Dysphagia DOI 10.1007/s00455-013-9505-6
ORIGINAL ARTICLE
The Effect of Voluntary Pharyngeal Swallowing Maneuvers on Esophageal Swallowing Physiology Ashli O’Rourke • Lori B. Morgan • Enrique Coss-Adame • Michele Morrison Paul Weinberger • Gregory Postma
•
Received: 10 April 2013 / Accepted: 12 December 2013 Ó Springer Science+Business Media New York 2014
Abstract The purpose of our study was to evaluate whether swallowing maneuvers designed to impact pharyngeal physiology would also impact esophageal physiology. Healthy volunteers underwent high-resolution manometry while performing three randomized swallowing maneuvers with and without a 5-ml bolus: normal swallowing, Mendelsohn maneuver, and effortful swallowing. We examined esophageal parameters of peristaltic swallows, hypotensive or failed swallows (‘‘nonperistaltic swallows’’), distal contractile integral (DCI), contractile front velocity (CFV), intrabolus pressure, and transition zone (TZ) defect. Four females and six males (median age 39 years; range 25–53)
Presented at the Dysphagia Research Society meeting, Toronto, ON, Canada, March 10, 2012. A. O’Rourke (&) Department of Otolaryngology – Head and Neck Surgery, Evelyn Trammell Institute for Voice and Swallowing, Medical University of South Carolina, 135 Rutledge Avenue, Suite 1130, Charleston, SC 29425, USA e-mail: [email protected] L. B. Morgan Department of Communication Sciences and Special Education, University of Georgia, Athens, GA, USA E. Coss-Adame Department of Gastroenterology, Georgia Regents University, Augusta, GA, USA M. Morrison Department of Otolaryngology – Head & Neck Surgery, Naval Medical Center Portsmouth, Portsmouth, VA, USA P. Weinberger G. Postma Department of Otolaryngology – Head and Neck Surgery, Center for Voice, Airway and Swallowing Disorders, Georgia Regents University, Augusta, GA, USA
were included in the study. The overall number of nonperistaltic swallows was 21/40 (53 %) during normal swallowing, 27/40 (66 %) during the Mendelsohn maneuver, and 13/40 (33 %) during effortful swallowing. There were significantly more overall nonperistaltic swallows with the Mendelsohn maneuver compared with effortful swallowing (p = 0.003). While swallowing a 5-ml bolus, there were more nonperistaltic swallows during the Mendelsohn maneuver (12/20, 60 %) compared to that during normal swallowing (6/20, 30 %) (p = 0.05) and more peristaltic swallows during effortful swallowing as compared to Mendelsohn maneuver (p = 0.003). Intrabolus esophageal pressure was greater during the Mendelsohn maneuver swallows in the bolus-swallowing condition as compared to normal swallowing (p = 0.02). There was no statistical difference in DCI, CFV, or TZ defect between swallowing conditions. The Mendelsohn maneuver may result in decreased esophageal peristalsis while effortful swallowing may improve esophageal peristalsis. Because it is important to understand the implications for the entire swallowing mechanism when considering retraining techniques for our patients, further investigation is warranted. Keywords Esophageal peristalsis Dysphagia Swallowing maneuvers High-resolution manometry Deglutition Deglutition disorders Hypotensive peristalsis
Introduction Esophageal hypoperistalsis is a commonly encountered esophageal motility disorder that is frequently associated with dysphagia [1, 2]. Unfortunately, effective medical treatments for esophageal hypotensive peristalsis are lacking and those medications that are available often have
123
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
side effects or contraindications that limit their use. In addition, there is no universally accepted surgical treatment for isolated esophageal hypomotility. Voluntary pharyngeal swallowing maneuvers are commonly used to alter pharyngeal physiology and/or bolus flow. And while the pharyngeal changes associated with various swallowing maneuvers have been well studied with manometry [3–8], the investigation of the effect of these maneuvers on esophageal motility is limited. Lever et al. [9] evaluated esophageal physiology with perfusion manometry during effortful swallowing and found that effortful swallowing resulted in increased distal esophageal amplitudes [9]. Butler et al. [10] used solid-state manometry to conclude that effortful swallowing yielded significantly greater esophageal pressure amplitudes, longer esophageal contraction durations, and decreased risk of incomplete bolus clearance [10]. However, we do not know if other voluntary swallowing maneuvers result in an improved esophageal swallowing function. It is imperative that clinicians are aware of the effect of interventions on the entire swallowing mechanism. Just as Martin-Harris et al.’s work [11] challenged the temporal distinction between the oral and oropharyngeal ‘‘phases’’ of swallowing, alterations in what has been traditionally defined as the pharyngeal phase of swallowing may meaningfully affect the esophageal phase of swallow. In addition, previous investigations have not utilized high-resolution manometry (HRM), which has the advantage of a more detailed representation of peristaltic activity along the entire esophagus [12, 13]. The purpose of this study was to evaluate the effect of voluntary oropharyngeal swallowing maneuvers on esophageal function, possibly providing an additional therapeutic intervention for patients with esophageal hypotensive peristalsis.
