Videofluoroscopic Assessment of Patients with Dysphagia: Pharyngeal Retention Is a Predictive Factor for Aspiration

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1 Edith Eisenhuber 1 Wolfgang Schima Ewald Schober Peter Pokieser Alfred Stadler Martina Scharitzer Elisabeth Oschatz Received June 4, 2001; accepted after revision September 28, Presented at the annual meeting of the American Roentgen Ray Society, Seattle, April May 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. Address correspondence to E. Eisenhuber. AJR 2002;178: X/02/ American Roentgen Ray Society Videofluoroscopic Assessment of Patients with Dysphagia: Pharyngeal Retention Is a Predictive Factor for Aspiration OBJECTIVE. This study evaluated the clinical significance of pharyngeal retention to predict aspiration in patients with dysphagia. 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. P haryngeal residue in the valleculae and in the piriform sinuses after swallowing is seen in up to 20% of elderly asymptomatic individuals [1]. It is not clear whether the occurrence of pharyngeal retention in these patients is a normal finding caused by aging or whether it should be considered abnormal [1, 2]. Nevertheless, an increased pharyngeal residual volume represents the cardinal feature of impaired or incomplete pharyngeal bolus transportation [3, 4]. A potentially severe complication of pharyngeal retention is overflow bolus aspiration into the airways after swallowing [3, 4]. Aspiration is the most serious abnormality during videofluoroscopic examination; it can lead to pulmonary complications such as aspiration pneumonia [5, 6]. 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. Materials and Methods Patients From October 1998 to July 2000, 386 consecutive patients (199 males, 187 females; mean age, 51 years) with symptoms indicative of a deglutition disorder were referred to our department for a videofluoroscopic study of the pharynx and esophagus. Videofluoroscopic and clinical findings and demographic data for all patients were prospectively entered into a computer database (Excel 97; Microsoft, Redmond, WA). Through retrospective review of the computer database, we identified 108 patients (28%) with pharyngeal residue seen at videofluoroscopy. The patients were 73 males and 35 females with an age range of years. The presenting symptom was dysphagia in 42 patients (for solids in 27, for solids and liquids in 14, for liquids only in one), suspected aspiration in 58, globus sensation in five, noncardiac chest pain in two, and nasal regurgitation in one patient. Duration of symptoms ranged from 1 week to 20 years. Underlying diseases or conditions that are known to cause deglutition disorders were found in 102 patients (94%). Thirteen patients had a AJR:178, February

2 Eisenhuber et al. history of stroke, seven patients had prior closed head trauma, seven had Parkinson s disease, two had myasthenia gravis, and 21 had other neurologic diseases. Twenty-seven patients had undergone surgery or radiation therapy for cancer of the floor of the mouth, the larynx, or pharynx, and eight had had surgery for benign or malignant stricture of the esophagus. Four patients had progressive systemic sclerosis, three had undergone thyroidectomy, two had surgery for Zenker s diverticula, and eight patients had other nonneurologic diagnoses. 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 lateral 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. Results Overall, pharyngeal paresis or weakness was present in 103 (95%) of 108 patients with pharyngeal retention. Pharyngeal paresis or weakness was unilateral in 26 patients (25%) (Fig. 1) and bilateral in 77 patients (75%). Overall, pharyngeal residue was found in 89 patients (82%) after the first swallow, which was graded as mild in 63%, moderate in 33%, and severe in 4% of patients. In 89 patients (82%), an increase in the amount of pharyngeal retention was seen with increasing bolus size or repeated swallowing. The maximum amount of pharyngeal retention during the entire examination was graded as mild in 11%, moderate in 29%, and severe in 60% of patients. In 89 patients (82%), pharyngeal residue was present in piriform sinuses and valleculae; in 10 patients (10%), exclusively in the valleculae; and in nine patients (8%), only in piriform sinuses. 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 < ). 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 394 AJR:178, February 2002

