Bolus effects on patient awareness of swallowing difficulty and swallow physiology after chemoradiation for head and neck cancer

ORIGINAL ARTICLE Bolus effects on patient awareness of swallowing difficulty and swallow physiology after chemoradiation for head and neck cancer Nicole M. Rogus-Pulia, PhD, CCC-SLP, 1* Margaret Pierce, RN, BSN, OCN, 2 Bharat B. Mittal, MD, 3 Steven G. Zecker, PhD, 4 Jeri Logemann, PhD, CCC-SLP 4 1 William S. Middleton Memorial Veterans Hospital, University of Wisconsin Madison, Division of Gastroenterology and Hepatology, Department of Medicine, School of Medicine and Public Health, Madison, Wisconsin, 2 Department of Radiation Oncology, Northwestern Memorial Hospital, Chicago, Illinois, 3 Department of Radiation Oncology, Northwestern University, Feinberg School of Medicine, Chicago, Illinois, 4 Northwestern University, Department of Communication Sciences and Disorders, Evanston, Illinois. Accepted 21 April 2014 Published online 28 August 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23720 ABSTRACT: Background. Patients treated for head and neck cancer frequently develop dysphagia. Bolus characteristics are altered during fluoroscopic swallowing studies to observe the impact on swallowing function. The purpose of this study was to determine bolus volume and consistency effects on oropharyngeal swallowing physiology and patient awareness of swallowing difficulty. Methods. Twenty-one patients with head and neck cancer were assessed pre-chemoradiation and post-chemoradiation. The Modified Barium Swallow Study (MBSS) was utilized to examine swallow physiology. Each patient provided perceptual ratings of swallowing difficulty after each swallow of varying bolus types. Results. Oral transit times were significantly longer with pudding boluses. There were trends for higher residue percentages as well as perceptual ratings for pudding and cookie boluses. One correlation between perceptual ratings and physiology was significant. Conclusion. Patient awareness of swallowing difficulty and aspects of swallowing physiology vary with bolus consistency. Patient awareness does not correlate with observed changes in swallowing physiology. VC 2014 Wiley Periodicals, Inc. Head Neck 37: 1122 1129, 2015 KEY WORDS: dysphagia, chemoradiation, head and neck cancer, perception, bolus, volume, consistency INTRODUCTION Patients with head and neck cancer who receive chemoradiation treatment frequently develop dysphagia as a result of radiation-induced fibrosis to the critical tissues and damage to the neuromuscular junctions of the head and neck region. 1 9 Changes in bolus size and consistency along with postural changes may be effective in eliminating aspiration, the most dangerous complication of dysphagia. 2,10 In clinical practice, bolus volume and/or consistency is often altered in order to observe effects on swallow physiology. Systematic changes in normal swallowing with increasing bolus volume have been well-documented. 10 19 With increasing viscosity of the bolus, various changes in the normal swallow also have been observed. 10,11,13,20,21 Alterations in swallow physiology that occur in response to changes in bolus volume and viscosity also have been documented in patients with various medical conditions that often lead to dysphagia. 10,22 Trends observed across all of these patient groups, including patients with head *Corresponding author: N. M. Rogus Pulia, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison GRECC (11G), Room D5216, Madison, WI 53705. E-mail: nicolepulia@gmail.com This work was presented at the American Speech-Language-Hearing Association Annual Convention in Atlanta, Georgia, November 17, 2012. Deceased and neck cancer, can be summarized as higher rates of aspiration with thin liquids, 4,6,22 increased residue with larger volume and pudding boluses, 23 higher generated pressure with increased volume and viscosity, 24 26 and improved pharyngeal delay time (when bolus first enters the pharynx until laryngeal elevation begins) with larger volumes. 15,27 Limitations of these previous studies include a limited number of bolus types and presentation of boluses in a traditional hierarchy of increasing volume and viscosity. As swallowing is a neuromuscular function that is susceptible to fatigue effects, 28 30 the potential influence of bolus presentation order on oropharyngeal swallow physiology during the modified barium swallow study (MBSS) requires consideration. To mitigate any potential confounding impact, a randomized order of bolus presentation was utilized in this study. The type of bolus swallowed may not only affect swallow physiology but may also affect patient awareness of swallowing difficulty. 31 One study by Pauloski et al 31 examined agreement between patients complaints of dysphagia and actual swallowing function. The results of this study indicated that patients with head and neck cancer treated with chemoradiation were able to perceive decreases in their swallowing function. Results also suggested that patient awareness of swallowing difficulty may vary with bolus type, but this was not specifically examined. A broader understanding of how awareness of swallowing as well as swallow physiology changes with bolus type in patients who receive chemoradiation for head and 1122 HEAD & NECK DOI 10.1002/HED AUGUST 2015

