AORXXX10.1177/0003489414538607Annals of Otology, Rhinology & LaryngologyFritz et al


Magnetic Resonance Imaging of the Effortful Swallow

Annals of Otology, Rhinology & Laryngology 2014, Vol. 123(11) 786­–790 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489414538607 aor.sagepub.com

Mark Fritz, MD1, Eric Cerrati, MD1, Yixin Fang, PhD2, Avanti Verma, BS1, Stratos Achlatis, MD1, Cathy Lazarus, PhD3, Ryan C. Branski, PhD1, and Milan Amin, MD1

Abstract Objective: The effortful swallow was designed to improve posterior mobility of the tongue base and increase intraoral pressures. We characterized the effects of this maneuver via dynamic magnetic resonance imaging (dMRI) in healthy patients. Methods: A 3-T scanner was used to obtain dMRI images of patients swallowing pudding using normal as well as effortful swallows. Ninety sequential images were acquired at the level of the oropharynx in the axial plane for each swallow; 3 series were obtained for each swallow type for each patient. Images were acquired every 113 ms during swallowing. The images were analyzed with respect to oropharyngeal closure duration, anteroposterior and transverse distance between the oropharyngeal walls, and oropharyngeal area before and after closure. Results: Preswallow reduced pharyngeal area was observed (P = .02; mean = 212.61 mm² for effortful, mean = 261.92 mm² for normal) as well as prolonged pharyngeal closure during the swallow (P < .0001; mean = 742.18 ms for effortful, mean = 437.31 ms for normal). No other differences were noted between swallow types. Interrater and intrarater reliability of all measurements was excellent. Conclusion: This preliminary investigation is the first to evaluate the effects of effortful swallows via dMRI. In our cohort, consistent physiologic changes were elicited, consistent with clinical dogma regarding this maneuver. Keywords magnetic resonance imaging, effortful swallow, imaging, deglutition

Introduction Swallowing disorders commonly affect patients, with a prevalence of 22.6% among adult primary care patients1 and significantly higher rates among at-risk populations, including the elderly2 and those with neurological injury.3 In addition, those who have had head and neck cancer can have dysphagia following treatment either due to resection of oral tongue or tongue base following surgery or due to xerostomia or restriction of tongue base propulsion after treatment with radiotherapy. These disorders also have a significant effect on quality of life as a result of prolonged hospitalizations and impaired nutrition, as well as anxiety and depression.4 Given the significance of swallowing disorders and current knowledge of the complex swallow mechanism, techniques such as the effortful swallow were developed as a therapeutic strategy. The effortful swallow involves instructing patients, as the name implies, to increase their effort throughout the entire oropharyngeal swallow. This maneuver has been shown to affect oropharyngeal closure, increasing posterior motion of the tongue base as well as anterior motion of the posterior pharyngeal

wall.5 This technique also facilitates increased bolus pressure, pharyngeal swallow duration, and upper esophageal sphincter (UES) relaxation.5-9 One study of patients with moderate and severe pharyngeal dysfunction showed that, although effortful swallow did not reduce the number of aberrant swallows, it did reduce the depth of contrast penetration in the larynx, thereby effectively reducing aspiration risk.10


NYU Voice Center, Department of Otolaryngology–Head and Neck Surgery, New York University School of Medicine, New York, New York, USA 2 Division of Biostatistics, Department of Population Health, New York University School of Medicine, New York, New York, USA 3 Department of Otorhinolaryngology–Head and Neck Surgery, Albert Einstein College of Medicine, New York, New York, USA Corresponding Author: Ryan C. Branski, PhD, NYU Voice Center, Department of Otolaryngology–Head and Neck Surgery, New York University School of Medicine, 345 East 37th Street, Suite 306, New York, NY 10016, USA. Email: [email protected]

