Content uploaded by Enrique Coss-Adame
Author content
All content in this area was uploaded by Enrique Coss-Adame on Jan 15, 2016
Content may be subject to copyright.
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
ÓSpringer Science+Business Media New York 2014
Abstract The purpose of our study was to evaluate whe-
ther 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, Men-
delsohn maneuver, and effortful swallowing. We examined
esophageal parameters of peristaltic swallows, hypotensive
or failed swallows (‘‘nonperistaltic swallows’’), distal con-
tractile integral (DCI), contractile front velocity (CFV), in-
trabolus pressure, and transition zone (TZ) defect. Four
females and six males (median age 39 years; range 25–53)
were included in the study. The overall number of nonperi-
staltic swallows was 21/40 (53 %) during normal swallow-
ing, 27/40 (66 %) during the Mendelsohn maneuver, and
13/40 (33 %) during effortful swallowing. There were sig-
nificantly 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 Men-
delsohn 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
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: aorourke@musc.edu
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
123
Dysphagia
DOI 10.1007/s00455-013-9505-6
side effects or contraindications that limit their use. In
addition, there is no universally accepted surgical treatment
for isolated esophageal hypomotility. Voluntary pharyn-
geal 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 con-
traction durations, and decreased risk of incomplete bolus
clearance [10]. However, we do not know if other volun-
tary swallowing maneuvers result in an improved esopha-
geal 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 peri-
staltic activity along the entire esophagus [12,13].
The purpose of this study was to evaluate the effect of
voluntary oropharyngeal swallowing maneuvers on esoph-
ageal 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 dis-
orders, 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
manometry (HRM) with the ManoScan
TM
system (Sierra
Scientific Instruments, Los Angeles, CA, USA) while
completing ‘‘normal’’ swallows, the Mendelsohn maneu-
ver, and effortful swallowing. The HRM catheter is a solid-
state assembly, with a 4.2-mm outer diameter and 36
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 2.0.1
TM
(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 oropha-
ryngeal 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 cri-
copharyngeal opening (for bolus passage into the esopha-
gus). 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 nor-
mative 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 swal-
lowing maneuvers. Simultaneous submental surface elec-
tromyography (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 experi-
enced 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 orophar-
ynx was anesthetized with a brief spray of Cetacaine
TM
(benzocaine 14.0 %, butamben 2.0 %, tetracaine hydro-
chloride 2.0 %; Cetylite Inc., Pennsauken, NJ, USA). The
catheter was passed through the nasal cavity and intro-
duced 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 var-
ious 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
123
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 sub-
ject 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 Fried-
man test (nonparametric repeated-measures analysis of
variance) to compare differences among all three swal-
lowing conditions. The Wilcoxon signed-rank test for
repeated measures was used for statistical analysis of
ordinal data when comparing two groups (i.e. two swal-
lowing 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
pB0.05.
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’’ swal-
lows. 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 dys-
phagia [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
Fig. 1 a Normal peristaltic
swallow, showing a continuous
30-mmHg isobaric contour in
the smooth muscle esophagus.
bFailed swallow with lack of
continuous 30-mmHg isobaric
contour in the distal smooth
muscle esophageal segments
(S2 and S3)
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
123
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 swal-
lowing resulted in a decrease in the number of
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).
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
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
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
123
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 maneu-
ver 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.
Discussion
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 differ-
ences 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 swal-
lows) when compared with normal effort during swallow-
ing. A mechanism for how voluntary pharyngeal skeletal
muscle contraction could affect a positive change in
esophageal smooth muscle contraction is yet to be deter-
mined 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 esopha-
geal intrabolus pressure. These findings could be explained
by esophageal pan-pressurization due to closure of the
lower esophageal sphincter. Increased intrathoracic pres-
sure 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 dur-
ing the Mendelsohn maneuver was seen in the topographic
pressure plots of many of our study participants (Fig. 8).
Table 1 Comparison of the number of non-peristaltic swallows in
dry versus wet swallows
Dry (N=20) Wet (N=20) Pvalue
Normal 15 (75 %) 6 (30 %) 0.007
Mendelsohn 15 (75 %) 12 (60 %) 0.32
Effortful 10 (50 %) 3 (15 %) 0.04
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
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
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
123
The greater variability in intrabolus pressure seen during
the Mendelsohn maneuver (Figs. 5,6) likely reflects dif-
ferences 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 com-
pleted, 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 func-
tion. 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
Fig. 7 Representative comparison of esophageal topographic pres-
sure plots during different swallowing conditions. Note the prolonged
elevation of the upper esophageal sphincter during the Mendelsohn
maneuver (*) and increase in distal esophageal pressures during
effortful swallowing (**)
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)
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
123
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. Neurogastroen-
terol 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, Kelley-
Salamon 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-res-
olution manometry in clinical practice: utilizing pressure topog-
raphy 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 classifica-
tion diagnosis of esophageal motility disorders. Neurogastroen-
terol Motil. 2012;24(10):509–16.
16. Pandolfino JE, Ghosh SK, Rice J, Clarke JO, Kwiatek MA,
Kahrilas PJ. Classifying esophageal motility by pressure topog-
raphy 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, double-
blind 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 MD
Michele Morrison DO
Paul Weinberger MD
Gregory Postma MD
A. O’Rourke et al.: Effect of Pharyngeal Swallowing Maneuvers on Esophageal Physiology
123