SILENT ASPIRATION AND SWALLOWING PHYSIOLOGY AFTER RADIOTHERAPY IN PATIENTS WITH NASOPHARYNGEAL CARCINOMA

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1 ORIGINAL ARTICLE SILENT ASPIRATION AND SWALLOWING PHYSIOLOGY AFTER RADIOTHERAPY IN PATIENTS WITH NASOPHARYNGEAL CARCINOMA Louisa K. Y. Ng, MSc, 1 Kathy Y. S. Lee, PhD, 1 Sung Nok Chiu, Dr.rer.nat., 2 Peter K. M. Ku, MD, 1 C. Andrew van Hasselt, MD, 1 Michael C. F. Tong, MD 1 1 Department of Otorhinolaryngology Head and Neck Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital, Hong Kong Special Administrative Region, China. mtong@cuhk.edu.hk 2 Department of Mathematics, Hong Kong Baptist University, Kowloon Tong, Hong Kong Special Administrative Region, China Accepted 12 August 2010 Published online 10 November 2010 in Wiley Online Library (wileyonlinelibrary.com). DOI: /hed Abstract: Background. There is a paucity of knowledge on dysphagia in patients with nasopharyngeal carcinoma postradiotherapy (NPC post-rt). The purpose of this study was to establish silent aspiration occurrence, safe bolus consistency, and their relationship with swallowing physiology in patients with dysphagic NPC post-rt. Methods. Eighty-five patients with dysphagic NPC post-rt were assessed across 4 bolus consistencies. We compared penetration-aspiration scores against 4 swallowing physiology impairments. Results. Silent aspiration occurred in 65.9% of patients with dysphagia, with 64.7% on thin fluids, 35.3% on thick fluids, 11.8% on pureed diet, and 5.9% on soft diet. Multivariate analysis of variance (MANOVA) indicated pharyngeal contraction and swallowing response had significant effect on thick fluids (p ¼.002), thin fluids (p ¼.017), and soft diet (p ¼.031). Conclusion. Silent aspiration of thin fluids is a common occurrence in dysphagic NPC post-rt, with least aspiration noted on soft diet. Considering the high incidence of silent aspiration, instrumental assessment in this cohort is crucial. VC 2010 Wiley Periodicals, Inc. Head Neck 33: , 2011 Keywords: nasopharyngeal carcinoma; dysphagia; penetrationaspiration; swallowing physiology; bolus consistency Nasopharyngeal carcinoma (NPC) is an endemic disease in Hong Kong. In 2006, the Hong Kong Centre for Health Promotion reported that 21.2 men and 7.4 women in 100,000 were affected with NPC. 1 The current optimum treatment for NPC is radiotherapy (RT). 2 However, radiotherapy often results in chronic dysphagia in patients with NPC. 3 5 In patients with NPC post-rt, silent aspiration on fluids has been observed to occur in up to 58% of Correspondence to: M. C. F. Tong VC 2010 Wiley Periodicals, Inc. patients with dysphagia, 6 rendering a cough response an unreliable aspiration indicator. 7 More than 1 year after radiotherapy, NPC post-rt patients with silent aspiration are at higher risk of aspiration pneumonia than their overtly aspirating counterparts. 2 One way to lower aspiration and consequential aspiration pneumonia risk in this cohort is to increase the viscosity of fluids. A study of 50 patients with NPC post- RT showed that silent aspiration of fluids in 11 patients (22%) was lowered to only 1 patient (2%) when ingesting paste. 8 To the best of our knowledge, no other study has further explored this trend or investigated if changes in diet texture can lower aspiration risks. Overall, patients with NPC post-rt have delayed onset dysphagia that is more severe than neurogenic dysphagia. Due to multiple cranial nerve palsies from perineural fibrosis, 6,9 patients with NPC post-rt suffer from multiple oral and pharyngeal phase swallowing impairments. These include impaired tongue movement, bolus formation, soft palate movement, pharyngeal contraction, epiglottic retroflexion, laryngeal elevation, and delayed swallowing. 2,7 9 Faced with such a range of problems, clinicians need to narrow their focus to swallowing physiologies that contribute most to aspiration, so as to better manage intervention and rehabilitation for patients with NPC post-rt. Regrettably, very little is known about swallowing physiologies that are critical in exacerbating aspiration. 5 To address the inadequate knowledge of the pattern of dysphagia in patients with NPC post-rt aspiration and swallowing physiology impairments, we have conducted this retrospective case series study. The purpose of this study was to (1) determine if there are fluid and diet consistencies that are least likely to be silently aspirated by dysphagic NPC post- RT, and (2) identify the significant pharyngeal swallowing physiologies that affect the severity of penetration-aspiration in this population. Postradiotherapy Swallowing in NPC HEAD & NECK DOI /hed September