Methods This pilot study was a prospective, repeated-measures design, with each subject serving as his/her own control. Healthy adult volunteers were recruited by word of mouth. Patients with a history of dysphagia, neuromuscular disorders, head and neck or digestive tract surgery, or cancer of the aerodigestive tract were excluded. This study was approved by the Georgia Health Sciences/Georgia Regents University Institutional Review Board. All participants provided informed written consent. Subjects underwent high-resolution esophageal TM manometry (HRM) with the ManoScan system (Sierra Scientific Instruments, Los Angeles, CA, USA) while completing ‘‘normal’’ swallows, the Mendelsohn maneuver, and effortful swallowing. The HRM catheter is a solidstate assembly, with a 4.2-mm outer diameter and 36
123
circumferential pressure sensors spaced at 1-cm intervals. Prior to each study, the catheter pressure transducers were calibrated from 0 and 300 mmHg using externally applied pressure in the pressure chamber. Analysis was completed utilizing the ManoView analysis software version 2.0.1TM (Sierra Scientific Instruments). Effortful swallowing primarily seeks to increase muscle contraction to generate greater pharyngeal pressures (to improve bolus clearance). Patients were asked to ‘‘swallow hard’’ using a ‘‘lingual focus’’ to maximize the oropharyngeal effect of the maneuver [14]. The Mendelsohn maneuver attempts to improve elevation of the larynx (for airway protection) and to increase the duration of the cricopharyngeal opening (for bolus passage into the esophagus). Patients were instructed that when they feel their larynx rise with swallowing, not to let it drop, but try to hold it up with their muscles for several seconds. All studies were performed with the subject in the upright position. While there is some debate on performing studies with the subject in the upright position, and normative data differences have been found between the upright and supine positions, we were not comparing the results to historical (or published) norms [15]. In addition, the upright position is more representative of how a patient participating in therapy would actually perform the swallowing maneuvers. Simultaneous submental surface electromyography (sEMG) was used for biofeedback to ensure that the swallowing maneuvers were performed correctly. Unsuccessful or erroneous attempts were not analyzed but rather repeated until the maneuver was properly performed. To decrease fatigue, subjects were trained by an experienced speech-language pathologist on how to complete the swallowing maneuvers on a day prior to performing the formal study. The most patent nasal cavity was anesthetized with lidocaine and vasoconstricted with a cotton pledget soaked with ephedrine. Care was taken not to oversaturate the pledget to reduce spillage into the pharynx. The oropharynx was anesthetized with a brief spray of CetacaineTM (benzocaine 14.0 %, butamben 2.0 %, tetracaine hydrochloride 2.0 %; Cetylite Inc., Pennsauken, NJ, USA). The catheter was passed through the nasal cavity and introduced into the esophagus while the subject performed sequential water swallows. Once the catheter spanned both the upper and lower esophageal sphincters, it was taped in place to the skin of the nose. Participants were given various times to acclimate to the catheter, with most requiring approximately 3–5 min. Acclimation was defined as the absence of excessive swallowing or gagging and the ability to easily follow provider instructions. Subjects completed two saliva (‘‘dry’’) swallows and two 5-ml water bolus (‘‘wet’’) swallows while performing each swallowing maneuver. Each bolus was presented
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Fig. 1 a Normal peristaltic swallow, showing a continuous 30-mmHg isobaric contour in the smooth muscle esophagus. b Failed swallow with lack of continuous 30-mmHg isobaric contour in the distal smooth muscle esophageal segments (S2 and S3)
orally via a catheter tip syringe to ensure uniform volume administration. A total of four swallows were recorded (two wet and two dry) for each subject for each swallowing condition (normal, effortful, and Mendelsohn maneuver). Therefore, a total of 40 swallows (four swallows per subject for ten subjects) were analyzed for each condition. The swallow maneuvers were completed by the subjects in random order. Statistical analysis was completed utilizing the Friedman test (nonparametric repeated-measures analysis of variance) to compare differences among all three swallowing conditions. The Wilcoxon signed-rank test for repeated measures was used for statistical analysis of ordinal data when comparing two groups (i.e. two swallowing conditions), and Fisher’s exact test was used for categorical data comparisons between two conditions. SPSS version 20 (SPSS, Inc., Chicago, IL, USA) was used for data analysis. Significance was determined a priori as p B 0.05. We examined the esophageal parameters of peristaltic swallows, hypotensive or failed swallows, distal contractile integral (DCI), contractile front velocity (CFV), intrabolus pressure (IBP), and transition zone (TZ) defect. We utilized the 2008–2009 Chicago classification system since it was the most widely accepted system in place at the time of study completion and data analysis [12, 16]. A normal peristaltic swallow was defined as a continuous 30-mmHg isobaric contour in the distal smooth muscle esophageal segments (S2 and S3) (Fig. 1a). A hypotensive swallow was defined as a C3-cm defect in the 30-mmHg isobaric
contour between the skeletal muscle esophagus (S1) and the smooth muscle esophagus (S2) segments. A failed swallow had no pressure [30 mmHg distal to the S1 esophageal segment (Fig. 1b). Failed or hypotensive swallows were grouped together as ‘‘nonperistaltic’’ swallows. Our primary outcome variable was the number of peristaltic versus nonperistaltic swallows. The transition zone is defined as the distance between the S1 and S2 segments. TZ defects greater than 3 cm have been associated with incomplete bolus transfer and dysphagia [17]. DCI is a measure of the length, strength, and duration of contraction and reflects the contractile vigor of the smooth muscle esophagus [16]. CFV is a measure of the speed (velocity) of the contraction. It is calculated from the slope of a line connecting the proximal to the distal margins of the smooth muscle segments (Fig. 2) [16]. IBP is the pressure generated by a bolus, created by the esophageal muscular contraction behind a bolus. Increased esophageal IBP can be seen in outflow obstruction at the esophagogastric junction (EGJ) or in areas of esophageal narrowing or obstruction.
