Examination of Swallowing Varies Depending on Food Types

Tohoku J. Exp. Med., 2010, 220, 41-46 The Risk of Penetration or Aspiration during VF 41 The Risk of Penetration or Aspiration during Videofluoroscopic Examination of Swallowing Varies Depending on Food Types Kenichiro Ozaki, 1,2 Hitoshi Kagaya, 1 Michio Yokoyama, 1 Eiichi Saitoh, 1 Sumiko Okada, 3 Marlís González-Fernández, 4 Jeffrey B. Palmer 4,5 and Hiroshi Uematsu 2 1 Department of Rehabilitation Medicine, School of Medicine, Fujita Health University, Toyoake, Aichi, Japan 2 Department of Gerodontology, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan 3 Faculty of Rehabilitation, School of Health Sciences, Fujita Health University, Toyoake, Aichi, Japan 4 Department of Physical Medicine and Rehabilitation, School of Medicine, Johns Hopkins University, Boltimore, Maryland, USA 5 Department of Otolaryngology-Head and Neck Surgery and Center for Functional Anatomy and Evolution, Johns Hopkins University, Boltimore, Maryland, USA Keywords: Aspiration/laryngeal penetration/videofluoroscopic examination of swallowing/deglutition/deglutition disorders Tohoku J. Exp. Med., 2010, 220 (1), 41-46. 2010 Tohoku University Medical Press Dysphagia is caused by a wide variety of diseases and disorders affecting the structure and/or function of oral cavity, larynx, or esophagus. Videofluoroscopic examination of swallowing (VF) is the gold standard in diagnosis and management of dysphagia. During the VF, the patient ingests radiopaque foods and liquids, and oral, pharyngeal, and esophageal stages of swallowing physiology are observed and evaluated (Palmer et al. 2006). Aspiration is defined as passage of materials through the vocal folds, while laryngeal penetration is defined as passage of materials into the larynx, but not through the vocal folds. Aspiration and laryngeal penetration during VF in patients with dysphagia depend on clinical variables as well as various food parameters such as consistency, viscosity, adhesiveness, cohesiveness or bolus volume. Previous studies suggest that larger Received October 5, 2009; revision accepted for publication November 20, 2009. doi:10.1620/tjem.220.41 Correspondence: Kenichiro Ozaki, D.D.S., Department of Gerodontology, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113-8510, Japan. e-mail: oza-gerd@tmd.ac.jp 41 liquid boluses are more likely to cause aspiration (Clavé et al. 2006; Daggett et al. 2006). Robbins et al. (1987) compared a 30-ml liquid swallow (by cup) to a 2-ml swallow (by teaspoon) and found that the cup swallow may not be more challenging than the teaspoon swallow because 6 subjects aspirated on the 30-ml swallow without aspirating on the teaspoon but 3 aspirated on the teaspoon only. Kuhlemeier et al. (2001) reported that patients were more likely to aspirate thin liquids (apple juice) than thick liquids (apricot nectar) and more likely to aspirate thick liquids than puddinglike ultrathick liquids. They also stated that patients were less likely to aspirate when the bolus was delivered by spoon than when it was delivered by cup. Linden and Siebens (1983) showed that laryngeal penetration tended to occur more frequently during liquid swallows than semisol-

42 K. Ozaki et al. id food swallows. Daggett et al. (2006) reported that aspiration was more likely with liquids than pudding, cookie or a bite of an apple. Since drinking differs from eating in that solid food requires mastication and that solid food tends to be lower in the foodway at swallow initiation (due to stage II transport) (Palmer et al. 1992; Hiiemae and Palmer 1999), the risk of aspiration is probably different. A recent study demonstrated that a two-phase mixture of liquid barium (liquid phase) and corned beef hash (solid phase) was significantly lower in the foodway at swallow onset compared to liquid barium or corned beef hash. It is possible that twophase food increases the risk of aspiration because it is lower in the foodway at swallow onset (Saitoh et al. 2007). To the best of our knowledge, however, no reports have described the risk of laryngeal penetration or aspiration in a large clinical sample of patients with a variety of