Fluoroscopic Swallowing Study in Elderly Patients Admitted to a Geriatric Hospital and a Long-Term Care Facility

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1 Original Article DOI: /jkgs Fluoroscopic Swallowing Study in Elderly Patients Admitted to a Geriatric Hospital and a Long-Term Care Facility Sang Jun Kim, MD, Tai Ryoon Han, MD Department of Rehabilitation Medicine, Seoul National University College of Medicine, Seoul, Korea Background: No study has been done to detect the aspiration using the videofluoroscopic swallowing study in the elderly patients. Elderly patients admitted to hospitals or long-term care facilities may intake the food orally without any evaluation of swallowing function and may be exposed to aspiration risk, which can be eliminated by some diet modification based on the fluoroscopic findings. Methods: Sixty-three elderly patients who had an oral-feeding status were recruited in this study. They swallowed diverse food textures twice in the following order; liquid, Yoplait yogurt, pudding, soft-bland diet, and a regular diet. Swallowing parameters were checked as subglottic aspiration, supraglottic penetration, delayed pharyngeal reflex, and vallecular and pyriform sinus residues. Results: Only 2 patients showed both aspiration signs and the subglottic aspiration in the fluoroscopic study. Six patients showed the subglottic aspiration in the fluoroscopic study without any clinical sign. Seven patients who complained of aspiration signs did not show the subglottic aspiration, but all of them presented the supraglottic penetration. Multivariate logistic regression analysis showed that no covariate was correlated with the subglottic aspiration whereas delayed pharyngeal reflex during liquid (p<0.001) or Yoplait (p=0.010) swallowing were correlated with aspiration plus penetration. Conclusion: This study demonstrates that a fluoroscopic swallowing study is important for the dysphagia diagnosis in elderly patients because of no significant correlation between the aspiration signs assessed clinically and the subglottic aspiration detected by the fluoroscopic swallowing study. Diet modifications, such as, liquid thickening will be necessary when patients demonstrate the evidence of subglottic aspiration during swallowing. Key Words: Deglutition, Fluoroscopy, Geriatrics INTRODUCTION Dysphagia is a common problem in geriatric medicine. Swallowing in the elderly is characterized by slow hyoid movement, delayed pharyngeal reflex 1), and vallecular and pyriform sinus residues caused by muscular weakness 2). Frequencies of piecemeal deglutition, premature loss of liquid, oral and pharyngeal residues, and laryngeal penetration are significantly greater in dentate elderly persons 3). These characteristics dispose the elderly to develop dysphagia, especially in the pharyngeal phase, a condition in which a young patient will not show dysphagia. Common diseases among the elderly, such as small vessel, Alzheimer s and Parkinson s disease, also in- Received: Jul 16, 2009 Revised: Set 15, 2009 Accepted: Set 25, 2009 Address for correspondence: Tai Ryoon Han, MD, PhD Department of Rehabilitation Medicine, Seoul National University College of Medicine, 28 Yeongun-dong, Jongro-gu, Seoul , Korea Tel: , Fax: , guitar1@snu.ac.kr *This study was supported by a research fund from the Korean Geriatric Society in J Korean Geriatr Soc 13(4) Dec

2 crease the risk of dysphagia 4). Moreover, the decreased defense systems (e.g., decreased immunity and reduced pulmonary clearance), increase the risk of aspiration pneumonia 5). Therefore, pharyngeal dysphagia is an important health issue in the elderly. In a chart review, Lin et al. 6) found that the prevalence of impaired swallowing was 31.9% among non tube-fed subjects in nursing and intermediate care facilities in Taiwan. Kawashima et al. 7) found a 13.8% prevalence rate of dysphagia by means of a questionnaire to screen community-dwelling elderly in the northern region of Honshu Island, Japan. Roy et al. 8) showed the prevalence of swallowing disorder to be 33% of the 117 seniors living independently in Utah and Kentucky via an interview questionnaire. However, none of these authors performed a videofluoroscopic swallowing study, considered the gold standard for diagnosing dysphagia. This is