Results Ten subjects were enrolled and completed the study. There were 4 female and 6 male participants with a median age of 39 years (range 25–53). In combined wet and dry swallowing conditions, there were significantly more nonperistaltic swallows while
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A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Fig. 2 DCI (a calculation of the average pressures seen in the distal isobaric contour, the black outlined area) reflects the magnitude of distal esophageal contraction. CFV indicates the velocity of the swallow and is represented by slope of the red line positioned over the distal isobaric contour (Color figure online)
Fig. 3 Overall number of nonperistaltic swallows (combined dry and wet conditions) by swallowing maneuver. There were significantly more nonperistaltic swallows during the Mendelsohn maneuver compared to that with effortful swallowing
subjects performed the Mendelsohn maneuver than when performing effortful swallowing (p = 0.003) (Fig. 3). In addition, during wet swallows, there was a significant increase in nonperistaltic swallows when the subjects were performing the Mendelsohn maneuver as compared normal swallowing (p = 0.05). Conversely, wet effortful swallowing resulted in a decrease in the number of
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Fig. 4 Number of nonperistaltic wet swallows by swallowing maneuver. Significantly more nonperistaltic swallows were seen during performance of the Mendelsohn maneuver than when the participants completed normal or effortful swallows
nonperistaltic swallows compared to normal swallowing, although this was not statistically significant (p = 0.2). During wet bolus swallows, there was a significant improvement (i.e. more peristaltic swallows) during effortful swallowing than during the Mendelsohn maneuver (p = 0.003) (Fig. 4).
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Table 1 Comparison of the number of non-peristaltic swallows in dry versus wet swallows
Normal
Dry (N = 20)
Wet (N = 20)
P value
15 (75 %)
6 (30 %)
0.007
Mendelsohn
15 (75 %)
12 (60 %)
0.32
Effortful
10 (50 %)
3 (15 %)
0.04
Fig. 6 Esophageal intrabolus pressure (IBP) during dry swallows by swallowing condition. There continued to be greater variation in IBP during the Mendelsohn maneuver, but overall the IBP was not statistically higher than during the other swallowing conditions
Discussion
Fig. 5 Esophageal intrabolus pressure (IBP) during wet swallows by swallowing condition. There was a large variation in the IBP during performance of the Mendelsohn maneuver and the average was statistically higher than during the other swallowing conditions
When comparing wet versus dry swallowing conditions, nonperistaltic swallows were less frequent during wet swallows than during dry swallows under the same condition (Table 1). Notably, the number of nonperistaltic swallows during normal dry swallowing (75 %) appears to be increased from the expectation of a normal individual to have B30 % failed swallows. It is important to note, however, that this normative percentage was derived from subjects during wet swallowing conditions while in the supine position. In fact, the number of nonperistaltic swallows during normal wet swallowing was 30 % in our study (Fig. 1). However, for reasons stated earlier, normative data cannot be compared to the data derived in the present study. Intrabolus esophageal pressure was greater during the Mendelsohn maneuver swallows than in both normal and effortful swallowing. This was statistically significant in comparison to normal swallowing in the wet condition (p = 0.02) (Fig. 5) but not in the dry condition (p = 0.08) (Fig. 6). We also observed greater variability in the IBP when individuals were performing the Mendelsohn maneuver as compared to normal or effortful swallowing. There was no statistical difference noted in DCI, CFV, or TZ defect between swallowing conditions. A representative comparison the HRM spatiotemporal pressure plots of each swallowing condition is shown in Fig. 7.
In our pilot study, we did not see an increase in DCI that would coincide with the increased esophageal amplitudes revealed in previous investigations. It may be that differences in DCI, which has a large variable range in normal individuals, were not able to be detected in our small sample size. In addition, Xiao et al. [15] described a reduction in DCI when the subject was in the sitting position as compared to swallowing while in the supine position. Voluntarily increased pharyngeal squeeze during effortful swallowing did result in a decrease in the number of nonperistaltic wet swallows (i.e. more peristaltic swallows) when compared with normal effort during swallowing. A mechanism for how voluntary pharyngeal skeletal muscle contraction could affect a positive change in esophageal smooth muscle contraction is yet to be determined but is intriguing. Performance of the Mendelsohn maneuver resulted in significantly more failed or hypotensive swallows than with normal swallowing, with a concurrent increase in esophageal intrabolus pressure. These findings could be explained by esophageal pan-pressurization due to closure of the lower esophageal sphincter. Increased intrathoracic pressure can develop from performance of the Valsalva maneuver while performing the Mendelsohn maneuver. In addition, abdominal/diaphragmatic contraction can create a transient functional outflow obstruction. These factors can result in the compartmentalization of pressure in the esophagus between the contractile front of the esophageal contraction and the EGJ [12]. This disrupts the primary peristaltic wave. Pan-pressurization of the esophagus during the Mendelsohn maneuver was seen in the topographic pressure plots of many of our study participants (Fig. 8).