2 Table 1. Consistency labels with description contrasted with other international scales. 12 Other scales Consistency label Description United States scale Australian scale Thin fluids Unmodified regular fluids Thin 1 50 cp Regular Thick fluids Fluids thickened to thick Honey-like thick fluids Level 400-moderately thick milkshake texture cp Pureed diet Diet blended to consistency of Dysphagia puree Texture C-smooth pureed apple sauce Soft diet Minced and softened sticky diet Dysphagia mechanically altered (0.6 cm) Texture B-minced and moist (0.5 cm) PATIENTS AND METHODS Between 2004 and 2007, patients with NPC post-rt þ/ surgery or chemotherapy who also underwent fiber-optic endoscopic examination of swallowing (FEES) 10,11 at the Prince of Wales Hospital in Hong Kong were included in this study. All patients were suspected to have swallowing difficulties with symptoms of choking on swallowing or self-perceived difficulty with swallowing. Patients were excluded if they had (1) other primary dysphagia etiologies such as cardiovascular accidents, neurodegenerative disorders, and brain injury, (2) tracheostomy, or (3) an incomplete record. Eighty-five patients (62 men and 23 women), with a mean age of 56.8 years and SD of 10.9 years were studied. During FEES, the patient s swallowing was observed using a nasendoscope. With the nasendoscope inserted to the level of the pharyngeal area, each patient was given 4 different consistencies as listed in Table 1. Each patient was given a minimum of 3 to a maximum of five 5-mL teaspoonfuls of each consistency. A speech therapist and an otorhinolaryngologist jointly rated each patient s performance in 2 aspects: penetration-aspiration severity and swallowing physiology impairments. A modified Penetration-Aspiration Rating Scale (PARS) based on Rosenbek s 8-point penetration-aspiration scale 13 was used in this study. Penetration scores were collapsed into 1 point (Table 2) because these scores are less reliable than the scores for aspiration and normal subjects. 13 The scores on the modified PARS were 0, 1, 2, 3, and 4, corresponding to 1, 2 5, 6, 7, and 8 respectively on the Penetration-Aspiration Scale. 13 Each PARS score was rated jointly by the speech therapist and otorhinolaryngologist according to the level of bolus invasion into the airway observed on FEES. Four pharyngeal phase swallowing physiologies most commonly impaired in NPC post-rt were evaluated: laryngeal elevation, pharyngeal contraction, epiglottic retroflexion, and swallowing response. For each of these physiologies, a rating scale between 0 and 4 was used: 0 ¼ normal, 1 ¼ mildly impaired, 2 ¼ moderately impaired, 3 ¼ severely impaired, and 4 ¼ absent. The speech therapist and the otorhinolaryngologist jointly rated each of the swallowing physiologies based on the performance on overall consistencies. For purposes of this study, laryngeal elevation refers to the range of upward movement of the larynx observed on FEES during swallow; pharyngeal contraction refers to the observed white-out during swallowing; epiglottic retroflexion refers to the inversion of the epiglottis during swallowing; and the swallowing response refers to the timeliness of Table 2. Penetration-aspiration score modification. Score Description Rosenbek s 8-point Penetration- Aspiration Scale 13 Penetration- Aspiration Rating Scale Contrast does not enter airway. 1 0 Contrast enters airway; remains above vocal fold; 2 1 no residue visible. Contrast remains above vocal folds; visible residue remains. 3 1 Contrast contacts vocal folds but no residue remains. 4 1 Contrast contacts vocal folds and visible residue remains. 5 1 Contrast passes the glottis but no subglottic residue remains. 6 2 Contrast passes the glottis and visible subglottic residue remains 7 3 despite patient s response. Contrast passes glottis and visible subglottic residue remains. Absent patient response (silent aspiration) Postradiotherapy Swallowing in NPC HEAD & NECK DOI /hed September 2011