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Fritz et al Investigations regarding the physiology of the swallow mechanism and swallowing techniques have largely depended on videofluoroscopy and flexible endoscopy. Both offer a limited view of the interaction between the oropharynx, tongue base, and pharyngeal walls. Our group previously described dynamic magnetic resonance imaging (dMRI) as a technique that allows examination of the swallow sequence with improved visualization of these structures in the axial plane during normal swallow in healthy patients.11,12 Further study demonstrated good intraexaminer and interexaminer reliability for measurements of the pharyngeal area.13 Although a limitation of dMRI includes supine positioning and a theoretically increased risk of aspiration, studies have shown that bolus transport to the UES and timing of muscle activation are not changed by the supine position.14 Although the physiologic effects of the effortful swallow technique have been studied using videofluoroscopy and manometry, results have varied and the imaging modalities have offered limited view of the structures that are manipulated during the effortful swallow, specifically the tongue base and posterior oropharynx. To date, the physiology of the effortful swallow has not been studied using dMRI imaging, which offers the benefit of examining the swallow mechanism temporally with no exposure to ionizing radiation. We hypothesized that the anteroposterior distance from tongue base to posterior pharyngeal wall would be reduced in the effortful swallow due to increased tongue base muscle recruitment. Alternatively, the mechanism of this finding may be related to preparatory motion at the onset of swallowing.

Methods Participants The current study was approved by the Institutional Review Board at the New York University School of Medicine. Twenty healthy participants 18 to 30 years of age were included based on the following exclusion criteria: any current or previous swallowing complaints, cranial neuropathy, and claustrophobia. After obtaining informed consent, participants underwent an oral-motor examination to rule out any abnormalities. Aberrant findings on this examination led to exclusion.

Magnetic Resonance Imaging Protocol Dynamic MRI of swallowing was performed with the participant in the supine position with a 3.0-T scanner (Siemens, Erlangen, Germany) with a 4-channel head coil and a dual-channel neck coil. The turbo-FLASH (turbo-fast low angle shot) imaging sequence parameters were as follows: repetition time/echo time, 2.3/1.2 ms;

flip angle, 5 degrees; slice thickness, 10 mm; base resolution, 192; phase resolution, 50%; field of view, 150 × 200 mm; parallel acceleration factor, 2 (GRAPPA). Ninety sequential images were acquired at the level of the oropharynx (mid-C2 cervical vertebrae) in the axial plane for each swallow. Images were obtained every 113 ms during swallowing.

Swallowing Protocol All participants were trained outside the scanner on bolus delivery via syringe prior to data acquisition. In addition, all participants were trained in how to perform the effortful swallow, given the instruction to “swallow really hard, squeezing hard with your throat muscles.”5 A technician adjacent to the scanner administered each participant 5 mL of a high-protein pudding (Boost; Nestle Health Science, Vevey, Switzerland) from a 10-mL syringe. The pudding bolus is the standard viscosity employed to gauge the utility of the effortful swallow under videofluoroscopic visualization.15 Furthermore, the 5 mL volume of pudding is standard for the assessment of oropharyngeal swallow function with a pudding bolus.16 Each participant performed 3 identical swallows when cued. The swallows were then repeated as the participants were instructed to perform an effortful or hard swallow. Therefore, a total of 6 swallows was recorded per participant.

Data Acquisition and Statistical Analysis The dependent variables for each swallow were (1) the duration of pharyngeal closure (ms), (2) the preswallow anteroposterior length (mm), (3) the preswallow transverse length (mm), (4) the preswallow area (mm²), (5) the postswallow anteroposterior length (mm), (6) the postswallow transverse length (mm), and (7) the postswallow area (mm²). The anatomic boundaries were easily visible for measurement and tracing via ImageJ (National Institutes of Health, Bethesda, Maryland, USA). Measurements were recorded for each frame of the swallow, starting from a point just before the arrival of the bolus (approximately 3-4 frames) and continuing until just after bolus passage (approximately 3-4 frames). Oropharyngeal activation noted at C2 was used as the referent event employed for the selection of these frames. As a baseline reference, the resting position of the oropharynx was employed to ensure that the frames of interest encompassed both the initiation and termination of the swallow. Measurement of pharyngeal closure was calculated by multiplying the number of frames with zero area by 113 ms, the temporal resolution of image acquisition. For each dependent variable, the median was employed as each involved several measurements over time. Consequently, all dependent variables were considered to be scalar.