BOLUS EFFECTS ON SWALLOWING IN PATIENTS WITH HEAD AND NECK CANCER neck cancer is both necessary and clinically useful. This information may allow for more informed expectations before swallow assessment, more accurate diet recommendations, and improved patient compliance with recommendations. The purpose of this study was to determine whether bolus type influences physiology of the oropharyngeal swallow or awareness of swallowing difficulty in patients treated for head and neck cancer with chemoradiation. Within this larger purpose, there were 2 specific aims. First, we set out to determine how measures of swallow physiology would change depending upon the type of bolus given to the patient. We hypothesized that measures of swallowing physiology would be significantly worse (longer transit times and higher amounts of residue) for more viscous and thicker boluses than for thinner or less viscous boluses, regardless of volume. Second, we wanted to observe whether patient awareness of swallowing ability varied depending upon bolus type. The hypothesis to be tested was that patients would report higher ratings of swallowing difficulty as viscosity (liquid boluses) and thickness (pudding and cookie boluses) increased, regardless of bolus volume. MATERIALS AND METHODS Subjects There were 21 patients diagnosed with head and neck cancer and treated with chemoradiation treatment. Patients were recruited through referrals from cooperating radiation oncologists, medical oncologists, and head and neck surgeons at Northwestern Memorial Hospital. The patients consisted of individuals from 36 to 80 years of age (average age, 56 years; see Table 1 for patient characteristics). These patients were diagnosed with oral, oropharyngeal, nasopharyngeal, or laryngeal tumors (see Table 2) and were treated with a full course of radiotherapy and chemotherapy. All patients received at least 60 Gy over an average of 7 weeks. Five of the 21 patients received induction chemotherapy followed by concurrent chemoradiation. The other 16 patients received concurrent chemoradiation only. Eight of the patients received surgical intervention (partial glossectomy, tonsillectomy, or neck dissection) followed by postoperative chemoradiation. The radiation delivery was intensitymodulated for all the patients but one who received conventional external-beam radiation (see Table 1). Inclusion criteria for the patient group were: (1) diagnosis of head and neck cancer by a medical doctor and (2) planned total radiation dosage of at least 50 Gy with concurrent chemotherapy. Exclusion criteria were: (1) other medical problems known to cause salivary gland hypofunction 32 and/ or dysphagia (e.g., neurological problems, gastroenterologic problems, etc), (2) prior swallowing treatment, and (3) prescribed medication that could affect swallowing. Study procedures The protocol was approved by the Institutional Review Board of Northwestern University, and all patients signed informed consent statements. Each patient was evaluated twice, once before initiation of chemoradiation treatment and once after completion of treatment. The pretreatment assessment point took place an average of 3.5 weeks before treatment began. The posttreatment assessment for the majority of patients was between 3 months and 1 year posttreatment (an average of 5 months). Three patients were up to 2 years posttreatment because of difficulty with follow-up. Data collection at each assessment point consisted of an MBSS and questions related to the patients awareness of difficulty swallowing. Modified Barium Swallow Study Each patient s swallowing was examined using a MBSS. MBSS enables visualization and measurement of the critical movements of the oropharyngeal swallow. Each patient was administered 2 boluses of each of the following consistencies: 1 and 10 ml of thin liquid barium, 3 and 10 ml of nectar thick liquid barium, 3 ml of thin paste (67% vanilla pudding and 33% EZ EM barium paste), 3 ml of standard barium paste; and one-fourth of a Lorna Doone cookie covered with 1 ml of EZ EM barium paste. All swallows were viewed in the lateral plane. All bolus volumes were measured by syringe and gently placed into the patient s mouth via either syringe or spoon. The patient was instructed to hold the bolus in his/ her mouth until directed to