diagnoses. The objective of this study was to determine laryngeal penetration or aspiration risk during VF associated with various liquid volumes and food consistencies in such a sample. Methods Five-hundred and twenty-four patients with suspected dysphagia underwent VF between January 2006 and September 2008 at our institution after providing written informed consent. Patients were seated comfortably in a chair. VF was performed upright unless, in the clinician s judgment, the risk of laryngeal penetration or aspiration was excessive, in which case VF was performed in a reclining position for patient safety. Usually, foods were administered to each patient in the following sequence: 1) 4 ml of pudding-thick barium (PD); 2) 4 ml of thin liquid barium (); 3) 10 ml of thin liquid barium (); 4) one swallow from a cup of thin liquid barium with volume controlled by the patient (); 5) 8 g of corned beef hash (corned beef, Nozaki, Tokyo, Japan) with barium (); and 6) a twophase mixture of 4 g of corned beef hash with barium and 5 ml of thin liquid barium (). The study progressed in that order depending on the findings of previous swallows. Commercially available thin liquid barium (50% wt/vol, Barytogen Sol, Fushimi, Kagawa, Japan) was used. Pudding thick barium (5,550 mpa.s) was prepared by adding 2 g of thickener (Toromerin-Hi, SANWA SKK, Aichi, Japan) to 100 ml of liquid barium. PD,, and boluses were placed in the mouth with a syringe, and the patients were asked to hold the bolus in their mouth until instructed to swallow. Patients were instructed to eat and food in their usual manner. Compensatory maneuvers or other foods such as honey thick liquids, nectar thick liquids, jelly and cookie were tested empirically as necessary. Of 524 patients, we included patients who received at least 2 out of 6 types of foods (PD,,,, and ) in an upright posture without compensatory maneuvers. In addition, any patient who aspirated PD was excluded from the study. Thus, 229 patients were evaluated in this study. VF was performed at 30 frames/s in lateral and antero-posterior projections. Each recording covered the interval from the food entering the mouth until the end of the terminal swallow. Severity of dysphagia was assessed by using Dysphagia Severity Scale (DSS); a 7-point ordinal scale consisting of: 1) saliva aspiration; 2) food aspiration; 3) water aspiration; 4) occasional aspiration; 5) oral problem; 6) minimum problem; and 7) within normal limits (Baba and Saitoh 2000). This scale is in common use in Japan. The presence or absence of laryngeal penetration or aspiration during each food trial was evaluated by agreement of at least 2 researchers including physiatrists, dentists and/or speech therapists. Table 1. Patients Characteristics. Age (Mean ± S.D.) 66 ± 14 Male, n (%) 153 (66.8) Cause of dysphagia, n (%) Stroke 100 (43.7) Neuromuscular disease 27 (11.8) Respiratory disease 17 (7.4) Cardiovascular disease 14 (6.1) Head and neck cancer 12 (5.2) Others 59 (25.8) Dysphagia severity scale (DSS), n (%) 7 within normal 46 (20.1) 6 minimum problem 36 (15.7) 5 oral problem 28 (12.2) 4 occasional aspiration 60 (26.2) 3 water aspiration 57 (24.9) 2 food aspiration 2 (0.9) 1 saliva aspiration 0 (0) n = 229 Table 2. Proportion of patients with penetration or aspiration of particular consistencies. Food Number of patients Penetration N (%) Aspiration N (%) Aspiration/Penetration N (%) PD 205 13 (6.3) 0 (0.0) 0.0 214 78 (36.4) 29 (13.6) 37.2 157 57 (36.3) 17 (10.8) 29.8 168 81 (48.2) 31 (18.5) 38.3 179 25 (14.0) 7 (3.9) 28.0 180 69 (38.3) 40 (22.2) 58.0 PD; pudding thick liquid, ; corned beef hash, ; 4 ml of thin liquid, ; 10 ml of thin liquid, ; one cup swallow from a cup, ; two-phase mixture of 4g of and 5 ml of thin liquid

