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GASTROENTEROLOGY 2002;122:1314 –1321
REZA SHAKER, CARYN EASTERLING, MARK KERN, TERILYNN NITSCHKE, BENSON MASSEY,
STEPHANIE DANIELS, BARBARA GRANDE, MARTA KAZANDJIAN, and KAREN DIKEMAN
MCW Dysphagia Institute, Division of Gastroenterology and Hepatology, Digestive Disease Center, Medical College of Wisconsin and
Zablocki VA Medical Center, Milwaukee, Wisconsin
Background & Aims: We evaluated the effect of a novel diseases, neuromuscular disorders, and therapy for head-
rehabilitative exercise on restoration of deglutition in a and-neck cancers. Failure of normal deglutition may
group of patients with deglutitive failure caused by ab- cause symptoms of dysphagia, coughing, and choking,
normal upper esophageal sphincter (UES) opening man- leading to malnutrition, pneumonia, and asphyxia.
ifested by postswallow residue and aspiration necessi- Separating the oropharynx and esophagus, the upper
tating percutaneous tube feeding. Methods: We studied
esophageal sphincter (UES) serves as a critical gateway in
a total of 27 patients by videofluoroscopy and functional
the coordination of breathing and swallowing. Between
assessment of swallowing scores before and after 6
weeks of a head-raising exercise program. Seven of 27 swallows, the UES prevents air entry into the digestive
patients, assigned randomly, participated in a sham tract during respiration and speech. However, during
exercise before entering the tested exercise program. swallows the cricopharyngeus muscle, the main compo-
Eleven of 27 were randomized to the real exercise pro- nent of the UES, relaxes and is pulled open forcibly by
gram. Results: Although there was no change in swallow the contraction of suprahyoid muscles such as mylohy-
function and biomechanics after the sham exercise, oid, geniohyoid, and digastric involved in UES open-
following 6 weeks of real exercise, all 11 patients exhib- ing.9,10 In a variety of pathologic conditions,11 including
ited a significant improvement in their UES opening, cerebrovascular accident, brainstem lesions, central de-
anterior laryngeal excursion (P < 0.01), as well as res- generative disorders, posterior cerebellar artery thrombo-
olution of postdeglutitive aspiration and were able to sis, and bulbar paralysis, the UES opening is inadequate
resume oral feeding. Similar results were found when and acts as a relative resistor to bolus flow out of the
the 7 patients in the sham group were crossed over to
pharynx. This, in turn, may result in postswallow residue
the real exercise group. Comparison of before and after
exercise values for anteroposterior UES opening (P <
and aspiration.
0.01) and laryngeal anterior excursion (P < 0.05), as The possibility of decreasing the resistance to bolus
well as functional outcome assessment of swallowing flow by increasing the deglutitive UES opening through
(P < 0.05) in the entire group of 27 patients also exercise aimed at the suprahyoid UES opening muscles
showed significant improvement. Etiology and duration was recently shown in a group of asymptomatic elderly
of dysphagia did not affect the outcome. Conclusions: who were found to have a significantly smaller UES
The proposed suprahyoid muscle strengthening exercise opening compared with young individuals.12 This study
program is effective in restoring oral feeding in some reported that after 6 weeks of an isometric-isokinetic
patients with deglutitive failure because of abnormal head-lift exercise, performed 3 times a day, there was a
UES opening. significant increase in UES anteroposterior opening di-
ameter and a significant decrease in hypopharyngeal in-
bnormalities of swallowing are common especially trabolus pressure; a marker of resistance to flow.13,14
A among elderly individuals1– 8 and may involve the
preparatory, oropharyngeal, or esophageal phases of swal-
The present study was undertaken to evaluate the
effect of this exercise on the deglutitive biomechanical
lowing. Normal deglutition requires an elaborate coor-
dination of neuromuscular activity to achieve passage of Abbreviations used in this paper: FOAMS, functional outcome as-
the swallowed material from the oropharynx into the sessment of swallowing; UES, upper esophageal sphincter.