3 Table 3. Penetration-Aspiration Rating Scale across 4 consistencies. Consistency Mean SD Thin fluids Thick fluids Pureed diet Soft diet laryngeal elevation that occurs when the head of the bolus travels beyond the base of the tongue region. Descriptive statistics of the data were calculated. The overall swallowing performances of the patients on the 4 consistencies were contrasted by paired sample t tests. Using the penetration-aspiration severity score as the dependent variable, we used the multivariate analysis of variance (MANOVA) 14 to examine the effect of the 4 swallowing physiologies across the 4 bolus consistencies. The significance level was set at a ¼ RESULTS Table 4. Paired sample t test comparing PARS of the 4 consistencies. Paired difference Mean SD 95% CI t test Thin vs thick Thin vs pureed Thin vs soft diet Thick vs pureed Thick vs soft diet Pureed vs soft diet Abbreviations: PARS, Penetration-Aspiration Rating Scale; CI, confidence interval. *p <.05, p <.01, p <.001. FIGURE 1. Distribution of penetration-aspiration severity in 85 patients with dysphagic nasopharyngeal carcinoma (NPC) postradiotherapy (post-rt) on 4 consistencies. Of 85 dysphagic patients with NPC post-rt, silent aspiration was recorded in 56 patients with NPC post-rt (65.9%). Decreased frequency of silent aspiration was observed as viscosity of fluids increased; from 55 aspiration episodes (64.7%) occurring on thin fluids to 30 episodes (35.3%) on thick fluids. Similarly, the number of occurrences of silent aspiration reduced as diet moves from 10 episodes (11.8%) on pureed diet to 5 episodes (5.9%) on soft diet. Mean scores of PARS further confirmed that thin fluids are the most unsafe consistency for patients with dysphagia NPC post-rt (Table 3). PARS between all consistency pairs were significantly different under the paired sample t test (Table 4). Figure 1 shows the distribution of silent aspiration, overt aspiration, and penetration across 4 consistencies in 85 patients with dysphagic NPC post-rt. Multivariate tests showed that pharyngeal contraction and swallowing response had a significant effect on penetration-aspiration severity, with a p value of.023 and.038, respectively. MANOVA tests of between-subjects effects (Table 5) specified 2 significant relationships: degree of pharyngeal contraction impairments had a significant effect on PARS of thick fluids, and degree of swallowing response impairments had a significant effect on PARS of thin fluids and soft diets. DISCUSSION Silent aspiration is more prevalent than overt aspiration in patients with dysphagic NPC post-rt, especially on thin fluids. The results suggest that coughing associated with oral feeding is not a reliable Table 5. MANOVA tests of between-subjects effects. Physiology Consistency df F Laryngeal elevation Thin fluids Thick fluids Pureed diet Soft diet Epiglottic retroflexion Thin fluids Thick fluids Pureed diet Soft diet Pharyngeal contraction Thin fluids Thick fluids * Pureed diet Soft diet Swallowing response Thin fluids * Thick fluids Pureed diet Soft diet * Error Thin fluids Thick fluids Pureed diet Soft diet Abbreviations: MANOVA, Multivariate analysis of variance; df, degrees of freedom. *p.05. Postradiotherapy Swallowing in NPC HEAD & NECK DOI /hed September

4 index for detecting aspiration in this cohort. Comparing thin fluids and thick fluids, less overt and fewer silent aspiration was observed on thick fluids, further confirming the findings of Hughes et al. 8 To the best of our knowledge, we are the first to report both overt and silent aspiration occurring infrequently on both pureed diet and soft diet. Between the 2 diets, soft diet is found to be safer. Given that avoidance of solid food has been reported in patients with dysphagic NPC post-rt due to oral phase difficulties, 6 9 soft diet is often perceived to be more difficult for this population due to its textured consistency. On the contrary, our data show that soft diet is safer than pureed diet for patients with dysphagic NPC post-rt, despite perceptually being more orally challenging. Perhaps soft diet provides a better balance of sensory stimulation and textured consistency for patients with NPC post-rt to manage safely. Further studies with larger sample size and oral phase analysis may confirm this hypothesis. To place the above penetration-aspiration severity findings in context, we analyzed the corresponding swallowing physiologies observed in the 85 patients with dysphagic NPC post-rt. Laryngeal elevation and epiglottic retroflection were found to have no significant effect on penetration-aspiration severity in patients with NPC post-rt across all food consistencies. Pharyngeal contraction, by contrast, was found to have a significant effect on the PARS of thick fluids, whereas the swallowing response was found to have a significant effect on the PARS of thin fluids and soft diet. The finding that the severity of the swallowing response affects the penetration-aspiration severity of thin fluids is not new. A study of patients with neurogenic dysphagia supports the view that the high velocity transfer of thin fluids from the oral cavity to the pharynx increases the risk of penetration-aspiration when the swallowing response is mistimed. 