The Risk of Penetration or Aspiration during VF 43 Table 3. 2 2 contingency tables and paired comparisons to determine the risk of laryngeal penetrations. P = 0.010 P = 0.001 P < 0.001 PD * + 0 23 23 + 10 41 51 + 23 56 79 8 131 139 16 104 120 15 64 79 8 154 162 26 145 171 38 120 158 PD is less likely to cause penetration a is less likely to cause penetration is less likely to cause penetration P < 0.001 P < 0.001 P = 0.015 + 5 68 73 + 13 35 48 + 15 53 68 7 116 123 9 78 87 30 73 103 12 184 196 22 113 135 45 126 171 PD is less likely to cause penetration b is less likely to cause penetration is less likely to cause penetration P < 0.001 P < 0.001 P = 0.003 + 2 48 50 + 12 57 69 + 24 43 67 1 92 93 8 65 73 19 50 69 3 140 143 20 122 142 43 93 136 PD is less likely to cause penetration is less likely to cause penetration is less likely to cause penetration P < 0.001 P < 0.001 P = 0.482 + 2 68 70 + 12 46 58 + 17 40 57 1 78 79 10 88 98 33 53 86 3 146 149 22 134 156 50 93 143 PD is less likely to cause penetration is less likely to cause penetration is less likely to cause penetration P < 0.001 P = 0.007 P = 0.135 + 1 59 60 + 14 42 56 + 26 31 57 4 97 101 20 79 99 45 46 91 5 156 161 34 121 155 71 77 148 PD is less likely to cause penetration is less likely to cause penetration is less likely to cause penetration Paired comparisons PD PD *PD; pudding thick liquid, ; corned beef hash, ; 4 ml of thin liquid, ; 10 ml of thin liquid, ; one cup swallow from a cup, ; two-phase mixture of 4g of and 5 ml of thin liquid + laryngeal penetration presence, laryngeal penetration absence *Less likely to penetrate by McNemar s test with Bonferroni correction with a significance level of 0.003 a PD is less likely to cause penetration than, because 23 patients penetrated but not PD, while 8 penetrated PD but not. b PD is less likely to cause penetration than, because 68 patients penetrated but not PD, while 7 penetrated PD but not. ; more likely to cause laryngeal penetration, ; less likely to cause laryngeal penetration Statistical Analysis Fifteen 2 2 contingency tables were created from 6 food or liquid groups. McNemar s test with Bonferroni correction was used for pairwise comparisons between food types to detect differences in the risk of laryngeal penetration or aspiration on VF with a significance level of P < 0.003. (StatMate III statistical software, ATMS, Tokyo, Japan). This level was selected to correct for multiple comparisons; 0.003 = 0.05/15. The paired comparisons method was used

44 K. Ozaki et al. Table 4. 2 2 contingency tables and paired comparisons to determine the risk of aspirations. P = 0.030 P = 0.060 P < 0.001 PD * + 0 6 6 + 1 16 17 + 5 25 30 0 156 156 6 148 154 3 125 128 0 162 162 7 164 171 8 150 158 PD is less likely to cause aspiration is less likely to cause aspiration c is less likely to cause aspiration d P < 0.001 P = 0.150 P < 0.001 * + 0 28 28 + 4 9 13 + 5 33 38 0 168 168 3 119 122 7 126 133 0 196 196 7 128 135 12 159 171 PD is less likely to cause aspiration is less likely to cause aspiration is less likely to cause aspiration P < 0.001 P < 0.001 P = 0.009 + 0 14 14 + 5 21 26 + 5 17 22 0 129 129 1 115 116 4 110 114 0 143 143 6 136 142 9 127 136 PD is less likely to cause aspiration is less likely to cause aspiration is less likely to cause aspiration P < 0.001 P < 0.001 P = 0.001 * + 0 26 26 + 6 28 34 + 7 23 30 0 123 123 0 122 122 5 108 113 0 149 149 6 150 156 12 131 143 PD is less likely to cause aspiration is less likely to cause aspiration is less likely to cause aspiration P < 0.001 P = 0.004 P = 0.360 + 0 36 36 + 0 17 17 + 12 18 30 0 125 125 3 135 138 12 106 118 0 161 161 3 152 155 24 124 148 PD is less likely to cause aspiration is less likely to cause aspiration is less likely to cause aspiration Paired comparisons PD PD *PD; pudding thick liquid, ; corned beef hash, ; 4 ml of thin liquid, ; 10 ml of thin liquid, ; one cup swallow from a cup, ; two-phase mixture of 4 g of and 5 ml of thin liquid + aspiration presence, aspiration absence * Less likely to aspirate by McNemar s test with Bonferroni correction with a significance level of 0.003 c is less likely to cause aspiration than, because 16 patients aspirated but not, while 6 aspirated but not. d is less likely to cause aspiration than, because 25 patients aspirated but not, while 3 aspirated but not. ; more likely to cause aspiration, ; less likely to cause aspiration to determine the risk of laryngeal penetration or aspiration for each of the 6 food types. Results Patient characteristics are shown in Table 1. No saliva aspiration patients (DSS 1) were included in this study.

