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Clinical Focus

Effect of a Tongue-Holding Maneuver


on Posterior Pharyngeal Wall Movement
During Deglutition

Masako Fujiu
Jeri A. Logemann
Northwestern University, Evanston, IL

Effects of a tongue-holding maneuver on movement of the PPW, which has not been a
anterior bulging of the posterior pharyngeal wall target for direct treatment in the past. At
(PPW) during swallowing were investigated in present, the tongue-holding maneuver can be
10 young adult normal subjects. Videofluoro- employed clinically as an easy method for
graphic images of 3-ml liquid barium swallows testing the compliance of the PPW videofluoro-
were digitized to quantify the extent of anterior graphically. However, the use of the maneuver
bulge of the PPW with and without the maneu- per se, which inhibits posterior retraction of the
ver at the mid and the inferior levels of the base of tongue (BOT), resulted in increasing
second cervical vertebra. A significant increase the pharyngeal (specifically vallecular) residue
in PPW bulging was seen with the maneuver at after the swallow. The results also indicate the
both pharyngeal levels. These findings indicate importance of tongue movement in triggering
potential for developing new treatment tech- the pharyngeal swallow.
niques to facilitate compensatory anterior

M
ovement of the posterior pharyngeal wall (PPW) 1982). Functionally, contraction of the PPW appears to be
during deglutition has been investigated by a important in three ways: (a) contact with the BOT, which
number of researchers in the past (Basmajian & is the primary pressure generator during swallowing
Dutta, 1961; Ekberg & Borgstrom, 1989; Kahrilas, (McConnel, 1988; McConnel, Cerenko, & Mendelsohn,
Logemann, Lin, & Ergun, 1992; Palmer, Tanaka, & 1988), to facilitate pressure generation for continuous
Siebens, 1988; Perlman, Luschei, & Du Mond, 1989; bolus propulsion through the pharynx; (b) shortening of the
Ramsey, Watson, Gramiak, & Weinberg, 1955; Yoshida, pharynx for a safer and more efficient swallow (Kahrilas et
1979). In normal deglutition, the pharyngeal wall muscles al., 1992; Palmer et al., 1988); and (c) clearance of the
are known to contract progressively superiorly to inferiorly bolus from the pharynx (Kahrilas et al., 1992).
during the pharyngeal stage of swallowing, which is seen To date, PPW contraction during swallowing has not
as an anterior bulge of the PPW in the lateral plane of been thought to respond to direct treatment in dysphagic
fluoroscopic images (Logemann, 1993a, pp. 7–15). Once patients (Logemann, 1993b, p. 173). Thus, little attention
the pharyngeal swallow is triggered, anterior movement of has been paid in swallowing research to possible volitional
the PPW starts at the level of the upper oropharynx alteration in PPW movement. Clinically, however, an
(Ekberg & Borgstrom, 1989; Kahrilas et al., 1992). The increase in anterior bulging of the PPW has been observed
PPW, together with the medially moving lateral pharyngeal videofluorographically in some surgically treated oral
walls, eventually meets with the posteriorly moving base cancer patients during the course of their postoperative
of tongue (BOT). This contact of the PPW and BOT recovery (Fujiu, Logemann, & Pauloski, 1995; Pauloski,
applies pressure to the bolus tail, and pharyngeal contrac- Logemann, Fox, & Colangelo, 1995). These were the
tion progresses downward to the esophageal entrance patients whose anterior portion of the tongue, which is
following the bolus tail (Ekberg & Borgstrom, 1989; known to be important for the anchoring function during
Kahrilas et al., 1992). bolus propulsion (Kahrilas, Lin, Logemann, Ergun, &
Anatomically, the superior, middle, and inferior Facchini, 1993), was impaired with the tumor. We hypoth-
pharyngeal constrictor muscles are responsible for the esize that, in these oral cancer patients, (a) the disturbed
sequential contraction of the pharyngeal wall (Miller, anchoring function of the anterior tongue caused reduced

