward and contacting the posterior wall of the oropharynx as frontal side closure (A, B, C). The signals of the superior pharyngeal constrictor muscles (B; arrows) and the levator veli palatini muscles (C; red arrows) are conspicuously increased and higher than those at rest. The signal intensities of the masseter muscles (B, C; arrowheads) show little change between before and during phonation.

same time, the superior pharyngeal constrictor muscles projected frontally and bilaterally as posterior, right, and left side closures. As for phonation, the signals of the levator veli palatini muscles and the superior pharyngeal constrictor muscles changed markedly during water swallowing on cine-MRI using the sequences described, and they were higher than those at rest (before and during water swallowing).

The rate of change in signal intensity was 1.50  0.50 for the levator veli palatini muscles in the oblique coronal images and 2.20  0.79 for the superior pharyngeal constrictor muscles in the axial images (mean  standard deviation), comparing before versus during water swallowing (Table 2). In contrast, the ratio of the signal intensity of the masseter muscles was 1.05  0.09 in the oblique coronal

images and 1.04  0.10 in the axial images, showing almost no change from before to during swallowing (Table 2). A significant difference in signal intensity was found between rest and activity of the levator veli palatini muscles in the oblique coronal images (paired t-test, P < 0.001). Similarly, a significant difference in signal intensity was found between rest and activity of the superior

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

6

Joujima et al.

Table 2. Differences in signal intensity in the levator veli palatini and superior pharyngeal constrictor muscles between before and during phonation or water swallowing. Slice for calculation Pronunciation Levator veli palatini muscle Superior constrictor pharyngeal muscle Masseter muscle Masseter muscle Water swallowing Levator veli palatini muscle Superior constrictor pharyngeal muscle Masseter muscle Masseter muscle

SIrest (Mean  SD)

SIworking (Mean  SD)

P-valuea

SI ratio (SIworking/SIrest) Mean  SD

95% CI

Oblique coronal Axial Oblique coronal Axial

1036  201 1411  201 1159  120 1333  278

1417  459 2787  720 1111  166 1314  230

<0.001* <0.001* 0.12 0.38

1.36  0.34b 1.98  0.45c 0.96  0.08b 0.99  0.05c

1.13–1.59 1.68–2.28 0.901–1.01 0.959–1.03

Oblique coronal Axial Oblique coronal Axial

949  192 1433  157 1171  186 1280  202

1399  466 3150  1228 1234  235 1332  205

<0.001* <0.001* 0.09 0.17

1.50  0.50d 2.20  0.79e 1.05  0.09d 1.04  0.10e

1.16–1.83 1.67–2.73 0.992–1.11 0.979–1.11

SI, signal intensity; SIworking, signal intensity in the working condition; SIrest, signal intensity at rest; SD, standard deviation; CI, confidence interval. a Paired t-test; *statistically significant (P < 0.05). b Significant difference, P = 0.004. c Significant difference, P < 0.001. d Significant difference, P = 0.014. e Significant difference, P < 0.001.

Table 3. Detectability during phonation and water swallowing. Mean  SD

Pronunciation Velopharyngeal closure Movements of soft palate Movements of levator veli palatini muscle Movements of superior constrictor pharyngeal muscle Total Swallowing Velopharyngeal closure Movements of soft palate Movements of levator veli palatini muscle Movements of superior constrictor pharyngeal muscle Total

Min

Median

Max

Inter-observer reliability

IQR

Intra-observer reliability

k value

Percentage agreement (%)

k value

Percentage agreement (%)

4.82  0.28 3.84  0.74 4.66  0.45

4.25 3 4

5 3.75 5

5 5 5

0.375 1 0.75

0.492 0.652 0.703

86.4 77.3 86.4

0.831 0.793 0.899

95.5 86.4 95.5

4.77  0.36

4

5

5

0.375

0.405

81.8

0.851

95.5

4.52  0.62

3

4.875

5

1

0.670

83.0

0.868

93.2

4.82  0.25 3.34  0.54 4.16  0.46

4.25 2.5 3.5

5 3 4.5

5 4.25 4.75

0.25 0.75 0.75

0.429 0.529 0.917

81.8 72.7 95.5

0.563 0.462 0.756

86.4 68.2 86.4

4.84  0.45

3.5

5

5

0

0.560

90.9

0.564

90.9

4.29  0.75

2.5

4.5

5

1.25

0.748

85.2

0.710

83.0

SD, standard deviation; IQR, interquartile range.