3 Videofluoroscopy of Dysphagia (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. 2 and 3) 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 < ). In the control group of patients without pharyngeal retention, postdeglutitive aspiration was found in three patients (3%) ( p < ). 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, ]; p < 0.01) and impaired laryngeal closure (odds ratio, 4.12 [95% CI, ]; 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, ; p < ]. Other factors of impaired deglutition did not increase the prediction of postdeglutitive aspiration. Discussion Pharyngeal residue after swallowing is a frequent finding during videofluoroscopic examination; it can be seen in up to 20% of the elderly population [1]. However, the clinical significance of this observation in patients without dysphagia remains controversial. Ekberg and Feinberg [1] concluded that elderly patients without dysphagia have altered swallowing function caused by normal aging without impairment. Dejaeger et al. [2] investigated the mechanisms involved in postdeglutition retention in the nondysphagic elderly and concluded that limited retention should be considered normal in the very elderly patient (mean age of 80 years) and usually is not accompanied by aspiration. The distinction between altered function due to normal aging and altered function due to disease in symptomatic patients is not always clear, because there are often discrepancies between the presenting symptoms and the functional pharyngeal abnormalities in these patients [13]. Nevertheless, an increase in the A Fig year-old woman with postpolio syndrome. A, Videofluoroscopy in lateral view shows severe pharyngeal retention of contrast material in piriform sinus (arrow ) but no aspiration of contrast material into trachea. B, Videofluoroscopy in anteroposterior direction shows dilatation of left piriform sinus with severe retention (arrow ) caused by left-sided pharyngeal paresis. Note minimal penetration of contrast material into laryngeal vestibule (arrowhead ). amount of residue remaining in the pharynx after swallowing is due primarily to impairment of pharyngeal bolus transportation, which predisposes the patient to develop postdeglutitive aspiration [3, 4]. 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 B AJR:178, February

4 Eisenhuber et al. A Fig year-old man with long-standing dysphagia for solids and liquids and history of radiation therapy of neck for Hodgkin s lymphoma. A, Lateral double-contrast pharyngogram shows severe pharyngeal retention of contrast material in piriform sinuses (arrow ) caused by radiation stricture at pharyngoesophageal segment (arrowhead ). B, Videofluoroscopy shows absence of anterior movement of posterior pharyngeal wall, indicative of pharyngeal paresis. Note severe postdeglutitive overflow aspiration of retained contrast material into trachea (arrow ). C, Double-contrast pharyngogram in anteroposterior view shows stricture (arrowhead ) and severe retention in piriform sinuses (white arrow ), resulting in aspiration. Aspirated contrast material in larynx and trachea is seen in midline (black arrow ). TABLE 1 Pharyngeal Residue After Swallowing: Relationship Between Functional Abnormalities and Aspiration Functional Finding No. of Patients No. (%) Who Aspirated p a Oral bolus transportation Normal (82) Impaired (84) NS Hyoid bone elevation Normal (77) Reduced (97) < 0.05 Laryngeal elevation Normal (76) Reduced or absent (97) < 0.05 Laryngeal closure Complete (66) Incomplete (93) < 0.01 Epiglottic tilting Normal (72) Impaired or absent (93) < 0.05 Opening of the pharyngoesophageal sphincter Normal (88) Abnormal (71) NS Total (82) Note. NS = not significant. a Chi-square test of independence. B [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. C 396 AJR:178, February 2002

5 Videofluoroscopy of Dysphagia C A Fig year-old man with dysphagia for solid food and occasional aspiration. A, During swallowing, videofluoroscopy reveals only minimal pharyngeal contraction (white arrow ) and incomplete laryngeal closure, with intradeglutitive penetration of contrast material (black arrow ). B, After swallowing, residue of contrast material is seen in larynx (black arrow ). Note also severe retention of contrast material in piriform sinuses (white arrow ), with aspiration into trachea (arrowhead ). C, At a later stage, contrast material that penetrated into larynx has also been aspirated (arrowheads). D, In anteroposterior view, videofluoroscopy reveals bilateral dilatation of piriform sinuses with retention (arrow ). Contrast material outlines vocal cords (arrowheads) and trachea. 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]. B D AJR:178, February