American Journal of Speech-Language Pathology • Vol. 5 • 1058-0360/96/0501-0023 © American Speech-Language-Hearing


Fujiu • Association
Logemann 23
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range of BOT movement; and (b) reduced BOT movement movement of the PPW, using an interactive computer
resulted in enhancing anterior bulge of the PPW. Since program (Logemann, Kahrilas, Begelman, Dodds, &
there is an anatomical link between the BOT and the PPW Pauloski, 1989). The following three measures were
by way of the glossopharyngeus muscle, one portion of the obtained for each swallow at the mid and the inferior levels
superior pharyngeal constrictor muscles (Zemlin, 1988, pp. of the second cervical vertebra (C2): (a) extent of PPW
272–273), influence of BOT movement on PPW bulge is bulging during BOT-PPW contact; (b) onset of the BOT-
possible. PPW contact in relation to cricopharyngeal opening
This study was designed to investigate the potential for (CPO); and (c) duration of the BOT-PPW contact. Mean
compensatory movement of the PPW during swallowing values for each measure for the three swallows with and
when movement of the BOT is restricted. A unique tongue- without maneuver were calculated from the individual
holding maneuver was developed in order to inhibit subjects for statistical analyses (paired t-test).
retraction of the BOT and potentially facilitate anterior In measuring the extent of anterior bulge of the PPW
bulge of the PPW in normal subjects. (Figure 2), the anterior-inferior corner of the C4 was marked
as an anchor point (labeled as “c”). Another point on the
anterior-inferior corner of the C2 (labeled as “b”) was also
Methods marked, forming the line “bc” for the approximate posture of
Subjects were 10 healthy male adults between ages 19 the vertebral column. The distance between point “b” and a
and 26 years with the mean age of 23 years. Six swallows point on the surface of the PPW “a” was measured by
of 3 ml liquid barium were performed, alternating with and drawing a line perpendicular to the line “bc”. The line “ab” is
without the tongue-holding maneuver (three swallows the extent of anterior bulge of the PPW. The same distance
each). For the tongue-holding maneuver, the subjects were measurement was performed at the level of mid C2.
asked to protrude the tongue maximally but comfortably,
holding it between the central incisors, after a bolus was Temporal Measures and Observations
introduced into the mouth (Figure 1). The fluorographic
images of the lateral view of each swallow were recorded The following six temporal measures and three observa-
with a videocassette recorder (Sony U-matic, model VO- tions were obtained from frame-by-frame analysis of the
5800) at 30 frames per second. Temporal information was video images. Intraobserver reliability for all measures and
encoded on the videotape with a counter-timer at 0.01-s observations ranged from 96% to 100%. Interobserver
intervals (Thalner Electronics). Only the initial swallow on reliability ranged from 85% to 100%.
each bolus was used for the biomechanical and temporal Temporal Measures:
analyses. Repeated dry swallows were not analyzed. 1. Oral transit time (OTT): the interval from the onset of
oral tongue movement propelling the bolus posteriorly
Biomechanical Analysis until the bolus head reaches the point where the
posterior line of the ramus of the mandible crosses the
Twenty to 30 frames of the videofluorographic images BOT.
of each swallow, including the start and the end of BOT-
PPW contact, were digitized to quantify the anterior 2. Pharyngeal response time (PRT): the interval from the
onset of rapid laryngeal elevation as an indicator of the
triggering of the pharyngeal swallow, or the pharyngeal
FIGURE 1. Sagittal section of the head showing tongue swallow response, until the bolus tail passes through the
position without and with the maneuver. The subject was cricopharyngeal region.
asked to protrude the tongue maximally but comfortably,
holding it between the central incisors, after a bolus was 3. Pharyngeal delay: the time lag between the end of oral
introduced into the mouth. transit and the triggering of the pharyngeal response.
4. Onset of airway closure in relation to CPO: the time
difference between the first arytenoid to epiglottic base
contact and the first CPO.
5. Duration of airway closure: the interval from the first
arytenoid to epiglottic base contact until the end of the
contact.
6. Duration of CPO: the interval from the first opening of
tongue
tongue the cricopharyngeal region until the bolus tail passes the
region.
epiglottis epiglottis
Observations:
7. Approximate percentage of residue: residual material
after the swallow estimated by percentage for the entire
oral cavity (total oral residue), entire pharynx (total
No Maneuver Tongue Holding Maneuver pharyngeal residue), and specifically in the valleculae
(vallecular residue).