important because silent aspiration, which is difficult to detect by questionnaire, occurs in up to 30% of dysphagic patients 9). Moreover, this topic will be of increasing concern as the number of geriatric hospitals and long term care facilities increase in many countries. Methods for managing pharyngeal dysphagia are diverse. Changing food consistency and texture (e.g., by adding food thickeners) is one example. It is generally believed that food viscosity is inversely proportional to the likelihood of laryngeal penetration or aspiration in dysphagic patients because the fast movement of food with low viscosity induces penetration or aspiration, whereas the slow movement with high viscosity will not do so in patients with delayed pharyngeal reflex. Lending support to this hypothesis is an earlier study 10), which revealed that increasing bolus viscosity greatly improves swallowing function in patients with neurological problems. However, another study 11) showed that there was more pharyngeal retention with ultra-thick liquids, like pudding, than with apple juice or apricot nectar, suggesting that high viscosity increased pharyngeal retention. Postdeglutitive overflow aspiration is found frequently in patients with pharyngeal retention, and the risk of aspiration increases markedly with increasing residual amount 12). Thus, increasing viscosity is not always a safe option in dysphagic patients. With age, elderly patients show decreased swallowing capacity, delayed triggering of the pharyngeal swallow, and significant vallecular and pyriform sinus residue 2). Thus, it is important to know the effects of swallowing parameters, including pharyngeal reflex delay and residue amount, on the risk of aspiration in elderly patients by using a fluoroscopic study. Elderly patients admitted to hospitals or long-term care facilities have diverse diseases, and may show dysphagia from underlying diseases or an unknown cause. Oral feeds may be given without evaluating the swallowing function, exposing them to the risk of aspiration, which can be eliminated by diet modification based on fluoroscopic findings. Therefore, the aim of this study was to compare subglottic aspiration detected by fluoroscopy with the aspiration signs seen clinically in elderly patients being fed orally at a geriatric hospital and a long term care facility and to find the swallowing parameters that correlate with aspiration and penetration. MATERIALS AND METHODS 1. Subjects From the inpatients at a local geriatric hospital and residents at a long-term care facility, 63 subjects were recruited in February 2005 in Gyeonggi do, Korea. Selected subjects had oral-feed statuses, and were competent enough to understand the purpose of this study and to agree to participate. All subjects provided informed consent for this study. The subjects comprised 43 women and 20 men with an average age of 76.0 ±7.0 years, and had various diagnoses (stroke-19; dementia-7; Parkinsonism-5; low back pain-4; arthritis-3; hip joint fracture-3; others-6; no identifiable disease-16). Seven subjects with dementia had their orientation and judgment evaluated through a mental status examination. All subjects, except those with no identifiable disease, experienced disease onset at least a year prior to the beginning of this study. Time of onset was 196 J Korean Geriatr Soc 13(4) Dec 2009

3 not known in 25 patients. At the beginning of this study, 50 subjects were on a regular diet while the others were on a soft-bland diet because of dental problems. 2. Swallowing evaluation Aspiration signs were delineated as wet voice and reflex cough during meal time. Aspiration was deemed to be present clinically when aspiration signs were present more than once per meal time. 1) Fluoroscopic swallowing study Fig. 1. Delayed pharyngeal reflexes were graded as none, mild, moderate, and severe. Below figures were captured at time of hyoid elevation (beginning of pharyngeal stage). Starting at the left upper corner (clockwise direction), figures show normal and mildly, moderately, and severely delayed pharyngeal reflex. One rehabilitation doctor (KSJ), one fluoroscopist (PKW), and one nutritionist (HMH) performed the fluoroscopic swallowing studies on the 63 participants. The results were immediately recorded on paper as they could not be recorded as video files for technical reasons. Subjects swallowed foods with diverse viscosities twice in the following order: 5 ml of water by syringe, then a spoonful of Yoplait yogurt, pudding, soft bland diet, and a regular diet. All foods were mixed with a 35% diluted barium solution (Solotop ; Taijoon, Seoul, Korea) without significant change to viscosity. In this study, Yoplait corresponds to the fluid-type yogurt, soft bland diet to the thin rice gruel, and a regular diet to the thick rice gruel of the previous study 13). 