pharyngeal constrictor muscles in the axial images (paired t-test, P < 0.001). On the other hand, no significant difference in signal intensity of the masseter muscles was found between rest and swallowing in the oblique coronal images (paired t-test, P = 0.09) or the axial images (paired t-test, P = 0.17). No significant difference in the change ratio was seen between swallowing water and phonation of ‘‘papa’’ (levator veli palatini muscles, paired t-test, P = 0.14; superior pharyngeal constrictor muscles, paired t-test, P = 0.17). A significant difference was found in the signal intensity ratio (SIworking/SIrest) between the levator veli palatini and masseter mus-

cles (paired t-test, P = 0.014) (Table 2). In addition, a significant difference was found in the signal intensity ratio (SIworking/SIrest) between the superior pharyngeal constrictor and masseter muscles (paired ttest, P < 0.001) (Table 2). The mean score of the two raters for the detectability of all water swallowing was 4.29  0.75. With regard to individual functions, the mean score of the two raters was 4.82  0.25 for velopharyngeal closure, 3.34  0.54 for movements of the soft palate, 4.16  0.46 for movements of the levator veli palatini muscles, and 4.84  0.45 for movements of the superior pharyngeal constrictor muscles (Table 3).

The kappa statistic indicated good diagnostic agreement between the radiologists (k = 0.748, percentage agreement 85.2%) and good intra-observer reliability (k = 0.710, percentage agreement 83.0%). Discussion

The most interesting finding of the present study is that the new cine-MRI based on T2-weighted sequences using the 1.5-Tesla MRI system to evaluate velopharyngeal functions could visualize the movements of the soft palate, the levator veli palatini muscles, and the superior pharyngeal constrictor muscles during phonation of the

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

Evaluation of velopharyngeal function by cine-MRI

7

Fig. 4. Representative cine-MRI (A, midsagittal; B, axial; C, oblique coronal) during rest (1) and water swallowing (2). During water swallowing, velopharyngeal closure is appropriately visualized and is associated with the soft palate and the levator veli palatini muscles moving backward and contacting the posterior wall of the oropharynx as frontal side closure (A, B, C). The signals of the superior constrictor pharyngeal muscles (B; arrows) and the levator veli palatini muscles (C; red arrows) are conspicuously increased and higher than those at rest. The signal intensities of the masseter muscles (B, C; arrowheads) show little change between before and during swallowing.

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

8

Joujima et al.

word ‘‘papa’’ and during water swallowing based on visual scores. In particular, the velopharyngeal closure associated with the movement of the soft palate, the levator veli palatini muscles, and the superior pharyngeal constrictor muscles during both phonation and water swallowing was appropriately observed in all volunteers. These important results indicate that this novel method of cine-MRI based on T2-weighted sequences could be applied clinically for the dynamic functional evaluation of velopharyngeal status, and that this method may be able to accurately visualize and appropriately diagnose velopharyngeal function in patients with velopharyngeal insufficiency. The most surprising and interesting result was that the signals of the levator veli palatini muscles and the superior pharyngeal constrictor muscles showed conspicuous changes during phonation and water swallowing on cine-MRI using the present sequences, and they were higher than those during rest. In previous studies investigating real-time cine-MRI, T1weighted imaging-related sequences using fast low angle shot (FLASH) and true fast imaging with steady-state precession (true FISP) were employed in almost all cases16–19. The reason for this is that cine-MRI using these sequences commonly has better temporal resolution in a shorter time than T2-weighted imagingrelated sequences. On brief review of the literature, only one other report has presented real-time cine-MRI based on T2weighted sequences, and this previous study used half-Fourier acquisition single-shot turbo spin-echo (HASTE)20. Thus is appears that MRI signal changes of the levator veli palatini and superior pharyngeal constrictor muscles during velopharyngeal function have not been reported previously. The current interesting findings are the result of cine-MRI using T2-weighted sequences, as used in previous studies on myometrium and the temporomandibular joint21,22. Blood flow should increase in the muscles during function, such as contraction or shrinking21. The study findings could be explained by the fact that the volume of blood-in-flow effects within the levator veli palatini muscles and the superior pharyngeal constrictor muscles associated with velopharyngeal function might reflect the increased magnetic resonance (MR) signals on T2-weighted images. There has been a report of a similar phenomenon, with MR signals of the posterior soft tissues of the temporomandibular disc being very increased during mouth opening on T2-weighted images22.