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Fig. 7 Representative comparison of esophageal topographic pressure plots during different swallowing conditions. Note the prolonged elevation of the upper esophageal sphincter during the Mendelsohn
Fig. 8 Pan-pressurization of the esophagus noted in a patient performing the Mendelsohn maneuver (***). Note the increase in LES and abdominal pressure at the same time (arrow)
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maneuver (*) and increase in distal esophageal pressures during effortful swallowing (**)
The greater variability in intrabolus pressure seen during the Mendelsohn maneuver (Figs. 5, 6) likely reflects differences in each individual’s technique in performing the maneuver. While submental sEMG was used to assess the pharyngeal correctness of the maneuver and training with an experienced speech-language pathologist was completed, we did not account for abdominal contraction. Most importantly, although there might be wide variability in the subjects’ performance of the maneuvers during this study, this variability likely represents that which is seen in a typical clinical setting. Our study does have limitations. First, we had a small sample size with a limited number of repeated swallows per maneuver per participant. This was a pilot study and evaluation of these swallowing maneuvers in a greater number of subjects is needed to confirm our findings. In addition, we did not use impedance in conjunction with manometry, so while we could postulate regarding bolus escape in nonperistaltic swallows, we did not measure it. Lastly, one may criticize the use of topical anesthesia in our study out of concern that it affected swallowing function. While some controversy persists regarding the effect of topical anesthesia on laryngeal function, a growing number of studies have shown that, in small amounts, nasal and/or oropharyngeal anesthetics have minimal effects on voice and swallowing function [18–21]. We considered the amount of anesthesia administered in our study to not be detrimental to the ability of normal individuals to
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
accurately perform the swallowing maneuvers nor likely to affect the primary outcome measurement of esophageal function.
Conclusion When considering novel deglutitive retraining techniques for patients, there should also be consideration of how the entire swallowing mechanism is affected to optimize therapeutic strategies. The results of this pilot study suggest that performance of the Mendelsohn maneuver can create transient outflow obstruction which results in esophageal pan-pressurization and decreased esophageal peristalsis. This could be detrimental to functional swallowing and bolus clearance throughout the length of the esophagus. These data suggest that an effortful swallow maneuver may be of benefit by improving esophageal peristalsis. Disclosures The authors declare that they have no conflicts of interest. A generous grant was provided by Atos Medical Inc for the implementation of this project.
References 1. Hoshino M, Sundaram A, Srinivasan A, et al. The relationship between dysphagia, pump function, and lower esophageal sphincter pressures on high resolution manometry. J Gastrointest Surg. 2012;16(3):495–502. 2. Smout A, Fox M. Weak and absent peristalsis. Neurogastroenterol Motil. 2012;24(Suppl 1):40–7. 3. Bu¨low M, Olsson R, Ekberg O. Videomanometric analysis of supraglottic swallow, effortful swallow, and chin tuck in healthy volunteers. Dysphagia. 1999;14(2):67–72. 4. Hoffman MR, Mielens JD, Ciucci MR, Jones CA, Jiang JJ, McCulloch TM. High-resolution manometry of pharyngeal swallow pressure events associated with effortful swallow and the Mendelsohn maneuver. Dysphagia. 2012;27(3):418–26. 5. McCulloch TM, Hoffman MR, Ciucci MR. High-resolution manometry of pharyngeal swallow pressure events associated with head turn and chin tuck. Ann Otol Rhinol Laryngol. 2010;119(6):369–76. 6. Takasaki K, Umeki H, Hara M, Kumagami H, Takahashi H. Influence of effortful swallow on pharyngeal pressure: evaluation using a high-resolution manometry. Otolaryngol Head Neck Surg. 2011;144(1):16–20. 7. Umeki H, Takasaki K, Enatsu K, et al. Effects of a tongue-holding maneuver during swallowing evaluated by high-resolution manometry. Otolaryngol Head Neck Surg. 2009;141(1):119–22. 8. Takasaki K, Umeki H, Kumagami H, Takahashi H. Influence of head rotation on upper esophageal sphincter pressure evaluated by high-resolution manometry system. Otolaryngol Head Neck Surg. 2010;142(2):214–7.