2) Swallowing parameters Subglottic aspiration, supraglottic penetration, delayed pharyngeal reflex, and vallecular and pyriform sinus residues were assessed using fluoroscopy with patients in the lateral position. Subglottic aspiration and supraglottic penetration were differentiated based on whether the bolus entered the true vocal fold. Delayed pharyngeal reflex was graded as none (hyoid elevation occurred before the head of the bolus passed the mandibular angle), mild (hyoid elevation occurred after the head of the bolus passed the mandibular angle but most of the bolus remained in the vallecular area), moderate (hyoid elevation occurred when the bolus passed the laryngeal vestibule along the groove to the pyriform sinus), or severe (hyoid elevation occurred when more than half of the pyriform sinus was filled with the bolus) (Fig. 1). This classification is similar to that used in an earlier study 12). Residue amounts were graded as none, scant (the vallecula or pyriform sinus was only coated with residue), little (the height of the residue was less than half the total height of the vallecula or pyriform sinus), or much (the height of residue was more than half the total height of the vallecula or pyriform sinus). In recording the grades, all three investigators were required to agree on the readings. If an investigator disagreed, swallowing trials were repeated (with subject approval) until agreement was reached. 3. Statistics Fisher s exact test was done to compare the coincidence of the subglottic aspiration detected by fluoroscopy to the aspiration signs found clinically. Multivariate logistic regression J Korean Geriatr Soc 13(4) Dec

4 analysis was performed to determine the aspiration risk according to swallowing parameters (residues and pharyngeal reflex delay). All alpha errors were determined to be The SPSS program version 12.0 program (SPSS Inc., Chicago, IL, USA) was used to perform the statistical analysis. RESULTS Nine patients (14.3%) showed clinical signs of aspiration but did not have aspiration pneumonia since admission. All 63 patients successfully swallowed the liquid, but 15 patients refused to swallow the Yoplait, two refused the pudding, and four the soft-bland and regular diet. Fluoroscopic findings revealed that 31 patients showed neither subglottic aspiration nor supraglottic penetration, but eight patients (12.7%) showed subglottic aspiration, and 24 patients (38.1%) supraglottic penetration during liquid swallowing. No patient showed subglottic aspiration while swallowing Yoplait, pudding, Table 1. Cross table of the aspiration signs detected clinically and the subglottic aspiration by fluoroscopic swallowing study in 63 elderly subjects Aspiration sign No aspiration sign Aspiration by fluoroscopy 2 6 No aspiration by fluoroscopy 7 48 Values are numbers of patients. soft-bland diet, and the regular diet. Three of 48 patients (6.3 %) showed supraglottic penetration during Yoplait swallowing. Of 59 patients, two (3.4%) and one (1.7%) showed suraglottic penetration of the soft-bland and regular diets, respectively. Only two patients showed both aspiration signs and subglottic aspiration in the fluoroscopic study. Six patients showed subglottic aspiration in the fluoroscopic study without any clinical sign. Seven patients who complained of aspiration signs did not show subglottic aspiration, but they all presented with supraglottic penetration (Table 1). Fisher s exact test did not reveal a significant correlation between the signs of aspiration and subglottic aspiration (odds ratio [OR], 2.286; 95% confidence interval [CI], [0.383, ]). Vallecular and pyriform sinus residues for foods are presented in Table 2. Most patients showed little or no pyriform sinus residue after