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FIGURE 2. Video print (above) and line drawing (below) illustrating measurement of the extent of anterior bulge of the posterior
pharyngeal wall (PPW). The anterior-inferior corner of C4 is marked as an anchor point (“c”) for determining the postural angle of
the vertebral column. Another point on the vertebral surface corresponding to the anterior-interior corner of C2 was marked as “b.”
Distance was measured by drawing a line, between point “b” and a point opposite on the PPW surface “a,” that is perpendicular to
the postural line “bc.” The same measurement method was performed at mid C2.

Fujiu • Logemann 25
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8. Resting position of the hyoid bone: level of the hyoid was no statistically significant difference in the onset of the
bone in relation to the cervical vertebrae prior to the BOT-PPW contact in relation to CPO or in the duration of
onset of posterior propulsion of the bolus. BOT-PPW contact between the swallows with and without
9. Location of the bolus head at the onset of the pharyn- the maneuver (Table 1).
geal swallow: pharyngeal structure(s) that bolus head When these three measures were compared between
reaches when the pharyngeal swallow is triggered. mid C2 and inferior C2 with the maneuver (Table 2),
anterior bulge of the PPW was significantly greater at mid
For statistical analyses, paired t-tests were used for C2 than at inferior C2 (p < 0.01). The onset of BOT-PPW
measures (1) through (7), and the sign test was used for contact was significantly earlier (p < 0.01), and contact
measure (8). duration was significantly longer, at mid C2 than at inferior
C2 (p < 0.01). These characteristics are also evident in the
graphs in Figure 4.
Results
Biomechanical Analysis Temporal Measures and Observations
All of the 10 subjects exhibited an increase in anterior There was no statistically significant difference with
bulge of the PPW with the maneuver as compared to their and without the maneuver in the temporal measures
swallows without the maneuver. Figure 3 shows the examined in this study, except the duration of airway
difference in the degree of anterior bulge of the PPW with closure, which was significantly shorter with the maneuver
and without the maneuver during BOT-PPW contact in one than without the maneuver (p < 0.05) (Table 3). Although
of the subjects (Subject 1). This subject exhibited notable not statistically significant, delay time was approximately
changes in anterior bulge with and without the maneuver 0.1 s longer with the maneuver than without the maneuver.
for all his swallows, although, in some subjects, the Some differences were noted with the maneuver in the
difference was less obvious. The graphs in Figure 4 show three observations. Table 4 shows the change in approxi-
sequential movements of the PPW and BOT during a mate percentage of residue. There was no statistically
swallow at the levels of mid C2 and inferior C2. This is the significant difference in oral residue with and without the
same swallow of the same subject (Subject 1) that is shown maneuver (p > 0.05). However, there was a significant
in Figure 3. increase in total pharyngeal residue with the maneuver (p <
Paired t-tests indicated that PPW bulging was signifi- 0.05). When specific locations of the pharyngeal residue
cantly greater with maneuver than without maneuver at were examined, vallecular residue was increased signifi-
both mid C2 and inferior C2 (p < 0.01) (Table 1). There cantly with the maneuver (p < 0.01) but not the residue in

FIGURE 3. Video prints of a subject illustrating the difference in the degree of anterior bulge of the PPW without (left) and with
(right) the maneuver during initial BOT-PPW contact. Anterior bulge of the PPW is greater with the maneuver than without the
maneuver.

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TABLE 1. Anterior bulge of the PPW at mid C2 and inferior C2.