9. Lever TE, Cox KT, Holbert D, Shahrier M, Hough M, KelleySalamon K. The effect of an effortful swallow on the normal adult esophagus. Dysphagia. 2007;22(4):312–25. 10. Butler S, Nekl C, Rees C, Leng I, Lever T. Effects of effortful swallow on esophageal peristalsis in healthy adults [abstract]. Dysphagia. 2011;46:440. 11. Martin-Harris B, Michel Y, Castell D. Physiologic model of oropharyngeal swallowing revisited. Otolaryngol Head Neck Surg. 2005;133:234–40. 12. Pandolfino JE, Fox MR, Bredenoord AJ, Kahrilas PJ. High-resolution manometry in clinical practice: utilizing pressure topography to classify oesophageal motility abnormalities. Neurogastroenterol Motil. 2009;21:796–806. 13. Ayazi S, Crookes P. High-resolution esophageal manometry: using technical advances for clinical advantages. J Gastrointest Surg. 2010;14(Suppl 1):S24–32. 14. Huckabee ML, Steele CM. An analysis of lingual contribution to submental surface electromyographic measures and pharyngeal pressure during effortful swallowing. Arch Phys Med Rehabil. 2006;87(8):1067–72. 15. Xiao Y, Read A, Nicode`me F, Roman S, Kahrilas PJ, Pandolfino JE. The effect of a sitting vs supine posture on normative esophageal pressure topography metrics and Chicago classification diagnosis of esophageal motility disorders. Neurogastroenterol Motil. 2012;24(10):509–16. 16. Pandolfino JE, Ghosh SK, Rice J, Clarke JO, Kwiatek MA, Kahrilas PJ. Classifying esophageal motility by pressure topography characteristics: a study of 400 patients and 75 controls. Am J Gastroenterol. 2008;103:27–37. 17. Bulsiewicz WJ, Kahrilas PH, Kwiatek MA, et al. Esophageal pressure topography criteria indicative of incomplete bolus clearance: a study using high-resolution impedance manometry. Am J Gastroenterol. 2009;104:2721–8. 18. Johnson PE, Belafsky PC, Postma GN. Topical nasal anesthesia and laryngopharyngeal sensory testing: a prospective, doubleblind crossover study. Ann Otol Rhinol Laryngol. 2003;112:14–6. 19. Kamarunas EE, McCullough GH, Guidry TJ, Mennemeier M, Schluterman K. Effects of topical nasal anesthetic on fiberoptic endoscopic examination of swallowing with sensory testing (FEESST). Dysphagia. 2013;. doi:10.1007/s00455-013-9473-x. 20. Walsh J, Branski RC, Verdolini K. Double-blind study on the effects of topical anesthesia on laryngeal secretions. J Voice. 2006;20(2):282–90. 21. Rubin AD, Shah A, Moyer CA, Johns MM. The effect of topical anesthesia on vocal fold motion. J Voice. 2009;23(1):129–31.
Ashli O’Rourke
MD
Lori B. Morgan CCC-SLP, PhD Enrique Coss-Adame Michele Morrison
MD
DO
Paul Weinberger
MD
Gregory Postma
MD
123
ORIGINAL ARTICLE
The Effect of Voluntary Pharyngeal Swallowing Maneuvers on Esophageal Swallowing Physiology Ashli O’Rourke • Lori B. Morgan • Enrique Coss-Adame • Michele Morrison Paul Weinberger • Gregory Postma
•
Received: 10 April 2013 / Accepted: 12 December 2013 Ó Springer Science+Business Media New York 2014
Abstract The purpose of our study was to evaluate whether swallowing maneuvers designed to impact pharyngeal physiology would also impact esophageal physiology. Healthy volunteers underwent high-resolution manometry while performing three randomized swallowing maneuvers with and without a 5-ml bolus: normal swallowing, Mendelsohn maneuver, and effortful swallowing. We examined esophageal parameters of peristaltic swallows, hypotensive or failed swallows (‘‘nonperistaltic swallows’’), distal contractile integral (DCI), contractile front velocity (CFV), intrabolus pressure, and transition zone (TZ) defect. Four females and six males (median age 39 years; range 25–53)
Presented at the Dysphagia Research Society meeting, Toronto, ON, Canada, March 10, 2012. A. O’Rourke (&) Department of Otolaryngology – Head and Neck Surgery, Evelyn Trammell Institute for Voice and Swallowing, Medical University of South Carolina, 135 Rutledge Avenue, Suite 1130, Charleston, SC 29425, USA e-mail: [email protected] L. B. Morgan Department of Communication Sciences and Special Education, University of Georgia, Athens, GA, USA E. Coss-Adame Department of Gastroenterology, Georgia Regents University, Augusta, GA, USA M. Morrison Department of Otolaryngology – Head & Neck Surgery, Naval Medical Center Portsmouth, Portsmouth, VA, USA P. Weinberger G. Postma Department of Otolaryngology – Head and Neck Surgery, Center for Voice, Airway and Swallowing Disorders, Georgia Regents University, Augusta, GA, USA
were included in the study. The overall number of nonperistaltic swallows was 21/40 (53 %) during normal swallowing, 27/40 (66 %) during the Mendelsohn maneuver, and 13/40 (33 %) during effortful swallowing. There were significantly more overall nonperistaltic swallows with the Mendelsohn maneuver compared with effortful swallowing (p = 0.003). While swallowing a 5-ml bolus, there were more nonperistaltic swallows during the Mendelsohn maneuver (12/20, 60 %) compared to that during normal swallowing (6/20, 30 %) (p = 0.05) and more peristaltic swallows during effortful swallowing as compared to Mendelsohn maneuver (p = 0.003). Intrabolus esophageal pressure was greater during the Mendelsohn maneuver swallows in the bolus-swallowing condition as compared to normal swallowing (p = 0.02). There was no statistical difference in DCI, CFV, or TZ defect between swallowing conditions. The Mendelsohn maneuver may result in decreased esophageal peristalsis while effortful swallowing may improve esophageal peristalsis. Because it is important to understand the implications for the entire swallowing mechanism when considering retraining techniques for our patients, further investigation is warranted. Keywords Esophageal peristalsis Dysphagia Swallowing maneuvers High-resolution manometry Deglutition Deglutition disorders Hypotensive peristalsis