swallowing liquid, with the exception of one patient who showed a substantial amount of residue. Much vallecular residue was found in some patients only during swallowing of the regular diet. However, little pyriform sinus residue was observed during the swallowing of all foods. Pharyngeal reflex delays for the various foods are shown in Table 3. Delayed pharyngeal reflex occurred in some patients during the swallowing of liquid, soft-bland diet, and regular diet. Multivariate logistic regression analysis with backward elimination approach showed that no covariate correlated with subglottic aspiration whereas delayed pharyngeal reflex during Table 2. Vallecular and pyriform sinus residues after swallowing of diverse food textures in 63 elderly subjects Vallecular residue Pyriform sinus residue L Y P S N L Y P S N None Scant Few Much N/A Values are number of patients. L, liquid; Y, yoplait; P, pudding; S, soft bland diet; N, normal regular diet, N/A, not applicable. 198 J Korean Geriatr Soc 13(4) Dec 2009

5 Table 3. Degree of pharyngeal reflex delay during swallowing of diverse food textures in 63 elderly subjects Delayed pharyngeal reflex L Y P S N None Mild Moderate Severe N/A Values are number of patients. L, liquid; Y, yoplait; P, pudding; S, soft-bland diet; N, normal regular diet, N/A, not applicable liquid (p<0.001) or Yoplait (p=0.010) swallowing correlated with aspiration plus penetration. When the subjects were divided into stroke (n=19) and nonstroke (n=44) groups, four patients (21.1%) in the stroke group showed supraglottic penetration, and four (21.1%) experienced subglottic aspiration. The non-stroke group revealed supraglottic penetration in 20 subjects (45.5%) and subglottic aspiration in four patients (9.1%). The incidences of aspiration in the two groups were not significantly different by Fisher s exact test (OR, 0.375; 95% CI, [0.083, 1.693]). When subjects were dichotomized by diseases that might cause dysphagia (stroke, dementia, and Parkinsonism) and those unlikely to do so, the incidences of aspiration were not significantly different between the two groups by Fisher s exact test (OR, 0.538; 95 % CI, [0.117, 2.475]). DISCUSSION This is the first study on the swallowing characteristics of elderly patients admitted to a geriatric hospital or a long term care facility using fluoroscopic swallowing study. Subglottic aspiration was observed in 12.7% of patients and supraglottic penetration in 38.1% in the fluoroscopic swallowing study whereas 14.3% of patients showed aspiration signs clinically. No significant correlation was found between the aspiration signs assessed clinically and the subglottic aspiration detected by the fluoroscopic swallowing study. Vallecular residues were significantly greater during swallowing of the regular diet, whereas the pyriform sinus residues were not. Subglottic aspiration was not correlated with residues and delayed pharyngeal reflex. However, delayed pharyngeal reflex during liquid or Yoplait swallowing correlated with aspiration plus penetration. The prevalence of aspiration in this study was 12.7% on the fluoroscopic swallowing study, in line with the findings of Kawashima et al. 7) ; however, it was lower than that of Lin et al. s study 6), although the number of patients was too small to represent the prevalence in elderly patients. From this study, it was expected that the prevalence rate would be similar to Lin et al. s study 6) because subjects admitted to a hospital or a facility were enrolled. In view of the findings of a previous study 14) which stated that deep laryngeal penetration often progressed to aspiration, it is possible that patients showing supraglottic penetration without subglottic aspiration might also be at risk of aspiration. If penetration cases were included, the prevalence rate of aspiration plus penetration would increase to 50.8%. The six patients who showed subglottic aspiration on the fluoroscopic study without any aspiration sign (silent aspiration) emphasize the importance of this study. Seven patients who showed supraglottic penetration with clinical aspiration signs suggest that supraglottic penetration also must not be overlooked in the detection of aspiration as only few swallowing trials are performed in most fluoroscopic swallowing studies. However, Daggett et al. 15) found that 16.8% of swallows showed penetration in normal subjects aged 50 and above in a videofluoroscopic swallowing study. Therefore, the diagnosis of aspiration must be considered in a comprehensive manner. It will be necessary to classify penetration cases according to several steps using the penetration aspiration scale 16), which was not done in this study. The prevalence of aspiration between stroke and non stroke groups did not show any difference. This suggests that aspiration in this study originated from multiple factors including J Korean Geriatr Soc 13(4) Dec