swallow. The specific bolus types chosen for inclusion in this study were based on the goal of representing a wide variety of bolus volumes and viscosities/thicknesses while limiting the total number of boluses administered for radiation safety. The order of presentation of these varying boluses was randomized in order to avoid any order effects, such as fatigue, that may occur. The order of presentation was the same at both assessment points so that changes in swallow physiology for particular bolus types posttreatment could be more accurately attributed to effects of chemoradiation. If a patient aspirated greater than 5% of the bolus on the first swallow of a given bolus type, the second swallow of this bolus type was not administered. Data reduction Two types of measures and observations were made from fluoroscopic recordings: (1) approximate amount (percentage) of residue as well as instances of penetration and aspiration and (2) selected temporal measurements of structural and bolus movement. MBSS data were recorded on one-half inch videotape. The measures and observations were made through visual inspection of the recordings at regular speed, slow motion, and frame-by-frame using a DVC-PRO machine. Ten percent of all swallows were reanalyzed by the same observer as well as by a different observer to determine intrajudge and interjudge reliability. Pearson correlation coefficients of intrajudge and interjudge reliability were high (0.95 0.99) for all measures. Approximate percentage of residue and instances of penetration and aspiration The only instrumentation that enables quantification of residue is scintigraphy, a nuclear medicine test involving swallows of measured amounts of a radioactive substance. Data from previous studies examining the correlations between oral residue measured from scintigraphy 33 and HEAD & NECK DOI 10.1002/HED AUGUST 2015 1123

ROGUS-PULIA ET AL. TABLE 1. Demographic variables and treatment details for all patients. Patient Age, y Sex Tumor site Tumor stage Total RT dose Induction chemo, Y/N Concurrent chemo, Y/N Chemo drugs administered Surgery Smoking/ alcohol abuse 1 36 M Nasopharynx T2bN3bM0 70 Gy Y Y TPF, cisplatin None No/No 2 48 F Nasopharynx T1N3M0 70 Gy Y Y Cisplatin, None No/No 5-fluorouracil 3 80 M Hypopharynx, T4N1M0, 70 Gy N Y Erbitux None Yes/No epiglottis T1N1M0 4 53 M Left base of T2N2bM0 70 GY Y Y Taxotere, None No/No erbitux 5 66 M Left tonsil T2N2bM0 66 Gy N Y Cisplatin Tonsillectomy Yes/Yes 6 59 M Nasopharynx T4N2M0 70 Gy Y Y TPF, cisplatin, None No/No and gemcitabine 7 55 M Right tonsil T1N2bM0 70 Gy N Y Cisplatin Tonsillectomy Yes/No 8 47 M Right oral T1N0M0 70 Gy N Y Unavailable* Partial No/No glossectomy 9 48 M Left base of T0N2bM0 70 Gy Y Y TPF, cisplatin Neck No/No dissection 10 54 M Base of T4aN2cM0 70 Gy N Y Cisplatin None No/Yes 11 59 M Left base of T1N2bM0 70 Gy N Y Cisplatin None Yes/Yes 12 45 M Right tonsil T2N2bM0 66 Gy Y Y Cisplatin Neck dissection No/No and tonsillectomy 13 76 M Right vocal T4N0M0 70 Gy N Y Cisplatin None Yes/No fold 14 56 M Unknown primary T0N1M0 70 Gy N Y Erbitux Tonsillectomy Yes/No 15 61 F Right tonsil T2N2bMX 70 Gy N Y Cisplatin Tumor Yes/Yes debulking 16 50 M Right tonsil T2N2bM0 70 Gy Y Y Carboplatin None Yes/Yes 17 67 M Base of T1N2cM0 70 Gy N Y Carboplatin None No/Yes 18 65 F Right base of T2N2bM0 70 Gy N Y Cisplatin None Yes/Yes 19 63 M Left base of T2N2bM0 72 Gy N Y Cisplatin None No/Yes 20 55 F Right base of T1N2cM0 70 Gy N Y Cisplatin Right neck Yes/No dissection 21 42 M Left palatine tonsil T2N2bM0 70 Gy N Y Cisplatin None No/No Abbreviations: RT, radiation treatment; chemo, chemotherapy; TPF, docetaxel, cisplatin, and 5-fluorouracil. * Specific chemotherapeutic agents were unavailable in this patient s electronic medical record due to treatment provided by an outside hospital. TABLE 2. Tumor location Distribution of tumor sites among patients. No. of patients Oral 1 Nasopharynx 3 Base of 8 Tonsil 5 Hypopharynx 1 Larynx (vocal folds) 1 Unknown primary 1 estimations of the amount of oral residue from the modified barium swallow indicate that observations of the approximate percentage of residue from videofluoroscopy can be accurate when done by well-trained staff. 34 The presence or absence as well as the amount of residue in the oral and pharyngeal cavities was determined. The number of instances of penetration and aspiration at different time points (before, during, or after the swallow) was recorded. Temporal analysis of bolus movement Using frame-by-frame analysis and slow motion, videoframes on which the bolus reached specific points in the oropharynx and when particular structural movements began and ended were identified. The recordings were captured at 30 frames per second (60 fields per second). The following events were recorded: (a) first backward movement of the bolus (defined as the onset of oral transit); (b) head (leading edge) of the bolus reaches the point where the ramus of the mandible crosses the base (the point by which the pharyngeal swallow should trigger); (c) beginning of laryngeal elevation (first elevation associated with the onset of the pharyngeal stage of the swallow; the arytenoid cartilages and/or true vocal folds were used as structural landmarks for this measure); and (d) end of cricopharyngeal opening (the tail of the 1124 HEAD & NECK DOI 10.1002/HED AUGUST 2015