Introduction Esophageal hypoperistalsis is a commonly encountered esophageal motility disorder that is frequently associated with dysphagia [1, 2]. Unfortunately, effective medical treatments for esophageal hypotensive peristalsis are lacking and those medications that are available often have
123
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
side effects or contraindications that limit their use. In addition, there is no universally accepted surgical treatment for isolated esophageal hypomotility. Voluntary pharyngeal swallowing maneuvers are commonly used to alter pharyngeal physiology and/or bolus flow. And while the pharyngeal changes associated with various swallowing maneuvers have been well studied with manometry [3–8], the investigation of the effect of these maneuvers on esophageal motility is limited. Lever et al. [9] evaluated esophageal physiology with perfusion manometry during effortful swallowing and found that effortful swallowing resulted in increased distal esophageal amplitudes [9]. Butler et al. [10] used solid-state manometry to conclude that effortful swallowing yielded significantly greater esophageal pressure amplitudes, longer esophageal contraction durations, and decreased risk of incomplete bolus clearance [10]. However, we do not know if other voluntary swallowing maneuvers result in an improved esophageal swallowing function. It is imperative that clinicians are aware of the effect of interventions on the entire swallowing mechanism. Just as Martin-Harris et al.’s work [11] challenged the temporal distinction between the oral and oropharyngeal ‘‘phases’’ of swallowing, alterations in what has been traditionally defined as the pharyngeal phase of swallowing may meaningfully affect the esophageal phase of swallow. In addition, previous investigations have not utilized high-resolution manometry (HRM), which has the advantage of a more detailed representation of peristaltic activity along the entire esophagus [12, 13]. The purpose of this study was to evaluate the effect of voluntary oropharyngeal swallowing maneuvers on esophageal function, possibly providing an additional therapeutic intervention for patients with esophageal hypotensive peristalsis.
Methods This pilot study was a prospective, repeated-measures design, with each subject serving as his/her own control. Healthy adult volunteers were recruited by word of mouth. Patients with a history of dysphagia, neuromuscular disorders, head and neck or digestive tract surgery, or cancer of the aerodigestive tract were excluded. This study was approved by the Georgia Health Sciences/Georgia Regents University Institutional Review Board. All participants provided informed written consent. Subjects underwent high-resolution esophageal TM manometry (HRM) with the ManoScan system (Sierra Scientific Instruments, Los Angeles, CA, USA) while completing ‘‘normal’’ swallows, the Mendelsohn maneuver, and effortful swallowing. The HRM catheter is a solidstate assembly, with a 4.2-mm outer diameter and 36
123
circumferential pressure sensors spaced at 1-cm intervals. Prior to each study, the catheter pressure transducers were calibrated from 0 and 300 mmHg using externally applied pressure in the pressure chamber. Analysis was completed utilizing the ManoView analysis software version 2.0.1TM (Sierra Scientific Instruments). Effortful swallowing primarily seeks to increase muscle contraction to generate greater pharyngeal pressures (to improve bolus clearance). Patients were asked to ‘‘swallow hard’’ using a ‘‘lingual focus’’ to maximize the oropharyngeal effect of the maneuver [14]. The Mendelsohn maneuver attempts to improve elevation of the larynx (for airway protection) and to increase the duration of the cricopharyngeal opening (for bolus passage into the esophagus). Patients were instructed that when they feel their larynx rise with swallowing, not to let it drop, but try to hold it up with their muscles for several seconds. All studies were performed with the subject in the upright position. While there is some debate on performing studies with the subject in the upright position, and normative data differences have been found between the upright and supine positions, we were not comparing the results to historical (or published) norms [15]. In addition, the upright position is more representative of how a patient participating in therapy would actually perform the swallowing maneuvers. Simultaneous submental surface electromyography (sEMG) was used for biofeedback to ensure that the swallowing maneuvers were performed correctly. Unsuccessful or erroneous attempts were not analyzed but rather repeated until the maneuver was properly performed. To decrease fatigue, subjects were trained by an experienced speech-language pathologist on how to complete the swallowing maneuvers on a day prior to performing the formal study. The most patent nasal cavity was anesthetized with lidocaine and vasoconstricted with a cotton pledget soaked with ephedrine. Care was taken not to oversaturate the pledget to reduce spillage into the pharynx. The oropharynx was anesthetized with a brief spray of CetacaineTM (benzocaine 14.0 %, butamben 2.0 %, tetracaine hydrochloride 2.0 %; Cetylite Inc., Pennsauken, NJ, USA). The catheter was passed through the nasal cavity and introduced into the esophagus while the subject performed sequential water swallows. Once the catheter spanned both the upper and lower esophageal sphincters, it was taped in place to the skin of the nose. Participants were given various times to acclimate to the catheter, with most requiring approximately 3–5 min. Acclimation was defined as the absence of excessive swallowing or gagging and the ability to easily follow provider instructions. Subjects completed two saliva (‘‘dry’’) swallows and two 5-ml water bolus (‘‘wet’’) swallows while performing each swallowing maneuver. Each bolus was presented