Without Maneuver With Maneuver p Value


Mean SD Mean SD

Mid C2
PPW bulge (mm) 10.226 2.405 12.670 2.901 <0.001a
Onset of BOT-PPW contact to CPO (s) -0.053 0.155 -0.034 0.086 0.765
Duration of BOT-PPW contact (s) 0.390 0.069 0.408 0.057 0.544

Inferior C2
PPW bulge (mm) 8.633 1.893 9.880 2.754 <0.005a
Onset of BOT-PPW contact to CPO (s) 0.085 0.082 0.097 0.077 0.506
Duration of BOT-PPW contact (s) 0.289 0.089 0.267 0.078 0.364
a
Significant p < 0.01

TABLE 2. Anterior bulge of the PPW at mid C2 and inferior C2 with manuever.

Mid C2 Inferior C2 p Value


Mean SD Mean SD

PPW bulge (mm) 12.670 2.901 9.873 2.754 <0.0001a


Onset of BOT-PPW contact to CPO (s) -0.034 0.086 0.097 0.077 <0.0001a
Duration of BOT-PPW contact (s) 0.408 0.057 0.267 0.078 <0.0001a
a
Significant p < 0.01

FIGURE 4. Movements of the posterior pharyngeal wall (PPW) and base of tongue (BOT) over time during a swallow at the levels of
mid C2 and inferior C2 with the maneuver. Time zero (0.0) corresponds to the opening of the cricopharyngeal region. At the start of
the graph, PPW and BOT were separated. The two structures eventually come to contact, first at the mid C2 level, and later at the
inferior C2 level. Separation of the PPW and BOT at both mid and inferior C2 occurs at the same time.

10

Pharyngeal Wall

0 Mid C2
Base of Tongue
Movement in mm

-10

10

Pharyngeal Wall

0 Inferior C2
Base of Tongue

-10
-0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4 0.5
Time in Seconds

Fujiu • Logemann 27
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TABLE 3. Temporal measures with and without maneuver.

Without Maneuver With Maneuver p Value

Mean (s) SD Mean (s) SD

PPW bulge (mm) 12.670 2.901 9.873 2.754 <0.0001a


OTT 0.371 0.208 0.309 0.074 0.391
PRT 0.685 0.091 0.675 0.081 0.572
Pharyngeal delay -0.070 0.111 0.176 0.488 0.103
Airway closure onset to CPO -0.098 0.064 -0.106 0.062 0.746
Airway closure duration 0.527 0.134 0.448 0.119 0.025a
CPO duration 0.385 0.086 0.388 0.076 0.914
a
Significant p < 0.05

TABLE 4. Approximate percentage of residue with and without maneuver.

Without Maneuver With Maneuver p Value

Mean (%) SD Mean (%) SD

Total Oral Residue 2.217 0.783 3.967 21.895 0.222


Total Pharyngeal Residue 2.264 1.821 5.160 17.329 0.016a
Vallecular Residue 1.101 0.438 2.434 2.744 0.004b
Other Pharyngeal Residue 1.163 0.977 2.726 3.389 0.110
a
Significant p < 0.05
b
Significant p < 0.01