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Annals of Otology, Rhinology & Laryngology 123(11)

Four independent examiners (1 otolaryngologist, 1 speech-language pathologist, 1 non-otolaryngology physician, and 1 medical student) performed the measurements. All of the examiners were trained on the measurements of the swallow and they demonstrated consistent interrater and intrarater reliability. Previous work by the group confirmed interrater and intrarater reliability to be very high. The raters reviewed only the frames selected for analysis. Descriptive analysis was conducted regarding differences between 2 swallowing types—normal versus effortful. Mixed effect models were fitted to the data to determine if the dependent variables differed significantly during the 2 swallowing types and if they were consistent as the participants performed 3 swallows for each type. Mixed effect models took into account correlations among multiple swallows repeated by the same participant within subjects and were implemented by PROC MIXED (SAS 9.2).

Results Twenty patients completed the study protocol. All participants were female and all images obtained were high quality with little to no artifact or distortion. All participants tolerated the complete study protocol, including the supine bolus delivery, and no adverse events were noted. The interrater and intrarater reliabilities for the measurements were found to be 80% and 85%, respectively, as noted previously. Figure 1 shows a depiction of the sequence of swallow images obtained at the level of C2 for visualization of the pharynx during effortful and normal swallows. Figure 2 shows an example of how all of the measurements were traced in ImageJ. Statistical results are summarized in Table 1, in which both the raw means and the model adjusted means of the dependent variables were compared between 2 swallow types. The effortful swallow yielded reduced pharyngeal area preswallow (P = .02) compared to the normal swallow (mean = 212.61 mm² for effortful, mean = 261.92 for normal). The effortful swallows were associated with a reduced transverse length of the oropharynx at the level of C2 compared to normal swallows (P = .05) approaching significance (mean = 22.38 mm for effortful swallow, mean = 24.19 mm for normal). In addition, the effortful swallow had a prolonged duration of pharyngeal closure (P < .0001) compared to normal swallow (mean = 742.18 ms for effortful, mean = 437.31 ms for normal). No significant differences in anteroposterior (P = .72) or transverse lengths (P = .65) for the postswallow measurements were observed. The postswallow pharyngeal area also was not significantly different between swallows (P = .12). Finally, no significant differences were observed between 3 consecutive swallows for all dependent variables (all Ps > .57).

Figure 1.  The sequence of images showing normal pharyngeal posture (top left), preswallow posture (top right), total constriction during pharyngeal bolus passage (bottom left), and postswallow posture (bottom right).

Figure 2.  Resting pharyngeal posture at C2 with associated markings used for quantification of the transverse and anteroposterior planes as well as pharyngeal area.

Discussion This study is the first time that dMRI has been used in the assessment of the effects of an effortful swallow;

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Fritz et al Table 1.  Summary Data of Normal and Effortful Swallows. Normal Preswallow transverse length, mm   Raw mean (SD)   Model adjusted mean (SE) Preswallow anteroposterior length, mm   Raw mean (SD)   Model adjusted mean (SE) Preswallow pharyngeal area, mm²   Raw mean (SD)   Model adjusted mean (SE) Duration of pharyngeal closure, ms   Raw mean (SD)   Model adjusted mean (SE) Postswallow transverse length, mm   Raw mean (SD)   Model adjusted mean (SE) Postswallow anteroposterior length, mm   Raw mean (SD)   Model adjusted mean (SE) Postswallow pharyngeal area, mm²   Raw mean (SD)   Model adjusted mean (SE)


P Valuea

25.01 (4.33) 24.19 (0.93)