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Fig. 1 a Normal peristaltic swallow, showing a continuous 30-mmHg isobaric contour in the smooth muscle esophagus. b Failed swallow with lack of continuous 30-mmHg isobaric contour in the distal smooth muscle esophageal segments (S2 and S3)
orally via a catheter tip syringe to ensure uniform volume administration. A total of four swallows were recorded (two wet and two dry) for each subject for each swallowing condition (normal, effortful, and Mendelsohn maneuver). Therefore, a total of 40 swallows (four swallows per subject for ten subjects) were analyzed for each condition. The swallow maneuvers were completed by the subjects in random order. Statistical analysis was completed utilizing the Friedman test (nonparametric repeated-measures analysis of variance) to compare differences among all three swallowing conditions. The Wilcoxon signed-rank test for repeated measures was used for statistical analysis of ordinal data when comparing two groups (i.e. two swallowing conditions), and Fisher’s exact test was used for categorical data comparisons between two conditions. SPSS version 20 (SPSS, Inc., Chicago, IL, USA) was used for data analysis. Significance was determined a priori as p B 0.05. We examined the esophageal parameters of peristaltic swallows, hypotensive or failed swallows, distal contractile integral (DCI), contractile front velocity (CFV), intrabolus pressure (IBP), and transition zone (TZ) defect. We utilized the 2008–2009 Chicago classification system since it was the most widely accepted system in place at the time of study completion and data analysis [12, 16]. A normal peristaltic swallow was defined as a continuous 30-mmHg isobaric contour in the distal smooth muscle esophageal segments (S2 and S3) (Fig. 1a). A hypotensive swallow was defined as a C3-cm defect in the 30-mmHg isobaric
contour between the skeletal muscle esophagus (S1) and the smooth muscle esophagus (S2) segments. A failed swallow had no pressure [30 mmHg distal to the S1 esophageal segment (Fig. 1b). Failed or hypotensive swallows were grouped together as ‘‘nonperistaltic’’ swallows. Our primary outcome variable was the number of peristaltic versus nonperistaltic swallows. The transition zone is defined as the distance between the S1 and S2 segments. TZ defects greater than 3 cm have been associated with incomplete bolus transfer and dysphagia [17]. DCI is a measure of the length, strength, and duration of contraction and reflects the contractile vigor of the smooth muscle esophagus [16]. CFV is a measure of the speed (velocity) of the contraction. It is calculated from the slope of a line connecting the proximal to the distal margins of the smooth muscle segments (Fig. 2) [16]. IBP is the pressure generated by a bolus, created by the esophageal muscular contraction behind a bolus. Increased esophageal IBP can be seen in outflow obstruction at the esophagogastric junction (EGJ) or in areas of esophageal narrowing or obstruction.
Results Ten subjects were enrolled and completed the study. There were 4 female and 6 male participants with a median age of 39 years (range 25–53). In combined wet and dry swallowing conditions, there were significantly more nonperistaltic swallows while
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A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Fig. 2 DCI (a calculation of the average pressures seen in the distal isobaric contour, the black outlined area) reflects the magnitude of distal esophageal contraction. CFV indicates the velocity of the swallow and is represented by slope of the red line positioned over the distal isobaric contour (Color figure online)
Fig. 3 Overall number of nonperistaltic swallows (combined dry and wet conditions) by swallowing maneuver. There were significantly more nonperistaltic swallows during the Mendelsohn maneuver compared to that with effortful swallowing
subjects performed the Mendelsohn maneuver than when performing effortful swallowing (p = 0.003) (Fig. 3). In addition, during wet swallows, there was a significant increase in nonperistaltic swallows when the subjects were performing the Mendelsohn maneuver as compared normal swallowing (p = 0.05). Conversely, wet effortful swallowing resulted in a decrease in the number of
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Fig. 4 Number of nonperistaltic wet swallows by swallowing maneuver. Significantly more nonperistaltic swallows were seen during performance of the Mendelsohn maneuver than when the participants completed normal or effortful swallows
nonperistaltic swallows compared to normal swallowing, although this was not statistically significant (p = 0.2). During wet bolus swallows, there was a significant improvement (i.e. more peristaltic swallows) during effortful swallowing than during the Mendelsohn maneuver (p = 0.003) (Fig. 4).