It was speculated that the present alterations in the signal intensities of the levator veli palatini muscles and the superior pharyngeal constrictor muscles during activity might more directly affect the motor functions of each muscle, and the present findings should be quite different from the results reported so far. Based on the current MR signal increasing effect, one can more exactly and objectively visualize and appropriately diagnose velopharyngeal function in patients with velopharyngeal insufficiency. For example, the MR signal change rates in patients with velopharyngeal insufficiency might indicate reduced velopharyngeal function when compared to the change rates in healthy volunteers. The intention is to apply this method clinically in patients with velopharyngeal insufficiency as the next stage of our research. In the present study, modified MRI sequences used previously to image cardiac movements were applied as a new technique to observe the soft palate, levator veli palatini muscles, and the superior pharyngeal constrictor muscles7,23,24. This novel technique is expected to help address two important issues. The first is to avoid the need for contrast medium and additional treatment beyond the oral administration of saline solution in the clinical evaluation of velopharyngeal insufficiency. The second is that bone defect areas and supplemental soft tissues in patients with cleft lips, alveoli, and palates may also be visualized non-invasively, easily, and three-dimensionally, in addition to the evaluation of phonation and swallowing. With the use of MRI, this technique avoids ionizing radiation. The system also offers the ability to examine phonation and swallowing in arbitrary image orientations without changing the position of the patient. MRI evaluation of velopharyngeal function could potentially provide new data for speech and swallowing rehabilitation or the preoperative counselling of patients with regard to expected functional outcomes. Although cine-MRI using T1-weighted imaging appears to offer better temporal resolution than that using T2-weighted imaging7, the high temporal resolution of 28 fps with the present technique resembles that of cine-MRI using T1weighted imaging. This new technique has successfully allowed visualization of the series of events in normal phonation25– 29 . One of the most significant disadvantages of the technique is the short scan time of 10 s. Phonation and water swallowing are rapid, taking only a few sec-

onds, but this could be as much as 5 s in patients with insufficiency30. The series of movements of the soft palate, levator veli palatini muscles, and the superior pharyngeal constrictor muscles during phonation and water swallowing could be visualized in all volunteers using the present technique, but acquisition must be performed appropriately. As a next stage, this technique will be applied to patients with velopharyngeal insufficiency to elucidate its usefulness and potential weaknesses. Another major problem with visualizing swallowing events using MRI systems is that the patient is commonly in the supine position. This position is almost unavoidable and was also used in the present study. In major MRI studies reported in the literature, the swallowing movements examined would thus differ in some respects from those made by an individual in the normal upright position25–29,31–36. In the present study, however, the sequence of swallowing events observed was almost identical to that described in textbooks using videofluoroscopy with the individual upright36. In particular, the present technique allows the evaluation of velopharyngeal and swallowing function, in addition to indirect visualization of 3D bone defects and soft tissue anomaly without additional treatment. A further limitation of the present study is that only the word ‘‘papa’’ was used for the evaluation of velopharyngeal function during phonation by cine-MRI based on T2-weighted images. However, various other words, for example ‘‘puppy’’, can affect velopharyngeal function, and these should be used for evaluation in the next stage37. The evaluation of velopharyngeal insufficiency using MRI should prove valuable, and it may replace other examinations such as water-swallowing tests in some instances. Funding

This study was supported in part by grantsin-aid for scientific research from the Ministry of Education, Science, Sports and Culture of Japan to YM (No. 17K11680). Competing interests

The authors declare that there is no conflict of interest. Ethical approval

This study was approved by the Institutional Review Board of Kyushu Dental University (No. 16-52).