© 2002 by the American Gastroenterological Association
esophagus while avoiding aspiration. Disorders of deglu- 0016-5085/02/$35.00
tition are common sequelae of central nervous system doi:10.1053/gast.2002.32999
May 2002 SWALLOW REHABILITATION EXERCISE 1315
events and functional outcome of swallowing in a group in a sham or real exercise protocol. The patients were random-
of patients with deglutitive failure because of abnormal ized by choosing an envelope that gave written directions for
UES opening manifested by postswallow residue and an exercise to be performed 3 times per day for the following
aspiration necessitating percutaneous tube feeding. 6 weeks. The enrolling speech-language pathologist was aware
of the randomly chosen exercise. The same speech pathologist
Materials and Methods performed the functional outcome assessment of swallowing
(FOAMS). The investigators that performed the videofluoro-
We studied a total of 27 consecutive outpatients (age scopic data analysis, however, were blinded to the assigned
range, 62– 89 years) with a median age of 72 years with exercise group. The enrolling speech pathologist observed the
pharyngeal phase dysphagia secondary to abnormal upper patients as they demonstrated the written exercise format and
esophageal sphincter opening because of a variety of causes. sequence. The speech pathologist gave them written exercise
Patients were enrolled in the study at the Veterans Adminis- instructions to follow while at home and a log on which to
tration Hospital, Froedtert Memorial Lutheran Hospital, and record completion of the exercise sequence 3 times per day for
St. Joseph’s Hospital. Studies were approved by the Human
6 weeks. The sham exercise comprised 15 repetitions of passive
Research Review Committee of the Medical College of Wis-
tongue lateralization performed 3 times a day for 6 weeks. The
consin and other respective institutions, and subjects gave
real exercise was performed as previously described.12 Briefly,
informed consent before their studies. Patients were enrolled in
the patients were instructed to lie flat on the bed or floor and
the study if they met the predetermined criteria for abnormal
perform 3 sustained head raisings for 1 minute in the supine
UES opening, namely, postswallow residue and aspiration and
position, interrupted by a 1-minute rest period. These sus-
were able to independently perform the exercise. Because of the
tained head-raisings were followed by 30 consecutive repeti-
severity of their dysphagia, 18 of 27 patients were fed by
gastrostomy and 9 by jejunostomy tubes. Tube-fed patients tions of head raisings in the same supine position. For both
resided in their homes. Patients with a history of cervical spine sustained and repetitive head raisings, participants were in-
surgery, inability to independently perform the exercise, and structed to raise their head high and forward enough to be able
patients with tracheostomy were excluded from the study. to observe their toes without raising their shoulders off the
Demographics for the patients included in the study are shown floor or bed. Both the sham and real exercises were performed
in the Table 1. Patients were randomized to either participate 3 times a day for a 6-week period. Although there was no
direct observation of patient exercise performance at home, the
patients recorded daily exercise participation on a log that was
Table 1. Patient Demographics returned to the enrolling speech pathologist when the exercise
Duration of was completed.
Patient Gender Age Etiology of dysphagia dysphagia On the day before and the day after completion of 6 weeks
JA M 69 Right CVA 42 days
of exercise, each participant’s deglutitive function was evalu-
FB M 65 Left carotid endarterectomy 42 days ated in the upright position using videofluoroscopy in lateral
WB M 76 Left CVA 30 days and anteroposterior projections during 3 dry and 3 barium
AD M 76 Right CVA 240 days swallows of 5-mL each. For calibration of videofluoroscopic
WD M 66 Pharyngeal radiation 150 days
measurements and to compensate for possible magnification
RG M 82 Myocardial revascularization 18 days
HG M 74 Brainstem stroke 10 days error, before each study a 4-mm diameter catheter with 3
DG M 78 Pharyngeal radiation 2880 days tantalum markers 3 cm apart was placed on the skin in the
FH M 79 Left carotid endarterectomy 107 days pharyngo-UES region and videotaped for subsequent spacial
EK M 67 Pharyngeal radiation 1080 days calibration of distance measurements.