The Risk of Penetration or Aspiration during VF 45 Subjects who aspirated PD were excluded from the study, as noted above, so the rate of PD aspiration in our sample was nil by definition. The lowest rate of laryngeal penetration was PD, followed by,,, and, while the lowest rate of aspiration after PD was, followed by,, and. More than half of the patients who had laryngeal penetration by aspirated (Table 2). PD and were each significantly less likely to result in laryngeal penetration than,, or. was significantly less likely to result in laryngeal penetration than. Using the paired comparisons method, laryngeal penetration risk increased in the following order: PD,,,,, and (Table 3). On the other hand, PD was significantly less likely to result in aspiration than,, or. and were each significantly less likely to result in aspiration than either or. was significantly less likely to result in aspiration than. Using the paired comparisons method, aspiration risk increased in the following order: PD,,,, and (Table 4). Discussion The absolute rate of aspiration of a food type should be interpreted with caution since progression from one consistency to another is determined by the findings in the previous trial. For example, the clinicians did not usually test high volumes of liquid in patients who aspirated small volumes (ie. was not tested when was aspirated). We used the paired comparisons method to determine the risk of laryngeal penetration or aspiration when more than one consistency was tested and found that and had the highest risk of laryngeal penetration and aspiration among the 6 types of foods and liquids, respectively. Combining solid and liquid phases in a single food is common during an ordinary meal. For example, we frequently consume soups that contain solid food particles. It has been reported that increased risk of aspiration in healthy subjects (Saitoh et al. 2007), but the present study suggests that has the highest risk of aspiration in many (but not all) individuals with dysphagia. Patients who aspirate should probably avoid eating multi-textured foods or add thickener to the thin liquid phase of these foods. drinking of thin liquid had the highest risk of laryngeal penetration and the second-highest risk of aspiration. However, while 18 patients aspirated but not, another 12 aspirated with but not. This suggests that is not merely a more challenging task than but is a qualitatively different task and that both and should be tested in patients who do not demonstrate aspiration of any other foods. The bolus volume of a natural, uninstructed drink from a cup is reported to be 14-15 ml on average (Bennett et al. 2009). In this study, was more likely to result in laryngeal penetration or aspiration than, and more likely than. Risk of thin-liquid laryngeal penetration or aspiration increased with volume. In addition, some patients spontaneously lift the chin during uninstructed drinking from a cup, which may increase aspiration risk (Ertekin et al. 2001). was less likely to result in laryngeal penetration or aspiration than,, or, suggesting that, with a homogenous soft solid food, mastication does not increase the risk of aspiration. The only thickened liquid consistency evaluated in this study was pudding, because honey- and nectar-thick liquid are not routinely tested in our institution. Thin liquids have low viscosity, run freely, and are difficult to contain in the oral cavity before swallowing compared to thick liquids (Palmer et al. 1993). In clinical practice, we usually try compensatory maneuvers, reclining position, or ultra-thick liquids in patients who aspirate PD rather than testing other foods or liquids. Because of