6 poor general condition and the aging process, rather than the disease itself. Four patients from the non stroke group with aspiration had additional diagnoses of herniated intervertebral disc, asthma, dementia, and poor oral intake without a disease cause. Their average age was 76.3 ± 5.3 years. This did not differ significantly from that of the other patients (p=0.921). They all showed a worse than moderately delayed pharyngeal reflex. They had no definite abnormal signs suggestive of stroke or other diseases that could cause dysphagia. However, none of them could ambulate without assist and tended to be bed bound. Deconditioning due to decreased activity might lead to dysphagia. Although cervical imaging was not performed, cervical osteophytes related to old age might be a cause of dysphagia in this study 17). The results of this study showed that delayed pharyngeal reflex during liquid or Yoplait swallowing had an effect on aspiration plus penetration. This finding is somewhat similar to Han et al. s study 18) which showed that delayed triggering of pharyngeal swallowing is related to penetration/aspiration, with an odds ratio of 2.98 during the drinking of 5 ml of water in 103 stroke patients using polychotomous logistic linear regression. When the dependent variable was restricted to subglottic aspiration, no covariates, including delayed pharyngeal reflex, were correlated with aspiration. This result coincides with Martin-Harris study 19), which concluded that a delay in pharyngeal swallowing per se cannot be assumed to indicate disordered swallowing in the absence of coexisting impairments of swallowing physiology. Schindler et al. 20) observed that pharyngeal swallowing is delayed in healthy elderly subjects, and that elderly subjects frequently require multiple swallows to effectively clear a bolus from the pharynx. This coincides with our results although they did not comment on vallecular or pyriform sinus residues. Kelly et al. 21) revealed that the bolus type had a significant effect on residue scores, which differed from our results. This mismatch might be due to the differences in residue scoring and the bolus amount. The Kelly study 21) used 10 ml of foods, while we used 5 ml of liquid and one spoonful of other textures, which might be too small to show the differences between foods. The pyriform sinus residue amounts for pudding, soft-bland diet, and regular diet were found to be unrelated to aspiration or penetration, unlike the initial hypothesis that high viscosities are likely to increase aspiration risk as a result of pharyngeal retention. This result differs from that of Eisenhuber et al. s study 12), which may be because Eisenhuber et al. s study 12) recruited more patients with moderate to severe pharyngeal retention. In the present study, the pyriform sinus residue was insufficient (residues were scant or few, not much) to evoke overflow aspiration with all food textures. The present study has a few limitations, one of which is that images could not be recorded (the fluoroscopic device did not have an image storing function). Thus, this study could only use semiquantitative data, rather than quantitative data, such as pharyngeal delay time. Further quantitative studies should be done to overcome this shortcoming. Intra- and interater reliability was not evaluated. However, all the swallowing parameters were easily divided into four grades and there were no contradictions between the three investigators. This study is also limited because the precise characteristics of the patients were not known, for example, onset and lesion location (in cases of stroke). Nevertheless, the authors believe that the findings in this study can be