RK M 76 Brainstem stroke 150 days
CL M 62 Right CVA 120 days
For videofluoroscopic recordings, the subjects were in-
GM M 89 Brainstem stroke 10 days structed to hold their head in a neutral position. Videofluoro-
MM M 83 Brainstem stroke 12 days scopic recordings were obtained at 90 keV, using a 9-inch
GM M 72 Left CVA 73 days image-intensifier mode and appropriate collimation so that an
WM M 65 Right CVA 90 days
image was obtained of the posterior mouth, pharynx, and
DM M 76 Myocardial revascularization 100 days
RM M 68 Pharyngeal radiation 9 days pharyngoesophageal region. Fluoroscopic images were re-
PK M 75 Pharyngeal radiation 61 days corded on a super-VHS videocassette recorder (AG-1960 Pro-
DP F 72 Pharyngeal radiation 540 days line; Panasonic, Tokyo, Japan), which recorded 30 frames/60
MR F 72 Suboccipital meningioma 240 days fields/s. Fluoroscopic recordings were timed using a specially
LS M 74 Brainstem stroke 210 days
GT M 64 Brainstem stroke 120 days designed timer. The output of the timer provided a video-
TT M 76 Brainstem stroke 180 days displayed time signal in hundredths of a second superimposed
LV M 71 Right carotid endarterectomy 30 days on the videofluoroscopic images. The videofluoroscopic record-
RW M 76 Right CVA 180 days ings were subsequently digitized and analyzed in a blinded
HW M 78 Right CVA 270 days
fashion with respect to group identity (real or sham) and
CVA, cerebrovascular accident. exercise status (before or after exercise). To determine the
1316 SHAKER ET AL. GASTROENTEROLOGY Vol. 122, No. 5
interobserver reproducibility, the data were subsequently re- Table 2. FOAMS Scoring Scale
analyzed by a second individual in a similar blinded fashion. FOAMS
The computer analysis system used for analyzing the video- score Description
fluoroscopic data consisted of a 486 IBM-compatible computer 1 Profound
operating at 33 MHz. The computer system drives an analog- Patient is NPO
to-digital conversion board and program specifically designed Requires enteral or paraenteral feeding to maintain
for image capture and analysis. The image-analysis and capture adequate nutrition and hydration
Profoundly impaired airway protection
software (JAVA, Jandel Scientific, San Mateo, CA) allows
2 Severe
capture of standard raster scan video images and morphological Primary mode of nutrition and hydration is non-oral
analysis of digitized image data. The digitized images are Oral intake is limited to therapeutic feeding/directed
stored as computer files for any subsequent recall or analysis. swallowing therapy supervised by speech pathologist
Using these techniques we measured (1) the anteroposterior due to severely impaired airway protection
3 Moderately/severe
and lateral diameters of the UES opening during 5-mL liquid
Partially dependent on non-oral enteral/paraenteral
barium swallows, taken from the narrowest area within the feeding for nutrition and hydration
pharyngoesophageal junction when this area became maxi- Fairly safe swallowing only when diet consistency and/
mally opened during bolus transit across the sphincter; (2) or liquid consistency is modified
maximum superior and anterior excursion of hyoid bone and Inconsistently utilizes compensatory swallowing
strategies even with close supervision or constant
maximum superior and anterior excursion of the larynx during
cuing
5-mL barium swallows; (3) height and width of pyriform sinus 4 Moderate
residue; and (4) presence or absence of aspiration. Primary mode of nutrition and hydration is oral
The clinical effect of exercise on swallowing was evaluated May require non-oral supplements
using the FOAMS from the Wisconsin Speech Language Pa- Safe swallowing function only when diet consistency
and/or liquid consistency is modified
thology and Audiology Association.15 In this scoring system a
Inconsistently utilizes compensatory swallowing
numerical score of 1 to 7 is assigned to each participant’s level strategies even with close supervision or constant
of swallowing competency, that is a score of 1 being the worst cuing
and 7 the best score corresponding to functional swallowing 5 Mild/moderate
(Table 2). Primary mode of nutrition and hydration is oral
Safe swallowing function only when diet consistency
Several months into the exercise enrollment period, the
and/or liquid consistency is modified
enrolling speech pathologist’s clinical observation of the pa- Requires compensatory swallowing strategies with
tient’s ability to handle and clear secretions demonstrated constant supervision
significant improvement in the patients performing the real Additional time usually necessary for meals because of
exercise, but not in the group performing the sham exercise. use of swallowing strategies
6 Mild
For this reason, a decision was made not to enroll additional
Safe and efficient swallowing only when diet
patients in the sham exercise group. Seven patients had been consistency and/or liquid consistency is modified
enrolled in the sham exercise group, and 11 patients were May require compensatory swallowing strategies with
enrolled in the real exercise group at this point. Patients who occasional cueing
had completed 6 weeks of sham exercise then participated in 6 Additional time usually necessary for meals because of
use of swallowing strategies
weeks of the real exercise program. Therefore, a total of 27
7 Functional
patients had completed 6 weeks of the real exercise, 7 of whom Safe and efficient swallowing of thin liquids and diet
had completed the sham exercise before doing the real exercise. that may be modified for dentition or digestive needs
Statistical analyses were performed using parametric and Adequate airway protection
nonparametric testing. The effect of the exercise on the mea- Requires no cueing to utilize compensatory swallowing
strategies
sured biomechanical parameters were tested using 2-way anal-
Additional time may be required during meals to ensure
ysis of variance (ANOVA) with repeated measures to account safe intake
for both intrasubject variability and the exercise effect.