BOLUS EFFECTS ON SWALLOWING IN PATIENTS WITH HEAD AND NECK CANCER bolus leaves the cricopharyngeal region, defined as the termination of the pharyngeal swallow). From these events, the following durational measures were made: oral transit time (OTT, b2a) 5 the time it takes the bolus to move through the oral cavity; pharyngeal delay time (PDT, c2b) 5 the time from bolus head passing the posterior edge of the ramus of the mandible until the initial observation of laryngeal elevation; pharyngeal response time (PRT, d2c) 5 the time from the onset of laryngeal elevation until the bolus tail passes through the cricopharyngeal sphincter; and pharyngeal transit time (PTT, d2b) 5 the time required for the bolus to move through the pharynx. Patient awareness of swallowing by bolus type After every swallow during the MBSS, each patient was asked to provide a rating of how difficult that particular bolus was to swallow. Patients were asked to indicate a number from 1 to 7 with 1 representing no difficulty with swallowing and 7 representing the most severe difficulty with swallowing. Statistical analysis Values for each dependent variable (percentages of residue, instances of penetration/aspiration, durational measures, and perception ratings) were averaged across trials to obtain one value per bolus type. A 2-way repeated measures analysis of variance (ANOVA) with independent variables of time (changes from pretreatment to posttreatment) and bolus type was performed for each dependent variable. A repeated measures ANOVA was also conducted at the posttreatment point to determine differences in the dependent variables based on bolus type alone. Changes in the number of penetration and aspiration instances from pretreatment to posttreatment were determined using McNemar s exact test. Pearson product-moment correlation coefficients were calculated to examine relationships between perception per bolus type and the measures of physiology for each bolus type. If a patient had missing data, which did occur for temporal data on <5% of the swallows because of difficulties with equipment or the image, then missing data specific to each analysis were excluded from that particular analysis. Correlations between the demographic variables of continuous nature (age, radiation total dose, time to pretreatment assessment, and time to posttreatment assessment) and the dependent variables in this study were also calculated at both pretreatment and posttreatment. Because there were no strong correlations present, these variables were not included as covariates in the analyses. Despite several patients with posttreatment evaluations further out from treatment completion, the time to posttreatment assessment variable did not appear to influence results. RESULTS Pretreatment to posttreatment comparison These comparisons allowed for examination of changes in percentages of residue, instances of penetration/aspiration, durational measures, perceptual ratings from pretreatment to posttreatment, and whether these changes were dependent upon the type of bolus being swallowed. FIGURE 1. Changes in mean oral residue percentages per bolus type. This figure illustrates the mean percentages of oral residue with standard error bars for each bolus type at pretreatment and posttreatment assessment points. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] Measures of swallow physiology PRT was the only durational measure that was found to be significantly longer following treatment. A two-way repeated measures ANOVA revealed a main effect for time (F (1,13) 5 4.87; p <.05) indicating longer PRTs across all bolus types posttreatment. There were no interactions or main effects present for the other individual durational measures (OTT, PDT, and PTT). Regardless of bolus type, a higher percentage of the bolus remained in both the oral (F (1,15) 5 18.94; p <.002) and pharyngeal (F (1,16) 5 10.39; p <.01) cavities after the swallow in the patients posttreatment as compared to pretreatment. There was a trend observed for higher percentages of oral and pharyngeal residue with pudding and cookie boluses as compared to other bolus types at the posttreatment point (see Figures 1 and 2). The incidence of penetration increased for certain bolus types after treatment while the incidence