this, all patients who aspirated PD were excluded from the present study, and we cannot draw any inferences about the risk of aspiration with PD compared to other food types. The present study has several limitations. We evaluated only the presence or absence of laryngeal penetration or aspiration. The amount of laryngeal penetration or aspiration, the timing and mechanism of laryngeal penetration or aspiration were not assessed. Food parameters were not blind to the evaluators, because food sequences during VF were determined in advance. Patients with very severe dysphagia (DSS 1) and patients who aspirated PD were excluded from this study. In conclusion, laryngeal penetration or aspiration risk varies among food types. The lowest risk of laryngeal penetration was PD, followed by,,, and. The aspiration risk after PD increased in the following order:,,, and. Aspiration risk was highest with the two-phase food; multi-textured foods should be used with caution in individuals with dysphagia. Because the risk of penetrating or aspirating a particular food varied greatly among subjects, an instrumental study such as VF or videoendoscopic evaluation of swallowing is necessary to establish a swallow-safe diet for individuals with significant risk of aspiration. Acknowledgments The authors are grateful to Dr. Shuji Hashimoto, at the Department of Hygiene, Fujita Health University School of Medicine, Japan and Dr. Hiroshi Yatsuya, at the Department of Public Health, Graduate School of Medicine, Nagoya University for their help with the statistical analyses. References Baba, M. & Saitoh, E. (2000) Indication of dysphagia rehabilitation. Rinsho Reha., 9, 857-863. (in Japanese) Bennett, J.W., Van Lieshout, P.H.H.M., Pelletier, C.A. & Steele, C.M. 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46 K. Ozaki et al. Palomera, E. & Serra-Prat, M. (2006) The effect of bolus viscosity on swallowing function in neurogenic dysphagia. Aliment. Pharmacol. Ther., 24, 1385-1394. Daggett, A., Logemann, J., Rademaker, A. & Pauloski, B. (2006) Laryngeal penetration during deglutition in normal subjects of various ages. Dysphagia, 21, 270-274. Ertekin, C., Keskin, A., Kiylioglu, N., Kirazli, Y., On, A.Y., Tarlaci, S. & Aydoğdu, I. (2001) The effect of head and neck positions on oropharyngeal swallowing: a clinical and electrophysiologic study. Arch. Phys. Med. Rehabil., 82, 1255-1260. Hiiemae, K.M. & Palmer, J.B. (1999) Food transport and bolus formation during complete feeding sequences on foods of different initial consistency. Dysphagia, 14, 31-42. Kuhlemeier, K.V., Palmer, J.B. & Rosenberg, D. (2001) Effect of liquid bolus consistency and delivery method on aspiration and pharyngeal retention in dysphagia patients. Dysphagia, 16, 119-122. Linden, P. & Siebens, A.A. (1983) Dysphagia: predicting laryngeal penetration. Arch. Phys. Med. Rehabil., 64, 281-284. Palmer, J.B., Rudin, N.J., Lara, G. & Crompton, A.W. (1992) Coordination of mastication and swallowing. Dysphagia, 7, 187-200. Palmer, J.B., Kuhlemeier, K.V., Tippett, D.C. & Lynch, C. (1993) A protocol for the videofluorographic swallowing study. Dysphagia, 8, 209-214. Palmer, J.B., Monahan, D.M. & Matsuo, K. (2006) Rehabilitation of Patients with Swallowing Disorders. In Physical Medicine and Rehabilitation, 3nd ed., edited by Braddom, R.M., W.B. Saunders Company, San Diego, CA, pp. 601-607. Robbins, J.A., Sufit, R., Rosenbek, J., Levine, R. & Hyland, J. (1987) A modification of the modified barium swallow. Dysphagia, 2, 83-86. Saitoh, E., Shibata, S., Matsuo, K., Baba, M., Fujii, W. & Palmer, J.B. (2007) Chewing and food consistency: effects on bolus transport and swallow initiation. Dysphagia, 22, 100-107.