FOAMS Scores were compared using the Wilcoxon signed
rank test. Normality was tested using Kolmogorov–Smirnov
analysis. Significance of P ⬍ 0.05 and power of 0.8 were used minor degree of anterior neck muscle discomfort during
as statistical criteria for rejecting the null hypothesis and the first few days of real exercise. However, the discom-
analysis of type II error. Data in the text are presented as fort was not severe enough to result in discontinuation of
means ⫾ SE unless stated otherwise. the exercise by any of the patients, and it resolved
spontaneously.
Results Comparison of the Sham and Real Exercise
All 27 patients successfully completed the exer- At the time of terminating the enrollment in the
cise protocols. Invariably, the patients reported some sham exercise group, as explained in the Materials and
May 2002 SWALLOW REHABILITATION EXERCISE 1317
NOTE. Numbers in bold type represent patients who were enrolled within 3 weeks of their cerebrovascular accident.
tribution to the rehabilitation of swallow function. This tion of the anterior neck muscles involved in UES open-
approach can potentially result in improvement of qual- ing.
ity of life and cost savings in managing some dysphagic The exercise used in the present study is another
patients in the acute and chronic care settings. example of physiological manipulation of the striated
Opening of the UES during swallowing is determined muscle group involved in deglutition to augment yet
by the combined effect of relaxation and distensibility of another aspect of UES opening, namely UES diameter
the cricopharyngeus muscle and retraction of the cricoid and to improve oropharyngeal swallowing.
cartilage caused by contraction of the suprahyoid muscle A direct comparison of the efficacy of our proposed
group involved in UES opening.9,10,16 –19 The relative exercise and the Mendelsohn maneuver is not currently
contribution of these individual factors to UES opening, available. Based on our experience, the exercise protocol
as well as the relative significance of malfunction of these is easier for the patient to learn and follow. Given the fact
factors to disordered UES opening, has not been quan- that the Mendelsohn maneuver primarily increases the
tified. Among the 3 previously mentioned factors, only duration of UES opening and our proposed exercise
the suprahyoid muscle group appears to be accessible to increases the magnitude of the UES opening, it is con-
external noninvasive manipulation, such as an exercise. ceivable that they may be helpful for different indica-
Although the exact muscles that were trained by the tions. Comparative studies are currently awaited to ad-
tested exercise program were not determined in this dress these issues.
study, significant increase in the anteroposterior diame- It is worth noting that although the patients partici-
ter of the UES opening, along with a significant increase
pating in the present study were extensively instructed
in anterior excursion of the thyroid cartilage, suggests
on performing the exercise, their actual exercise during
that the UES opening muscles, including the mylohyoid/
the 6-week period was not supervised. Day-to-day vari-
geniohyoid muscle group, and possibly the anterior seg-
ability in compliance and effort cannot be excluded and
ment of the digastric muscle, were involved in the exer-
might have influenced the outcome.
cise performed by these dysphagic patients. This notion
Time-related improvements in swallowing indepen-
is supported by the previous documentation of fatigue in
dent of exercise-related improvements were not system-
suprahyoid muscles during the isometric part of the
proposed exercise using spectral analysis of surface elec- atically evaluated in this study and represented a possible
tromyographic recordings.20 –22 source of error. Given the long-standing and severe dys-
Functional rehabilitation for activities of daily living phagia exhibited by most of the patients in this study,
of the arms and legs after stroke, surgery, radiation, or along with the patients’ unresponsiveness to conven-
accident is well documented. However, swallow rehabil- tional treatment modalities, time-related improvement
itation has lagged behind other advances in the rehabil- alone seems to be an unlikely explanation for the docu-
itation field. Volitional control of UES opening muscles mented improvement. This notion is further supported
has been previously used in Mendelsohn’s maneuver to by the lack of improvement in the sham exercise group.
prolong the superior and anterior excursion of the larynx In summary, the suprahyoid muscle strengthening
and thus improve swallowing efficiency. This maneuver exercise program was shown to be effective in restoring
has been found to result in prolongation of the duration oral feeding in a small group of patients with deglutitive
of the UES opening during swallowing.23 failure caused by abnormal UES opening. Although the
Mendelsohn’s maneuver is performed by voluntarily proposed exercise was successful in restoring oral intake
holding the larynx at the apogee of its deglutitive ex- in this group of patients with a diverse etiology and
cursion after swallowing. This maneuver differs from the duration of dysphagia, a larger clinical trial with a long-
exercise described in this article. The exercise described term follow-up period, is necessary to further evaluate
in this study is performed without the involvement of the clinical efficacy and indications of this exercise in
swallowing and includes isotonic and isokinetic contrac- various patient groups.
May 2002 SWALLOW REHABILITATION EXERCISE 1321