of aspiration did not change significantly. McNemar s exact test revealed significantly more instances of penetration posttreatment for the 10 ml thin liquid boluses (p <.03) and the 3 ml nectar-thick boluses (p <.03). There were no significant changes for the other bolus types. All instances of penetration both pretreatment and posttreatment were silent (no throat clear or cough in response). There were no instances of aspiration pretreatment, but 89% (8 of 9) of aspiration occurrences posttreatment also were silent. The one occurrence of aspiration for which a patient coughed in response was on a 3 ml nectar-thick liquid bolus (see Table 3 for the incidence of penetration and aspiration by bolus type). Patient awareness of swallowing by bolus type Patient ratings of swallowing difficulty did not vary significantly based on bolus type or time relative to treatment. The two-way repeated measures ANOVA revealed no interaction effect for bolus type by time (F (6,15) 5 1.93; p 5.436) or main effect for time (F (1,20) 5 0.147; p 5.706). However, there was a trend for ratings of swallowing difficulty to be higher on paste and cookie boluses HEAD & NECK DOI 10.1002/HED AUGUST 2015 1125

ROGUS-PULIA ET AL. FIGURE 2. Changes in mean pharyngeal residue percentages per bolus type. This figure illustrates the mean percentages of pharyngeal residue with standard errors bars for each bolus type at pretreatment and posttreatment assessment points. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] FIGURE 3. Mean perception per bolus ratings by bolus type. This figure shows the mean patient ratings for swallowing difficulty with standard errors bars for each bolus type at pretreatment and posttreatment. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] as compared to all of the liquid bolus types at the posttreatment assessment point (see Figure 3). Posttreatment comparison based on bolus type These comparisons allowed for examination of differences among bolus types for percentages of residue, instances of penetration/aspiration, durational measures, and perception ratings at the posttreatment assessment point. Measures of swallow physiology OTT and PDT were the durational measures found to vary significantly with bolus type at the posttreatment assessment point. A significant main effect for bolus type was found for OTT (Wilks lambda 5 0.295; F (6,11) 5 4.37; p <.02). Post-hoc analyses revealed that OTT was significantly longer for pudding boluses as compared to 1 ml thin liquid, 10 ml thin liquid, 3 ml nectar-thick liquid, and 10 ml nectar-thick liquid. OTT was significantly shorter for cookie boluses as compared to 1 ml thin liquid, 10 ml nectar-thick liquid, thin pudding, and standard pudding boluses. A significant main effect for bolus type also was found for PDT (Wilks lambda 5 0.245; F (6,10) 5 5.13; p 5.012) with significantly shorter PDTs for cookie boluses as compared to all other bolus types. There were no significant effects for PRT or PTT. There were no significant effects for bolus type for the oral and pharyngeal residue levels or instances of penetration or aspiration. Patient awareness of swallowing by bolus type At the posttreatment point, awareness of swallowing difficulty did not differ between bolus types. A repeated measures ANOVA showed no significant effect for bolus type (Wilks lambda 5 0.501; F (6,15) 5 2.49; p 5.071). Correlations between perception and physiology by bolus type No significant correlations were found between patient awareness ratings and the following measures: oral residue, OTT, PRT, PDT, or PTT. For the pudding bolus only, there was a moderate, positive correlation between percentage of pharyngeal residue and the awareness rating (r 5 0.508; p <.02; see Table 4). As the amount of pharyngeal residue increased on pudding boluses, patients perceived more difficulty swallowing the pudding. Summary of results In summary, results revealed longer PRTs as well as more residue in the oral cavity and pharynx for all bolus types following treatment. There were higher incidences of penetration on 10 ml thin liquid and 3 ml nectarthick liquid boluses after treatment. Patient perception of swallowing difficulty did not change significantly TABLE 3. Pretreatment and posttreatment incidence of penetration and aspiration by bolus type. Bolus type Pretreatment: penetration occurrences Posttreatment: penetration occurrences Pretreatment: aspiration occurrences Posttreatment: aspiration occurrences 1 ml thin liquid 0 3 0 1 10 ml thin liquid 2 6 0 2 3 ml nectar-thick liquid 1 6 0 3* 10 ml nectar-thick liquid 0 5 0 1 3 ml thin puree 0 1 0 0 3 ml standard puree 0 3 0 2 Cookie 0 1 0 0 * The one instance in which a patient coughed in response to aspiration was on this bolus type (8 of 9 occurrences were silent ). 1126 HEAD & NECK DOI 10.1002/HED AUGUST 2015