other pharyngeal locations, such as the aryepiglottic folds Previous studies from our laboratory indicate that
and pyriform sinuses (p > 0.1). increased anterior bulge of the PPW occurred over time in
In 7 of the 10 subjects, the resting position of the hyoid patients with an impairment in the anterior tongue (Fujiu et
bone was slightly higher with the maneuver. This was al., 1995; Pauloski et al., 1995). We speculate that the
statistically significant (sign test, p < 0.05) The change in patient’s impairment in the anterior tongue disturbed its
position was approximately 8 mm. In all of the 10 subjects, anchoring function during swallowing and affected
on swallows with the maneuver, the bolus head reached posterior retraction of the BOT. Since there is an anatomic
lower pharyngeal structures before the pharyngeal swallow link between the PPW and the BOT by the glossopharyn-
was triggered. Without the maneuver, the pharyngeal geus muscle (Zemlin, 1988, pp. 272–273), we hypothesize
swallow was triggered when the bolus head was between that disturbance in one end of the muscle’s attachment
the posterior tongue and the valleculae. With the maneu- might have affected the attachment of the other end.
ver, triggering of the pharyngeal swallow took place when Although the mean age of the subjects in this study (i.e., 23
the bolus head was between the BOT and the pyriform years) is younger than that of the oral cancer patients in the
sinuses. other two studies mentioned above (i.e., 58 and 55 years,
respectively), a study by Robbins, Hamilton, Lof, and
Kempster (1992) suggests no significant age effect on the
Discussion PPW movement. If that is the case, the same mechanisms
Contraction of the PPW and its contact with BOT is an and hypotheses might be applied to both groups. Signifi-
essential part of the pharyngeal swallow. However, in the cantly earlier onset of PPW-BOT contact at mid C2 than at
past, PPW contraction has not been thought to respond to inferior C2 (Table 2 and Figure 4) confirmed the concept
direct treatment in dysphagic patients (Logemann, 1993b, of sequential contraction of the pharyngeal constrictor
p. 173), and no therapeutic technique directed to the PPW muscles during the pharyngeal swallow (Ekberg &
has been introduced. This study demonstrates that, in Borgstrom, 1989; Kahrilas et al., 1992).
normal young adults, the degree of anterior bulging of the Clinically, the tongue-holding maneuver may be
PPW can be altered by changing the position of the employed for two purposes: (a) evaluation and (b) treat-
anterior tongue. Specifically, the anterior bulge of the PPW ment. Since the use of this maneuver immediately facili-
during swallowing was significantly greater with the tated anterior bulge of the PPW, it can be used as an easy
tongue-holding maneuver than without the maneuver, at method for testing the compliance of the PPW in
the levels of mid and inferior C2 (Table 1). dysphagic patients. Individuals with a more compliant