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

Evaluation of velopharyngeal function by cine-MRI Patient consent

Not required. 10.

Appendix A. Supplementary data

Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.ijom.2019. 08.001.

11.

References 1. Cousins N, MacAulay F, Lang H, MacGillivray S, Wells M. A systematic review of interventions for eating and drinking problems following treatment for head and neck cancer suggests a need to look beyond swallowing and trismus. Oral Oncol 2013;49:387–400. http://dx.doi.org/10.1016/j.oraloncology.20 12.12.002. 2. Murphy BA, Gilbert J. Dysphagia in head and neck cancer patients treated with radiation: assessment, sequelae, and rehabilitation. Semin Radiat Oncol 2009;19:35–42. http://dx.doi.org/10.1016/j.semradonc.2008. 09.007. 3. Rudnick EF, Sie KC. Velopharyngeal insufficiency: current concepts in diagnosis and management. Curr Opin Otolaryngol Head Neck Surg 2008;16:530–5. http://dx.doi.org/ 10.1097/MOO.0b013e328316bd68. 4. Westein D. Functional endoscopic tests of swallowing. In: Carrau RL, Murry T, Howell RJ, editors. Comprehensive management of swallowing disorders. second edition. San Diego, CA: Plural Publishing; 2017. p. 123–8. 5. Breyer T, Echternach M, Arndt S, Richter B, Speck O, Schumacher M, Markl M. Dynamic magnetic resonance imaging of swallowing and laryngeal motion using parallel imaging at 3 T. Magn Reson Imaging 2009;27:48–54. http://dx.doi.org/10.1016/j. mri.2008.05.018. 6. Mayo R, Warren DW, Zajac DJ. Intraoral pressure and velopharyngeal function. Cleft Palate Craniofac J 1998;35:299–303. 7. Tanaka T, Oda M, Nishimura S, Kito S, Wakasugi-Sato N, Kodama M, Kokuryo S, Habu M, Miyamoto I, Yamashita Y, Aso A, Sadasue K, Nagashima R, Tominaga K, Yoshioka I, Morimoto Y. The use of highspeed, continuous, T2-weighted magnetic resonance sequences and saline for the evaluation of swallowing. Oral Surg Oral Med Oral Pathol Oral Radiol 2014;118:490–6. http://dx.doi.org/10.1016/j.oooo.2014.05. 014. 8. Perry JL, Sutton BP, Kuehn DP, Gamage JK. Using MRI for assessing velopharyngeal structures and function. Cleft Palate Craniofac J 2014;51:476–85. http://dx.doi.org/10. 1597/12-083. 9. Wermker K, Jung S, Joos U, Kleinheinz J. Nasopharyngeal development in patients

12.

13.

14.

15.

16.

17.

18.

19.

