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1 All authors: Department of Radiology and Ludwig Boltzmann-Institute for Clinical and Experimental Radiologic Research, University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria.
Received June 4, 2001;
accepted after revision September 28, 2001.
Presented at the annual meeting of the American Roentgen Ray Society,
Seattle, April-May 2001.
Abstract
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MATERIALS AND METHODS. At videofluoroscopy, pharyngeal retention was found in 108 (28%; 73 males, 35 females; mean age, 60 years) of 386 patients with a suspected deglutition disorder. Swallowing function was assessed videofluoroscopically. The amount of residual contrast material in the valleculae or piriform sinuses was graded as mild, moderate, or severe. The frequency, type, and grade of aspiration were assessed.
RESULTS. Pharyngeal retention was caused by pharyngeal weakness or paresis in 103 (95%) of 108 patients. In 70 patients (65%) with pharyngeal retention, postdeglutitive overflow aspiration was found. Aspiration was more often found in patients who had additional functional abnormalities such as incomplete laryngeal closure or impaired epiglottic tilting (p < 0.05). Postdeglutitive aspiration was diagnosed in 25% patients with mild, in 29% with moderate, and in 89% with severe pharyngeal retention (p < 0.05).
CONCLUSION. Postdeglutitive overflow aspiration is a frequent finding in patients with pharyngeal retention, and the risk of aspiration increases markedly with the amount of residue. Functional abnormalities other than pharyngeal weakness, such as impaired laryngeal closure, may contribute to aspiration.
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Videofluoroscopic examination of swallowing is a valuable and reliable tool for evaluating the pharyngeal stage of deglutition [7]. To date, no studies examining the clinical relevance of pharyngeal retention in symptomatic patients have been performed. The aim of our study was to evaluate the functional abnormalities associated with pharyngeal retention and the clinical significance of pharyngeal retention in patients with dysphagia.
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Videofluoroscopic Examination Technique
All videofluoroscopic examinations were performed by one of three
radiologists using a fluoroscopy unit (Pantoskop, Siemens, Erlangen, Germany;
and Diagnost 76, Philips, Best, The Netherlands) connected to a videorecorder
(Betacam BVW 75 SP; Sony, Tokyo, Japan). Videofluoroscopic studies were
performed in lateral and anteroposterior projections with the patient in the
upright position. If a patient complained of dysphagia or a globus sensation,
the examination was started with a bolus of 15 mL of high-density (250% grams
per volume) barium suspension (Prontobario; Gerot, Vienna, Austria) in the
lateral view with the field of view centered on the oral cavity and the
pharynx. If the patient had no difficulty in swallowing a 15-mL bolus, the
patient was asked to swallow a bolus of 30 mL of high-density barium with the
field of view centered on the pharyngoesophageal segment. Thereafter, the
patient was asked to take another 15-mL swallow of high-density barium for an
examination of the pharynx in the anteroposterior view. In addition,
double-contrast radiographs of the pharynx in the lateral and anteroposterior
positions were obtained. In patients with suspected aspiration, swallowing
studies were started with 3 mL of thin liquid, nonionic iodinated contrast
material (iopamidol [Gastromiro]; Gerot). If the patient was able to swallow a
bolus of 3 mL, the bolus size was increased to 5, 10, and 15 mL. Thereafter,
this stepwise augmentation of the bolus size was repeated with a highdensity
barium suspension (Prontobario).
The videofluoroscopic studies of all patients were retrospectively analyzed by two radiologists experienced in performing and interpreting modified barium swallowing studies. The videofluoroscopic tapes of all patients were reviewed in real time and slow motion, frame by frame. In addition, all double-contrast spot films of the pharynx were reviewed. The radiographic diagnosis was made by consensus of the two radiologists.
We defined pharyngeal retention as residual material that exceeded a thin mucosal coating in the valleculae or piriform sinuses after swallowing. Depending on the amount of residual material in the valleculae or piriform sinuses, pharyngeal retention was graded on a scale of 1-3, in which 1 represented mild; 2, moderate; and 3, severe pharyngeal retention [4]. Our definitions were as follows: In mild pharyngeal retention, the level of contrast material in the valleculae or piriform sinus constituted less than 25% of the height of the structure. In moderate residue, the level of contrast material constituted between 25% and 50%; and in severe retention, the barium level was higher than 50%. The amount of pharyngeal residue was graded after the first swallow of contrast material. The maximum amount of pharyngeal retention during the entire videofluoroscopic examination was always assessed after the administration of a bolus of a thick liquid barium suspension.
Pharyngeal weakness or paresis was classified as unilateral or bilateral. Weakness or paresis was diagnosed when there was incomplete obliteration of the pharyngeal cavity by the peristaltic pharyngeal contraction [8]. Pharyngeal paresis was suspected when medial movement of the pharyngeal wall was absent or diminished, or when anterior movement of the posterior wall was absent. In addition, appropriateness of oral bolus transportation and tongue thrust, triggering of pharyngeal contraction on swallowing, elevation of the hyoid bone and the larynx, completeness of laryngeal closure, epiglottic tilting, and opening of the pharyngoesophageal sphincter were assessed. Impaired oral bolus transportation and reduced tongue thrust may result in contrast material residue in the valleculae.