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology Table 1 Comparison of the number of non-peristaltic swallows in dry versus wet swallows
Normal
Dry (N = 20)
Wet (N = 20)
P value
15 (75 %)
6 (30 %)
0.007
Mendelsohn
15 (75 %)
12 (60 %)
0.32
Effortful
10 (50 %)
3 (15 %)
0.04
Fig. 6 Esophageal intrabolus pressure (IBP) during dry swallows by swallowing condition. There continued to be greater variation in IBP during the Mendelsohn maneuver, but overall the IBP was not statistically higher than during the other swallowing conditions
Discussion
Fig. 5 Esophageal intrabolus pressure (IBP) during wet swallows by swallowing condition. There was a large variation in the IBP during performance of the Mendelsohn maneuver and the average was statistically higher than during the other swallowing conditions
When comparing wet versus dry swallowing conditions, nonperistaltic swallows were less frequent during wet swallows than during dry swallows under the same condition (Table 1). Notably, the number of nonperistaltic swallows during normal dry swallowing (75 %) appears to be increased from the expectation of a normal individual to have B30 % failed swallows. It is important to note, however, that this normative percentage was derived from subjects during wet swallowing conditions while in the supine position. In fact, the number of nonperistaltic swallows during normal wet swallowing was 30 % in our study (Fig. 1). However, for reasons stated earlier, normative data cannot be compared to the data derived in the present study. Intrabolus esophageal pressure was greater during the Mendelsohn maneuver swallows than in both normal and effortful swallowing. This was statistically significant in comparison to normal swallowing in the wet condition (p = 0.02) (Fig. 5) but not in the dry condition (p = 0.08) (Fig. 6). We also observed greater variability in the IBP when individuals were performing the Mendelsohn maneuver as compared to normal or effortful swallowing. There was no statistical difference noted in DCI, CFV, or TZ defect between swallowing conditions. A representative comparison the HRM spatiotemporal pressure plots of each swallowing condition is shown in Fig. 7.
In our pilot study, we did not see an increase in DCI that would coincide with the increased esophageal amplitudes revealed in previous investigations. It may be that differences in DCI, which has a large variable range in normal individuals, were not able to be detected in our small sample size. In addition, Xiao et al. [15] described a reduction in DCI when the subject was in the sitting position as compared to swallowing while in the supine position. Voluntarily increased pharyngeal squeeze during effortful swallowing did result in a decrease in the number of nonperistaltic wet swallows (i.e. more peristaltic swallows) when compared with normal effort during swallowing. A mechanism for how voluntary pharyngeal skeletal muscle contraction could affect a positive change in esophageal smooth muscle contraction is yet to be determined but is intriguing. Performance of the Mendelsohn maneuver resulted in significantly more failed or hypotensive swallows than with normal swallowing, with a concurrent increase in esophageal intrabolus pressure. These findings could be explained by esophageal pan-pressurization due to closure of the lower esophageal sphincter. Increased intrathoracic pressure can develop from performance of the Valsalva maneuver while performing the Mendelsohn maneuver. In addition, abdominal/diaphragmatic contraction can create a transient functional outflow obstruction. These factors can result in the compartmentalization of pressure in the esophagus between the contractile front of the esophageal contraction and the EGJ [12]. This disrupts the primary peristaltic wave. Pan-pressurization of the esophagus during the Mendelsohn maneuver was seen in the topographic pressure plots of many of our study participants (Fig. 8).
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A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
Fig. 7 Representative comparison of esophageal topographic pressure plots during different swallowing conditions. Note the prolonged elevation of the upper esophageal sphincter during the Mendelsohn
Fig. 8 Pan-pressurization of the esophagus noted in a patient performing the Mendelsohn maneuver (***). Note the increase in LES and abdominal pressure at the same time (arrow)
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maneuver (*) and increase in distal esophageal pressures during effortful swallowing (**)
The greater variability in intrabolus pressure seen during the Mendelsohn maneuver (Figs. 5, 6) likely reflects differences in each individual’s technique in performing the maneuver. While submental sEMG was used to assess the pharyngeal correctness of the maneuver and training with an experienced speech-language pathologist was completed, we did not account for abdominal contraction. Most importantly, although there might be wide variability in the subjects’ performance of the maneuvers during this study, this variability likely represents that which is seen in a typical clinical setting. Our study does have limitations. First, we had a small sample size with a limited number of repeated swallows per maneuver per participant. This was a pilot study and evaluation of these swallowing maneuvers in a greater number of subjects is needed to confirm our findings. In addition, we did not use impedance in conjunction with manometry, so while we could postulate regarding bolus escape in nonperistaltic swallows, we did not measure it. Lastly, one may criticize the use of topical anesthesia in our study out of concern that it affected swallowing function. While some controversy persists regarding the effect of topical anesthesia on laryngeal function, a growing number of studies have shown that, in small amounts, nasal and/or oropharyngeal anesthetics have minimal effects on voice and swallowing function [18–21]. We considered the amount of anesthesia administered in our study to not be detrimental to the ability of normal individuals to
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
accurately perform the swallowing maneuvers nor likely to affect the primary outcome measurement of esophageal function.
Conclusion When considering novel deglutitive retraining techniques for patients, there should also be consideration of how the entire swallowing mechanism is affected to optimize therapeutic strategies. The results of this pilot study suggest that performance of the Mendelsohn maneuver can create transient outflow obstruction which results in esophageal pan-pressurization and decreased esophageal peristalsis. This could be detrimental to functional swallowing and bolus clearance throughout the length of the esophagus. These data suggest that an effortful swallow maneuver may be of benefit by improving esophageal peristalsis. Disclosures The authors declare that they have no conflicts of interest. A generous grant was provided by Atos Medical Inc for the implementation of this project.
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Ashli O’Rourke
MD
Lori B. Morgan CCC-SLP, PhD Enrique Coss-Adame Michele Morrison
MD
DO
Paul Weinberger
MD
Gregory Postma
MD
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