with cleft lip and palate: a retrospective case–control study. Int J Otolaryngol 2012;2012:458507. http://dx.doi.org/10.11 55/2012/458507. Choi HJ, Kim JK, Ahn H, Kim CS, Kim MH, Cho KS. Value of T2-weighted MR imaging in differentiating low-fat renal angiomyolipomas from other renal tumors. Acta Radiol 2011;52:349–53. http://dx.doi.org/10.1258/ ar.2010.090491. Rosen SP, Abdelhalim SM, Jones CA, McCulloch TM. Effect of body position on pharyngeal swallowing pressures using high-resolution manometry. Dysphagia 2018;33:389–98. http://dx.doi.org/10.1007/ s00455-017-9866-3. Skirko JR, Weaver EM, Perkins JA, Kinter S, Eblen L, Sie KC. Validity and responsiveness of VELO: a velopharyngeal insufficiency quality of life measure. Otolaryngol Head Neck Surg 2013;149:304–11. http://dx.doi. org/10.1177/0194599813486081. Mozzanica F, Lorusso R, Robotti C, Zambon T, Corti P, Pizzorni N, Vanderwegen J, Schindler A. Effect of age, sex, bolus volume, and bolus consistency on whiteout duration in healthy subjects during FEES. Dysphagia 2019;34:192–200. http://dx.doi. org/10.1007/s00455-018-9961-0. George TN, Kotlarek KJ, Kuehn DP, Sutton BP, Perry JL. Differences in the tensor veli palatini between adults with and without cleft palate using high-resolution 3-dimensional magnetic resonance imaging. Cleft Palate Craniofac J 2018;55:697–705. http://dx.doi.org/10.1177/1055665617752 802. Dentino KM, Marrinan EM, Brustowicz K, Mulliken JB, Padwa BL. Pharyngeal flap is effective treatment for post maxillary advancement velopharyngeal insufficiency in patients with repaired cleft lip and palate. J Oral Maxillofac Surg 2016;74:1207–14. http://dx.doi. org/10.1016/j.joms.2015.12.016. Nunthayanon K, Honda E, Shimazaki K, Ohmori H, Inoue-Arai MS, Kurabayashi T, Ono T. Differences in velopharyngeal structure during speech among Asians revealed by 3-Tesla magnetic resonance imaging movie mode. Biomed Res Int 2015;2015:126264. http://dx.doi.org/10.1155/2015/126264. Sinko K, Czerny C, Jagsch R, Baumann A, Kulinna-Cosentini C. Dynamic 1.5-T vs 3-T true fast imaging with steady-state precession (trueFISP)-MRI sequences for assessment of velopharyngeal function. Dentomaxillofac Radiol 2015;44:20150028. http://dx.doi.org/ 10.1259/dmfr.20150028. Raol N, Sagar P, Nimkin K, Hartnick CJ. New technology: use of cine MRI for velopharyngeal insufficiency. Adv Otorhinolaryngol 2015;76:27–32. http://dx.doi.org/ 10.1159/000368011. Sagar P, Nimkin K. Feasibility study to assess clinical applications of 3-T cine MRI coupled with synchronous audio recording during speech in evaluation of velo-

20.

21.

22.

23.

24.

25.

26.

27.

28.

29.

30.

9

pharyngeal insufficiency in children. Pediatr Radiol 2015;45:217–27. http://dx.doi.org/ 10.1007/s00247-014-3141-7. Kulinna-Cosentini C, Czerny C, Baumann A, Weber M, Sinko K. TrueFisp versus HASTE sequences in 3T cine MRI: evaluation of image quality during phonation in patients with velopharyngeal insufficiency. Eur Radiol 2016;26:2892–8. Masui T, Katayama M, Kobayashi S, Nakayama S, Nozaki A, Kabasawa H, Ito T, Sakahara H. Changes in myometrial and junctional zone thickness and signal intensity: demonstration with kinematic T2-weighted MR imaging. Radiology 2001;221:75–85. http://dx.doi.org/10.1148/radiol.221100 1390. Suenaga S, Hamamoto S, Kawano K, Higashida Y, Noikura T. Dynamic MR imaging of the temporomandibular joint in patients with arthrosis. Am J Roentgenol 1996;166:1475– 81. http://dx.doi.org/10.2214/ajr.166.6.8633 468. Scha¨r M, Kozerke S, Fischer SE, Boesiger P. Cardiac SSFP imaging at 3 Tesla. Magn Reson Med 2004;51:799–806. http://dx.doi. org/10.1002/mrm.20024. Li W, Li BSY, Polzin JA, Mai VM, Prasad PV, Edelman RR. Myocardial delayed enhancement imaging using inversion recovery single-shot steady-state free precession: initial experience. J Magn Reson Imaging 2004;20:327–30. http://dx.doi.org/10.1002/ jmri.20095. Flaherty RF, Seltzer S, Campbell T, Weisskoff RM, Gilbert RJ. Dynamic magnetic resonance imaging of vocal cord closure during deglutition. Gastroenterology 1995;109:843–9. http://dx.doi.org/10.1016/0016-5085(95) 90393-3. Anagnostara A, Stoeckli S, Weber OM, Kollias SS. Evaluation of the anatomical and functional properties of deglutition with various kinetic high-speed MRI sequences. J Magn Reson Imaging 2001;14:194–9. http:// dx.doi.org/10.1002/jmri.1172. Barkhausen J, Goyen M, von Winterfeld F, Lauenstein T, Debatin JF. Visualization of swallowing using real-time trueFISP MR fluoroscopy. Eur Radiol 2002;12:129–33. http:// dx.doi.org/10.1007/s00330-001-1146-8. Karac¸ay S, Akin E, Sayin MO, Bulakbaşi N. Real time balanced turbo field echo cine-MRI in the analysis of deglutition events and transit times. J Oral Rehabil 2006;33:646–53. http:// dx.doi.org/10.1111/j.1365-2842.2005.01605.x. Panebianco V, Ruoppolo G, Pelle G, Schettino I, Roma R, Bernardo S, De Vincentiis C, Longo L, Passariello R. Morpho-functional patterns of physiologic oropharyngeal swallowing evaluated with dynamic fast MRI. Eur Arch Otorhinolaryngol 2010;267:1461–6. http://dx.doi. org/10.1007/s00405-010-1232-0. Shibata S, Inamoto Y, Saitoh E, Kagaya H, Aoyagi Y, Ota K, Akahori R, Fujii N, Palmer JB, Gonza´lez-Ferna´ndez M. The effect of bolus volume on laryngeal closure and UES