Impaired epiglottic movement was defined as absent or incomplete tilting if the epiglottis did not completely invert. Defective laryngeal closure was defined as incomplete or delayed closure of the laryngeal vestibule during swallowing, with air being present or penetration of contrast material into the vestibule. Reduced hyoid elevation was defined as limited superior or anterior movement of the hyoid during the swallow. Laryngeal elevation was considered reduced if the laryngeal elevation did not exceed that of the hyoid during swallowing [9]. Penetration of contrast medium into the upper, subepiglottic portion of the laryngeal vestibule was considered normal [10, 11]. Penetration of contrast material into the lower, supraglottic portion of the larynx and aspiration into the trachea were considered abnormal [11, 12]. Aspiration was classified according to the time of its occurrence as pre-, intra-, or postdeglutitive (before, during, or after swallowing). We assessed the frequency of postdeglutitive overflow aspiration directly related to pharyngeal retention in the piriform sinuses or valleculae. We quantified aspiration by degree of severity: mild, moderate, or severe. Mild aspiration constituted less than 10% of the barium bolus; moderate aspiration, up to 25% of the bolus; and severe aspiration, more than 25% of the bolus [13]. The amount of aspiration was judged primarily in the latteral but also in the anteroposterior view. The maximum amount during the entire examination with several swallows was assessed.
The opening of the pharyngoesophageal sphincter was considered normal if no posterior indentation of the pharyngoesophageal segment occurred during bolus passage [7]. Pharyngoesophageal sphincter dysfunction can be divided into four types: delayed opening, incomplete opening, premature closure, and prolonged opening on swallowing. Other causes of obstruction at the level of the pharyngoesophageal sphincter (cervical osteophytes, strictures, webs) were assessed.
For comparison, we established a control group of 108 consecutive patients (46 men, 62 women; mean age, 51 years) with deglutition disorders who did not exhibit pharyngeal residue at videofluoroscopy.
Statistical Analysis
The relationship between the independent variables and aspiration was
examined with a chi-square test of independence. Logistic regression was used
to identify which factors were the strongest predictors of aspiration.
Univariate logistic regression models were performed to evaluate the influence
of age, amount of pharyngeal retention, presence of concurrent disease,
reduced hyoid elevation, reduced laryngeal elevation, defective laryngeal
closure, and impaired epiglottic movement on aspiration. Odds ratios and 95%
confidence intervals (CIs) were calculated to describe the nonadjusted
relative risk of aspiration. In addition, we performed a stepwise multivariate
logistic regression model to identify which variables significantly increase
the risk of aspiration while the presence of the other factors was controlled.
A chi-square test was used to compare the frequency of aspiration seen in the
study group with that seen in the control group, and the frequency among the
groups of patients with different underlying diseases. A p value of
0.05 or less was considered significant.
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Supraglottic laryngeal penetration or aspiration was found in 100 patients (93%) with pharyngeal retention. In comparison, supraglottic laryngeal penetration or aspiration was found in only 33 patients (31%) without pharyngeal retention (p < 0.0001). In these patients, penetration or aspiration was due to leaking or delayed triggering of pharyngeal contraction, resulting in aspiration before swallowing, or due to incomplete laryngeal closure, resulting in aspiration during swallowing. In 11 patients (10%), penetration of contrast material into the supraglottic portion of the larynx was detected. Aspiration was seen in 89 patients (83%), and was graded minimal in 44%, moderate in 36%, and severe in 20% of patients.
In 70 patients (65%) with pharyngeal residue, postdeglutitive overflow aspiration was found (Figs. 2A,2B,2C and 3A,3B,3C,3D) in three (25%) of 12 patients with mild, in nine (29%) of 31 patients with moderate, and in 58 (89%) of 65 patients with severe pharyngeal retention (p < 0.0001). In the control group of patients without pharyngeal retention, postdeglutitive aspiration was found in three patients (3%) (p < 0.0001).
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No statistically significant relationship was found between unilateral or bilateral pareses or weakness and aspiration. Of 77 patients with bilateral pharyngeal pareses or weakness, 62 patients (81%) were found to aspirate, compared with 23 (88%) of 26 patients with unilateral pharyngeal paresis or weakness.
Aspiration was found in three (50%) of six patients who had no concurrent diseases. Aspiration was detected in 41 (82%) of 50 patients with a neurologic diagnosis, in 24 (89%) of 27 patients who had undergone surgery or radiation therapy for cancer of the pharynx or larynx, and in 21 (84%) of 25 patients with other underlying diseases (not significant).