15 Combined with multiple oral and pharyngeal deficits, we should not be surprised that patients with dysphagic NPC post-rt are more predisposed to thin fluid aspiration when swallowing is mistimed. On the other hand, the notion that the swallowing response affects soft diet penetration-aspiration severity is new. Because this correlation has only been observed in patients with dysphagic NPC post-rt, it is likely related to impairments that are unique to this group. Oral phase impairments have been well-documented in patients with NPC post-rt; including oral transfer difficulties, 7 poor bolus formation, 8 and oral transit abnormalities. 6 Because poor oral phase often results in premature spillage of bolus into the pharynx or airway and patients with dysphagic NPC post-rt suffer from multiple oral phase difficulties, premature spillage into the pharynx and airway is expected in patients with dysphagic NPC post-rt. Considering that thick fluids and pureed diet are cohesive by definition, 12 soft diet and thin fluids are comparatively less cohesive in this study. Therefore, timely swallowing response plays a crucial role in preventing separated pieces of soft diet from spilling prematurely into the airway. In other words, due to coexisting oral phase impairments in patients with NPC post-rt, the swallowing response has a direct effect on the penetrationaspiration severity of soft diet. Pharyngeal contraction impairments have a significant effect on penetration-aspiration severity of thick fluids, not soft diet, in patients with NPC post-rt. This is contrary to Logemann s suggestion that thick, higher viscosity foods such as soft diet is most at risk when pharyngeal contraction is impaired. 15 Recent research can explain this discrepancy. Butler et al 16 studied the bolus of 4 consistencies, ranging from thin fluids to pudding-thick fluids, in 44 normal subjects using concurrent manometry and FEES. Unexpectedly, she found significantly lowered pharyngeal pressure solely in thick fluids, possibly due to the ideal viscosity, weight, and consistency range of thick fluids, enabling the force of gravity to take over the transfer of flow through the pharynx. Taken together, we believe this finding by Butler et al 16 explains why thick fluids, not soft diet, is most at risk when NPC RT has impaired the patient s pharyngeal contraction. In this study, our data show that epiglottic retroflexion and laryngeal elevation did not determine the severity of penetration-aspiration, even though they are often impaired in NPC post-rt. 2,8 Interestingly, the same findings are reported in normal human subjects and cats. Shaker et al 17 studied concurrent FEES, pharyngeal intraluminal manometry, and submental surface electromyography on 8 normal human subjects during dry swallow, water swallow, and barium swallow. Shaker et al 17 demonstrated that although laryngeal elevation is an essential feature of laryngeal closure, the most crucial physiology in preventing aspiration was laryngeal movement coordination, not laryngeal elevation. In the same way, through a study of 14 adult cats, epiglottectomy was found to affect neither penetration-aspiration severity nor any phase of swallowing. 18 To the best of our knowledge, although no epiglottectomy swallowing functions study has yet been performed on human subjects, the similar laryngeal structures of cats and humans strongly suggest that epiglottic retroflexion does not play an essential role in preventing penetrationaspiration during swallowing. Due to the retrospective nature of this study, limitations of this study include the lack of information such as inter-rater and intra-rater reliability, dysphagia incidence, effects of RT, effects of other thickened consistency fluids on penetration-aspiration severity, and the true significance of aspiration on this population. A prospective study will benefit from the inclusion of (1) inter-rater and intra-rater reliability, (2) both patients with NPC post-rt with and without dysphagia to yield a more representative silent aspiration occurrence estimate, (3) more years of followup post-rt, (4) a wider range of fluid consistencies to determine the effectiveness of thickened fluids in 1338 Postradiotherapy Swallowing in NPC HEAD & NECK DOI /hed September 2011