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.

YIJOM-4257; No of Pages 10

10

Joujima et al.

opening in swallowing: kinematic analysis using 320-row area detector CT study. J Oral Rehabil 2017;44:974–81. http://dx.doi.org/ 10.1111/joor.12573. 31. Zhang S, Olthoff A, Frahm J. Real-time magnetic resonance imaging of normal swallowing. J Magn Reson Imaging 2012;35:1372–9. http://dx.doi.org/10.1002/jmri.23591. 32. Kreeft AM, Rasch CR, Muller SH, Pameijer FA, Hallo E, Balm AJ. Cine MRI of swallowing in patients with advanced oral or oropharyngeal carcinoma: a feasibility study. Eur Arch Otorhinolaryngol 2012;269:1703–11. http://dx.doi. org/10.1007/s00405-011-1861-y. 33. Suto Y, Kamba M, Kato T. Technical note: dynamic analysis of the pharynx during swallowing using Turbo-FLASH magnetic resonance imaging combined with an oral positive contrast agent—a preliminary study.

Br J Radiol 1995;68:1099–102. http://dx. doi.org/10.1259/0007-1285-68-814-1099. 34. Hartl DM, Albiter M, Kolb F, Luboinski B, Sigal R. Morphologic parameters of normal swallowing events using single-shot fast spin echo dynamic MRI. Dysphagia 2003;18:255–62. http://dx.doi.org/10.1007/ s00455-003-0007-9. 35. Ohkubo M, Sano T, Ishida R, Higaki T, Nishikawa K, Hayakawa Y, Otonari T, Yamamoto-Otonari M, Harada T, Wakoh M. Static MR images for diagnosis of swallowing. Bull Tokyo Dent Coll 2008;49:113– 9. http://dx.doi.org/10.2209/tdcpublication. 49.113. 36. Corbin-Lewis K, Liss JM, Sciortino KL. Clinical anatomy and physiology of the swallow mechanism. New York, NY: Thomson Delmar Learning; 2005: 146–7.

37. Popat H, Richmond S, Zhurov AI, Rosin Paul L, Marshall David. A geometric morphometric approach to the analysis of lip shape during speech: development of a clinical outcome measure. PLoS One 2013;8: e57368. http://dx.doi.org/10.1371/journal. pone.0057368.

Address: Yasuhiro Morimoto Division of Oral and Maxillofacial Radiology Kyushu Dental University 2-6-1 Manazuru Kokurakita-ku Kitakyushu 803-8580 Japan Tel.: +81 93 285 3094 Fax: +81 93 285 3094 E-mail: [email protected]

Please cite this article in press as: Joujima T, et al. Evaluation of velopharyngeal function using high-speed cine-magnetic resonance imaging based on T2-weighted sequences: a preliminary study, Int J Oral Maxillofac Surg (2019), https://doi.org/10.1016/j.