23.20 (5.22) 22.38 (0.91)


12.07 (3.72) 12.07 (0.55)

11.68 (4.25) 11.68 (0.54)

261.79 (115.53) 261.92 (14.68)

212.52 (97.90) 212.61 (14.41)

439.57 (119.78) 437.31 (28.70)

742.41 (270.07) 742.18 (28.19)

20.81 (5.48) 17.22 (1.22)

21.26 (6.43) 17.71 (1.21)

15.43 (3.06) 15.42 (0.50)

15.17 (4.18) 15.17 (0.49)

292.57 (91.48) 272.15 (21.35)

259.03 (125.15) 238.89 (21.05)

  .62     .02     < .0001     .65     .72     .12

Abbreviations: SD, standard deviation; SE, standard error. a Bold indicates statistical significance.

this technique continues to yield reproducible and reliable information regarding the mechanics of swallowing. The effortful swallow was associated with a significant reduction of pharyngeal area preswallow, likely associated with preparatory tongue base contraction, as well as increased pharyngeal closure time during effortful swallow. Our findings are consistent with previous data from Lazarus et al5 confirming prolonged contact duration, likely yielding enhanced tongue base-pharyngeal wall pressures with the use of maneuvers. Dynamic MRI offers several advantages over different imaging and detection methods in the assessment of swallowing physiology. Dynamic MRI offers temporal and spatial measurements of swallow at predetermined levels along the pharynx and upper esophagus. Simple calculations based on the frame acquisition rate can yield valuable temporal information regarding deglutition. Furthermore, spatial quantification of swallow dynamics is enhanced via axial sections, which allow for measurements of lateral wall motion and therefore pharyngeal area, dependent variables previously unmeasureable via videofluoroscopy. Although videofluoroscopy allows for real-time observations of swallow function and is critical in the detection of aspiration events, it is not inherently sensitive to detect small temporal changes as well as anteroposterior displacements. Similarly, manometry permits for ideal evaluation of pressures as well as temporal relationships at the level of the transducer but lacks the ability to characterize pharyngeal wall motion or

preswallow and postswallow events. Flexible endoscopic evaluation of swallowing allows for great assessment of preswallow and postswallow events and the determination of aspiration, but it is hampered by being blind during the actual act of deglutition. Dynamic MRI is not without limitations; primarily, the complexity of the imaging system allows for only 1 level at a time to be measured during 1 swallow. In the current study, C2 was selected as it is the level of the tongue base that would yield the biggest difference between swallowing trials. Due to the limited view, little information can be gathered about how much residue is left behind or whether there is aspiration. In addition, dMRI is much more expensive than fluoroscopy. Furthermore, another limitation of dMRI is related to temporal resolution. Identification of precise moments of interest in the context of the complexity of swallowing is challenging, likely related to the temporal resolution of 0.113 sec/frame. Finally, dMRI also lacks the ability to be performed and analyzed in real time, limiting the amount of information that can be gathered into discrete time intervals and measurements. In conclusion, dMRI represents a feasible way to evaluate the effects of a voluntary swallowing maneuver (effortful swallow) in normal participants. Although it has some limitations, dMRI offers several advantages not currently feasible with other modalities; these include characterization of transverse displacements, pharyngeal area, and delineation of soft tissue planes. We remain optimistic that

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Annals of Otology, Rhinology & Laryngology 123(11)

this modality will continue to evolve as an adjunct to fluoroscopy. Authors’ Note Portions of data contained in this article were accepted for poster presentation at the Combined Otolaryngology Spring Meetings/ American Bronchoesophageal Association, May 2014, Las Vegas, Nevada.

Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported, in part, by the Clinical and Translational Science Institute at the New York University School of Medicine.

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Magnetic resonance imaging of the effortful swallow.

The effortful swallow was designed to improve posterior mobility of the tongue base and increase intraoral pressures. We characterized the effects of ...
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