6 Eisenhuber et al. TABLE 2 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. References Predictive Factors for Aspiration (Before, During, and After Deglutition) Variable Odds Ratio 95% Confidence Interval p Amount of pharyngeal retention < Reduced hyoid bone elevation < 0.05 Reduced laryngeal elevation < 0.05 Defective laryngeal closure < Impaired epiglottic movement < 0.01 TABLE 3 Note. NS = not significant. Predictive Factors for Overflow Aspiration (After Deglutition) Variable Odds Ratio 95% Confidence Interval p Amount of pharyngeal retention < Reduced hyoid bone elevation < 0.05 Reduced laryngeal elevation < 0.05 Defective laryngeal closure NS Impaired epiglottic movement < Ekberg O, Feinberg MJ. Altered swallowing function in elderly patients without dysphagia: radiologic findings in 56 cases. AJR 1991;156: Dejaeger E, Pelemans W, Ponette E, Joosten E. Mechanisms involved in postdeglutition retention in the elderly. Dysphagia 1997;12: Dodds WJ, Logemann JA, Stewart ET. Radiologic assessment of abnormal oral and pharyngeal phases of swallowing. AJR 1990;154: Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia 1994;9: Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia 1998;13: Feinberg MJ, Ekberg O. Videofluoroscopy in elderly patients with aspiration: importance of evaluating both oral and pharyngeal stages of deglutition. AJR 1991;156: Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR 1990;154: Olsson R, Nilsson H, Ekberg O. Simultaneous videoradiography and computerized pharyngeal manometry: videomanometry. Acta Radiol 1994;35: Ekberg O. The normal movements of the hyoid bone during swallow. Invest Radiol 1986;21: Ekberg O, Nylander G. Cineradiography of the pharyngeal stage of deglutition in 150 individuals without dysphagia. Br J Radiol 1982;55: Robbins J, Coyle J, Rosenbek J, Roecker E, Wood J. Differentiation of normal and abnormal airway protection during swallowing using the penetration aspiration scale. Dysphagia 1999;14: Friedman B, Frazier JB. Deep laryngeal penetration as a predictor of aspiration. Dysphagia 2000; 15: Frederick MG, Ott DJ, Grishaw EK, Gelfand DW, Chen MYM. Functional abnormalities of the pharynx: a prospective analysis of radiographic abnormalities relative to age and symptoms. AJR 1996;166: Pick N, McDonald A, Bennett N, et al. Pulmonary aspiration in a long-term care setting: clinical and laboratory observations and an analysis of risk factors. J Am Geriatr Soc 1996;44: Bryan CS, Reynolds KL. Bacteremic nosocomial pneumonia: analysis of 172 episodes from a single metropolitan area. Am Rev Respir Dis 1984; 129: Jones B, Donner MW. Examination of the patient with dysphagia. Radiology 1988;167: Levine MS, Rubesin SE. Radiologic investigation of dysphagia. AJR 1990;154: Auffermann W, Geisel T, Wohltmann D, Gunther RW. Tissue reaction following endobronchial application of iopamidol and ioxithalamate in rats. Eur J Radiol 1988;8: Jones B, Donner M. The tailored examination. In: Jones B, Donner M, eds. Normal and abnormal swallowing. New York: Springer, 1991: Kahrilas PJ, Logemann JA, Lin S, Ergun GA. Pharyngeal clearance during swallowing: a combined manometric and videofluoroscopic study. Gastroenterology 1992;103: Olsson R, Castell J, Johnston B, Ekberg O, Castell DO. Combined videomanometric identification of abnormalities related to pharyngeal retention. Acad Radiol 1997;4: Groher ME. The detection of aspiration and videofluoroscopy. (editorial) Dysphagia 1994;9: Langmore SE, Schatz K, Olson N. Endoscopic and videofluoroscopic evaluations of swallowing and aspiration. Ann Otol Rhinol Laryngol 1991; 100: AJR:178, February 2002