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PPW may show greater increases in anterior bulge of the bolus head reached lower pharyngeal structures with the
PPW over time. maneuver before the pharyngeal swallow was triggered. It
Although more systematic studies in patient populations appears that the 0.1-s increase in pharyngeal delay time
are needed before applying the maneuver in treatment, the introduced by the maneuver allowed the bolus to flow to a
results of this study suggest the potential for developing lower level of the pharynx. Slightly elevated resting
new approaches in therapy. Interestingly, in our previous position of the hyoid bone before the swallow with the
study (Fujiu et al., 1995), an increase in anterior bulge of maneuver might also have contributed to bringing the
the PPW was particularly notable in the patients who had pharyngeal structures to a higher level, so that the bolus
received “range of motion exercises” for the tongue, which reached these structures faster.
were not for facilitation of the PPW movement. Such The increased pharyngeal delay time seen in this study
exercises are designed to extend vertical and antero- with the tongue-holding maneuver supports the hypothesis
posterior range of motion of the tongue (Logemann, 1989, that tongue movement may provide critical sensory input
p. 1027), and are likely to affect the muscles attached to the to trigger the pharyngeal swallow. Larson (1985) posited
tongue base. It is possible that the lingual range of motion that lingual movements or a particular posturing of the
exercises influenced the function of the glossopharyngeus tongue could excite groups of receptors in such a way as to
muscle from its lingual attachment, and anatomically trigger the pharyngeal swallow. Without smooth tongue
facilitated the greater movement of its pharyngeal attach- movement, the timing of sensory input to the swallowing
ment, the PPW. center (Jean, 1984) might not be adequate, in turn delaying
In addition to its impact on PPW movement, the the triggering of the pharyngeal swallow.
maneuver also affected other aspects of swallowing. In the When the oral tongue moves backward to propel the
present study, three negative outcomes, which could bolus, high pressure is generated in the oral cavity
increase the risk of aspiration in some dysphagic patients, (Cerenko, McConnel, & Jackson, 1989; McConnel, 1988;
were observed. These include: (a) increased pharyngeal Shaker, Cook, Dodds, & Hogan, 1988). Such pressure and
residue, particularly in the valleculae; (b) shortened bolus movement in combination with tongue movement
duration of airway closure; and (c) increased pharyngeal may stimulate mechanoreceptors and pressure receptors in
delay time in triggering the pharyngeal swallow. the oral cavity, including the anterior faucial pillars,
The statistically significant increase in the total pharyn- reported to be one of the most sensitive sites to elicit
geal residue with the maneuver, particularly in the vallecu- swallowing with pressure (Pommerenke, 1928). Fujiu,
lae, is considered to be caused by reduced BOT movement Toleikis, Logemann, and Larson (1994) provided electro-
introduced by the maneuver. Even though the maneuver physiological data to support the importance of applying
facilitated anterior bulge of the PPW, holding the anterior pressure to the anterior pillar in eliciting the pharyngeal
portion of the tongue resulted in reduced posterior move- swallow in awake humans. Thus, the role the tongue plays
ment of the BOT. Under such conditions, anterior bulge of in triggering the pharyngeal swallow needs to be empha-
the PPW might not be sufficient to clear material from the sized along with its relation to various sensory receptors in
valleculae. These results confirm the importance of BOT the oral cavity, including chemoreceptors and mechanore-
retraction in clearing the bolus from the valleculae. ceptors, as well as proprioceptors in the tongue and other
Presumably, in a swallow in which tongue movement is oropharyngeal muscles.
not inhibited, pharyngeal clearance may be improved when Because of the possible increase in pharyngeal residue
anterior bulge of the PPW is increased. and pharyngeal delay time, the tongue-holding maneuver
Shortened airway closure with the maneuver might be per se may not result in an immediate improvement in
explained as follows. Since posterior retraction of the BOT swallowing function. Moreover, the shortened duration of
is reduced with the maneuver, posterior movement of the airway closure negatively affects the safety of swallowing
epiglottic base, a key component in airway entrance in some patients. However, the present study provides
closure (Logemann et al., 1992), may also be reduced. This clinicians with the possibility of actively changing the
might have resulted in later onset and earlier separation of degree of muscular contraction of the PPW, which has
the arytenoid to epiglottic base contact with the maneuver previously been thought not to respond to treatment.
than without the maneuver. Even though the time differ- Further investigations concerning the value of the tongue-
ence in each component of closure is not significantly holding maneuver as a treatment technique are warranted.
different, the total of both differences, reflected in duration At the same time, additional research studies (e.g., mano-
of airway closure, may be significant. This may explain metric and electromyographic studies) in both normal
why, in this study, there was no statistically significant individuals and patients are necessary, in order to better
difference in the onset of arytenoid to epiglottic base understand the physiologic mechanisms underlying the
contact with and without the maneuver, but the duration of tongue-holding maneuver. Such information will help
airway closure was significantly shorter with the maneuver clinicians to select adequate strategies for intervention and
than without the maneuver. appropriate candidates for a particular treatment technique.
Application of the maneuver also resulted in an approxi-
mately 0.1-s increase in pharyngeal delay time. Although
the value was not statistically significant, the difference Acknowledgments
might be clinically important because of the higher risk of The authors would like to express gratitude to Barbara Roa
aspiration. As a matter of fact, in all of the 10 subjects, the Pauloski, Cathy Lazarus, and Joan C. Fox for their assistance in

Fujiu • Logemann 29
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data collection and analyses. This research was supported by Logemann, J. A., Kahrilas, P. J., Cheng, J., Pauloski, B. R.,
National Institute of Health Grants PO1-CA40007-09 and Gibbons, P. J., Rademaker, A. W., & Lin, S. (1992).
R01-NS28525-03. Closure mechanisms of laryngeal vestibule during swallow.
American Journal of Physiology, 262, G338–G344.
McConnel, F. M. S. (1988). Analysis of pressure generation and
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