5 reducing aspiration risks, and (5) a group comparison between nonrestricted intake of fluids or food consistencies versus restricted intake of thick fluids and soft diet to find the true significance of the safer consistencies found in this study. Although this study concentrated on aspiration and penetration, it is important to remember that their occurrences are insufficient to cause pneumonia unless other risk factors are present as well. In a landmark study of 189 elderly nursing home residents, feeding dependence and functional status were found to be significant risk factors. 19 Given that patients with NPC post-rt are mostly self-feeders and community ambulant, they can frequently tolerate aspiration for years without developing aspiration pneumonia. For that reason, this study serves as a reference for assessment and management and not as a directive for fluids and diet modification in this population. In conclusion, thick fluids and soft diet were found to be the least risky fluid and diet combination for patients with NPC post-rt. High silent aspiration occurrence also alerted us that instrumental assessment is vital in evaluating the penetration-aspiration risks of NPC post-rt. In swallowing physiology effects, we have shown that the degree of swallowing response impairments directly exacerbates penetration-aspiration severity of thin fluids and soft diet in NPC post- RT, whereas the degree of pharyngeal contraction impairments directly increases the risk of aspiration on thick fluids in patients with NPC post-rt. Acknowledgment. The authors thank Dr. Phua Sin Yong, Kit Chan, and Kristy Chung for their contributions to this study. REFERENCES 1. Centre for Health Protection. Nasopharyngeal carcinoma 2008;2009:1. Available at: lang¼en&info_id¼54&id¼25&pid¼9. 2. Chang YC, Chen SY, Lui LT, et al. Dysphagia in patients with nasopharyngeal cancer after radiation therapy: a videofluoroscopic swallowing study. Dysphagia 2003;18: Huang HY, Wilkie DJ, Schubert MM, Ting LL. Symptom profile of nasopharyngeal cancer patients during radiation therapy. Cancer Pract 2000;8: Kam MK, Teo PM, Chau RM, et al. Treatment of nasopharyngeal carcinoma with intensity-modulated radiotherapy: the Hong Kong experience. Int J Radiat Oncol Biol Phys 2004;60: Wu CH, Hsiao TY, Ko JY, Hsu MM. Dysphagia after radiotherapy: endoscopic examination of swallowing in patients with nasopharyngeal carcinoma. Ann Otol Rhinol Laryngol 2000;109: Marshall JN, Ku PK, Kew J, Cheung D, van Hasselt CA. Assessment and management of dysphagia in patients with nasopharyngeal carcinoma. Asian J Surg 1998;21: Ku PK, Yuen EH, Cheung DM, et al. Early swallowing problems in a cohort of patients with nasopharyngeal carcinoma: symptomatology and videofluoroscopic findings. Laryngoscope 2007;117: Hughes PJ, Scott PM, Kew J, et al. Dysphagia in treated nasopharyngeal cancer. Head Neck 2000;22: Mok P, Seshadri RS, Siow JK, Lim SM. Swallowing problems in post irradiated NPC patients. Singapore Med J 2001;42: Leder SB, Sasaki CT, Burrell MI. Fiberoptic endoscopic evaluation of dysphagia to identify silent aspiration. Dysphagia 1998;13: Langmore SE, Schatz K, Olson N. Endoscopic and videofluoroscopic evaluations of swallowing and aspiration. Ann Otol Rhinol Laryngol 1991;100: Atherton M, Bellis-Smith N, Cichero JA, Suter M. Texturemodified foods and thickened fluids as used for individuals with dysphagia: Australian standardised labels and definitions. Nutrition & Dietetics 2007;64:S53 S Rosenbek JC, Robbins JA, Rocker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia 1996;11: Sheskin DJ. Handbook of parametric and nonparametric statistical procedures. Boca Raton: Chapman & Hall/CRC; Logemann JA. Dysphagia: evaluation and treatment. Folia Phoniatr Logo 1995;47: Butler SG, Stuart A, Castell D, Russell GB, Koch K, Kemp S. Effects of age, gender, bolus condition, viscosity, and volume on pharyngeal and upper esophageal sphincter pressure and temporal measurements during swallowing. J Speech Lang Hear Res 2009;52: Shaker R, Dodds WJ, Dantas RO, Hogan WJ, Arndorfer RC. Coordination of deglutitive glottic closure with oropharyngeal swallowing. Gastroenterology 1990;98: Medda BK, Kern M, Ren J, et al. Relative contribution of various airway protective mechanisms to prevention of aspiration during swallowing. Am J Physiol Gastrointest Liver Physiol 2003;284:G933 G Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia 1998;13: Postradiotherapy Swallowing in NPC HEAD & NECK DOI /hed September