useful to accurately detect aspiration through fluoroscopic study. Having completed this study, the diets of patients who showed subglottic aspiration were changed to the better-tolerated thickened liquids, and their aspiration symptoms and fluoroscopic findings improved. An attempt was made to follow up on these patients one year later by telephone or direct contact. Although only 14 of the 63 patients (22.2%) responded, responders, including patients who underwent diet modification, had no symptoms of aspiration or events of aspiration pneumonia. However, to confirm this, another study is required to evaluate improvement in general condition and reduced rates of aspiration pneumonia after diet modification. Though this study has several limitations, it demonstrates that a fluoroscopic swallowing study is important for diagnos- 200 J Korean Geriatr Soc 13(4) Dec 2009

7 ing dysphagia. Moreover, it reveals that diet modification, such as thickening liquids, is necessary when patients show evidence of subglottic aspiration during swallowing. Additional studies are required to confirm the clinical usefulness of diet modification. CONCLUSION This study demonstrates that a fluoroscopic swallowing study is important for diagnosing dysphagia in elderly patients because of no significant correlation between the aspiration signs assessed clinically and the subglottic aspiration detected by a fluoroscopic swallowing study. Diet modification, such as thickening liquids, is necessary when patients demonstrate evidence of subglottic aspiration during swallowing. ACKNOWLEDGEMENTS I especially thank Park Kun Woong for performing the fluoroscopic swallowing studies and interpreting their results, Hyeong Mi Hyeong for preparing the textured foods and interpreting the results, and Janette Villagonzalo (Customer Service Manager of Professional Editing Services) for helping with the English writing. REFERENCES 1. Robbins J, Hamilton JW, Lof GL, Kempster GB. Oropharyngeal swallowing in normal adults of different ages. Gastroenterology 1992;103: Logemann JA. Evaluation and treatment of swallowing disorders. Austin: PRO-ED; Yoshikawa M, Yoshida M, Nagasaki T, Tanimoto K, Tsuga K, Akagawa Y, et al. Aspects of swallowing in healthy dentate elderly persons older than 80 years. J Gerontol A Biol Sci Med Sci 2005;60: Rumeau P, Vellas B. Dysphagia, a geriatric point of view. Rev Laryngol Oto Rinol (Bord) 2003;124: Kikawada M, Iwamoto T, Takasaki M. Aspiration and infection in the elderly: epidemiology, diagnosis and management. Drugs Aging 2005;22: Lin LC, Wu SC, Chen HS, Wang TG, Chen MY. Prevalence of impaired swallowing in institutionalized older people in Taiwan. J Am Geriatr Soc 2002;50: Kawashima K, Motohashi Y, Fujishima I. Prevalence of dysphagia among community-dwelling elderly individuals as estimated using a questionnaire for dysphagia screening. Dysphagia 2004;19: Roy N, Stemple J, Merrill RM, Thomas L. Dysphagia in the elderly: preliminary evidence of prevalence, risk factors, and socioemotional effects. Ann Otol Rhinol Laryngol 2007;116: Ramsey D, Smithard D, Kalra L. Silent aspiration: what do we know? Dysphagia 2005;20: Clavé P, de Kraa M, Arreola V, Girvent M, Farré R, Palomera E, et al. The effect of bolus viscosity on swallowing function in neurogenic dysphagia. Aliment Pharmacol Ther 2006;24: Kuhlemeier KV, Palmer JB, Rosenberg D. Effect of liquid bolus consistency and delivery method on aspiration and pharyngeal retention in dysphagia patients. Dysphagia 2001; 16: Eisenhuber E, Schima W, Schober E, Pokieser P, Stadler A, Scharitzer M, et al. Videofluoroscopic assessment of patients with dysphagia: pharyngeal retention is a predictive factor for aspiration. AJR Am J Roentgenol 2002;178: Paik NJ, Han TR, Park JW, Lee EK, Park MS, Hwang IK. Categorization of dysphagia diets with the line spread test. Arch Phys Med Rehabil 2004;85: Friedman B, Frazier JB. Deep laryngeal penetration as a predictor of aspiration. Dysphagia 2000;15: Daggett A, Logemann J, Rademaker A, Pauloski B. Laryngeal penetration during deglutition in normal subjects of various ages. Dysphagia 2006;21: Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration aspiration scale. Dysphagia 1996;11:93-8. J Korean Geriatr Soc 13(4) Dec

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