Evaluating swallowing muscles essential for hyolaryngeal elevation by using muscle functional magnetic resonance imaging

Abstract

Purpose: Reduced hyolaryngeal elevation, a critical event in swallowing, is associated with radiation therapy. Two muscle groups that suspend the hyoid, larynx, and pharynx have been proposed to elevate the hyolaryngeal complex: the suprahyoid and longitudinal pharyngeal muscles. Thought to assist both groups is the thyrohyoid, a muscle intrinsic to the hyolaryngeal complex. Intensity modulated radiation therapy guidelines designed to preserve structures important to swallowing currently exclude the suprahyoid and thyrohyoid muscles. This study used muscle functional magnetic resonance imaging (mfMRI) in normal healthy adults to determine whether both muscle groups are active in swallowing and to test therapeutic exercises thought to be specific to hyolaryngeal elevation.

Methods and materials: mfMRI data were acquired from 11 healthy subjects before and after normal swallowing and after swallowing exercise regimens (the Mendelsohn maneuver and effortful pitch glide). Whole-muscle transverse relaxation time (T2 signal, measured in milliseconds) profiles of 7 test muscles were used to evaluate the physiologic response of each muscle to each condition. Changes in effect size (using the Cohen d measure) of whole-muscle T2 profiles were used to determine which muscles underlie swallowing and swallowing exercises.

Results: Post-swallowing effect size changes (where a d value of >0.20 indicates significant activity during swallowing) for the T2 signal profile of the thyrohyoid was a d value of 0.09; a d value of 0.40 for the mylohyoid, 0.80 for the geniohyoid, 0.04 for the anterior digastric, and 0.25 for the posterior digastric-stylohyoid in the suprahyoid muscle group; and d values of 0.47 for the palatopharyngeus and 0.28 for the stylopharyngeus muscles in the longitudinal pharyngeal muscle group. The Mendelsohn maneuver and effortful pitch glide swallowing exercises showed significant effect size changes for all muscles tested, except for the thyrohyoid.

Conclusions: Muscles of both the suprahyoid and the longitudinal pharyngeal muscle groups are active in swallowing, and both swallowing exercises effectively target muscles elevating the hyolaryngeal complex. mfMRI is useful in testing swallowing muscle function.

Fig. 1

Illustration of muscles underlying hyolaryngeal elevation in swallowing. This mechanism stretches open an inhibited cricopharyngeus, which in turn forms the upper esophageal sphincter. The suprahyoid muscles comprise an anterior group that suspends the hyoid bone, and the long pharyngeal muscles form a posterior group that suspends the larynx. The thyrohyoid muscle is intrinsic to the hyolaryngeal complex and is thought to approximate the larynx and hyoid synergistically with the long pharyngeal muscles.

Fig. 2

Method for semiautomated muscle segmentation. The Osirix “growing region of interest” interface uses dynamic thresholding by averaging the 8 voxels immediately surrounding a seed point (red box) selected by the investigator (in bold). The algorithm determines the means and standard deviations of signal intensities of these 9 voxels and then selects all neighboring voxels falling within a standard deviation of the mean (in blue). In principle, tissue types that match the signal intensity of the seed point are segmented while other voxels are excluded.

Fig. 3

Effect size changes of mean T2 signal profiles under the stated conditions compared to those of the pre-swallow T2 signals. A value greater than 0.20 is considered significant, with >0.50 interpreted as a medium effect size and >0.80 as a large effect size change.

Fig. 4

T2 signal profiles of negative and positive control muscles. (a) Comparison of T2 profiles of negative control muscle (sterno-cleidomastoid) from pre- to post-swallowing. (b) Comparison of T2 signal profiles of the masseter after swallowing and after a prolonged bite (80 seconds) in 2 subjects. Post-bite T2 signal profiles show a significant difference (P =. 02) compared to post-swallowing profiles.