Table 1 summarizes the relationship between additional functional abnormalities and aspiration in patients with pharyngeal retention. Tables 2 and 3 summarize the results of univariate logistic regression models to describe the nonadjusted relative risk of aspiration in general (Table 2) or of overflow aspiration (Table 3) for the different functional abnormalities. No statistically significant difference between increasing age, underlying diagnosis, and aspiration was found. The stepwise multiple logistic regression model revealed that the amount of residue (odds ratio, 3.72 [95% CI, 2.19-9.92]; p < 0.01) and impaired laryngeal closure (odds ratio, 4.12 [95% CI, 1.24-13.7]; p < 0.05) increase the adjusted risk of aspiration significantly. If other functional abnormalities were included, the prediction of aspiration was not significantly increased, indicating the strong relationship among the different functional abnormalities. For postdeglutitive aspiration, the stepwise multiple logistic regression model revealed that the amount of pharyngeal residue was the only significant factor that increases the risk of aspiration (odds ratio, 8.46 [95% CI, 3.73-19.2; p < 0.0001]. Other factors of impaired deglutition did not increase the prediction of postdeglutitive aspiration.
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Aspiration is the most serious complication during swallowing, which puts the patient at high risk for developing a variety of pulmonary complications such as aspiration pneumonia [5]. Aspiration pneumonia is a major cause of morbidity and mortality, especially among the elderly, with an overall mortality ranging between 20% and 50% [14, 15]. Aspiration is often accompanied by other functional abnormalities of swallowing. Aspiration can result from many causes such as delayed initiation of swallowing, reduced hyoid or laryngeal elevation, defective laryngeal closure, or impaired epiglottic tilting [4]. The differentiation between normal and abnormal airway protection during swallowing is crucial. Robbins et al. [11] showed with the penetration—aspiration scale that entry of contrast material into the airway occurs in 21% of healthy individuals. However, the contrast material remains above the vocal folds and is almost always ejected from the airway before completion of the swallow [11]. On the other hand, deep laryngeal penetration was found to be a predictor of aspiration in symptomatic children [12]. Because of these results, we classified high laryngeal penetration as normal and deep laryngeal penetration and aspiration as abnormal.
Videofluoroscopic swallowing studies are the gold standard for evaluating the pharyngeal phase of swallowing [7, 16, 17]. Videofluoroscopy allows precise assessment of the dynamic aspects of swallowing, especially of the pharyngeal stage of deglutition. The different underlying causes of aspiration can often be identified with videofluoroscopy.
Our results indicate that the amount of pharyngeal retention markedly increases with increasing bolus size and repeated swallowing. In more than 80% of patients, an increase in the amount of pharyngeal retention was seen during the examination after several swallows. These findings emphasize the importance of repeated swallowing and increasing bolus size for development of pharyngeal retention. On the other hand, our results indicate that the risk of bolus aspiration increases considerably with the amount of pharyngeal retention. The risk of postdeglutitive aspiration is negligibly low for patients without pharyngeal retention and very high for patients with moderate to severe pharyngeal residue. In our study, patients with severe pharyngeal retention had a 30 times greater risk of postdeglutitive aspiration than patients without pharyngeal retention.
Another important issue in the examination of patients with pharyngeal retention concerns the viscosity of contrast material used. In patients with a history of aspiration, the examination was begun with thin liquid nonionic iodinated contrast material, because the use of low-osmolar, water-soluble contrast material has been proven to be safe in patients with aspiration [18]. However, aspiration is more likely with thin liquids. Patients who aspirate thin liquids may tolerate thicker consistencies, but pharyngeal retention increases with thicker consistency [19]. Thus, the use of different consistencies during the videofluoroscopic examination yields additional information about different functional abnormalities. In addition, the use of various contrast materials provides important information for developing recommendations for feeding and food consistency. In our study, the maximum amount of pharyngeal retention was always assessed after administration of a bolus of thick liquid barium so that conditions would be uniform for all patients. However, we did not study the effects of bolus consistency on the amount of residue, which may affect swallowing function.
Different mechanisms responsible for the development of pharyngeal retention after swallowing have been identified with videomanometry [2, 20]. The development of pharyngeal residues was found to be influenced by different quantitative parameters, including a low tongue-driving force, reduced pharyngeal shortening, and reduced amplitude of pharyngeal contraction [2, 20, 21].
One limitation of our study is the relatively high age of our patients (mean, 60 years), which makes the differentiation between normal aging and functional abnormalities difficult [13]. Therefore, we cannot exclude the possibility that in some of our patients pharyngeal abnormalities may reflect an aging phenomenon of the pharynx and may have no clinical relevance. However, pharyngeal retention is likely to gain clinical relevance if it leads to aspiration.
In general, the observation of aspiration during the videofluoroscopic examination is limited because of the controlled condition and the limited time under which videofluoroscopic examinations are typically performed [4]. Clinically apparent aspiration may be missed during a videofluoroscopic examination. However, even with these limitations, videofluoroscopy is the standard of reference for detecting aspiration [22, 23].
Another limitation of our study is that no long-term follow-up of the patients was available to identify all patients who developed aspiration pneumonia. Therefore, the true incidence of aspiration pneumonia in patients with pharyngeal retention is unknown. However, the significance of dysphagia or aspiration as an important risk factor for aspiration pneumonia is well established [5].
In conclusion, the presence and, in particular, the amount of pharyngeal retention are important risk factors for the occurrence of postdeglutitive aspiration. The clinician must pay attention to the high risk of aspiration in patients with pharyngeal residue found during swallowing studies.
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