BOLUS EFFECTS ON SWALLOWING IN PATIENTS WITH HEAD AND NECK CANCER TABLE 4. Correlations between perception ratings and measures of swallow physiology by bolus type. Perception ratings by bolus type OTT PRT PDT PTT Oral residue Pharyngeal residue 1 ml thin liquid 0.258 0.065 20.076 20.061 0.029 0.108 10 ml thin liquid 0.152 20.225 0.105 20.133 0.012 0.144 3 ml nectar-thick liquid 20.044 20.044 20.102 0.126 20.046 0.066 10 ml nectar-thick liquid 20.093 20.188 0.102 20.05 0.098 0.159 3 ml thin puree 20.125 20.323 0.063 20.091 20.204 20.088 3 ml standard puree 20.028 0.053 0.059 0.064 20.128 0.508* Cookie 0.357 20.224 20.113 20.220 20.167 0.415 Abbreviations: OTT, oral transit time; PRT, pharyngeal response time; PDT, pharyngeal delay time; PTT, pharyngeal transit time. * Asterisk denotes a statistically significant Pearson s correlation coefficient. following treatment despite documented worsening of swallowing function, as stated above. However, there were trends for slightly higher ratings on pudding and cookie boluses. Following treatment, OTT was longest for pudding boluses and shortest for cookie boluses. PDT was shortest for cookie boluses. There was only one significant correlation between patient awareness ratings and measures of swallow physiology by bolus type. DISCUSSION The purpose of this study was to clarify whether changes in measures of swallow physiology and patient awareness of swallowing difficulty after chemoradiation treatment are dependent upon the type of bolus swallowed. Increased amounts of residue in the oral cavity and pharynx as well as longer PRTs posttreatment occurred across all bolus types. When comparing bolus types, there were significantly longer OTTs for pudding boluses as well as trends toward higher amounts of residue and patient ratings of swallowing difficulty for pudding and cookie boluses. By randomizing the order of bolus presentation, the results observed could be more accurately attributed to variations in swallowing related to bolus type rather than to potential fatigue effects. The higher percentages of residue observed in the oral cavity and pharynx along with longer PRTs after treatment could reflect fibrosis of the head and neck musculature resulting in reduced strength and therefore poor pharyngeal constriction. This may lead to more difficulty clearing the pharynx during the swallow. The role of salivary gland hypofunction 32 resulting from inclusion of salivary glands in the radiation field also may contribute to increased amounts of residue. Decreased production of saliva (hyposalivation) may result in less coating of oral and pharyngeal structures as well as poor lubrication of the bolus that becomes critical to transport. There were significantly longer OTTs at the posttreatment point for pudding boluses as compared to multiple liquid bolus types. These changes could be due to known fibrosisrelated decreases in lingual strength after chemoradiation treatment. 3,35 37 They also may be related to salivary gland hypofunction resulting in poor lubrication, which could impact the transport of viscous boluses to a greater degree. However, the OTTs for cookie boluses, not including mastication times, were found to be significantly shorter as compared to multiple liquid boluses and pudding boluses. This unexpected finding could be related to possible stimulation of saliva, which occurs during mastication and may improve bolus transport in patients with salivary gland hypofunction. In addition, OTT reflects duration of bolus transit through the oral cavity and into the pharynx after completion of mastication. Future research should include an additional measure of oral preparation or mastication time as this may be prolonged in patients after treatment due to salivary gland hypofunction and/or reductions in lingual strength. In addition, PDTs that reflect the timing of the pharyngeal response were shorter for cookie boluses. This was again an unexpected finding since typically, while chewing, some of the bolus moves into the vallecular space. This finding reflects the way cookie boluses were analyzed during frame-by-frame analysis of videofluoroscopic recordings. When determining PDT, the arrival of the bolus into the pharynx was considered as it relates to initiation of the oral transport during the swallow and not entry into the vallecular space during chewing. It is also possible that the additional sensory stimulation provided by the process of mastication will explain quicker triggering of the swallow with cookie boluses. Findings of increased frequency of penetration during the swallow for 10 ml thin liquid and 3 ml nectar-thick boluses is consistent with findings by Daggett et al 38 who reported a lower incidence of penetration with non-liquid (and thicker) consistencies in normal subjects. The lower frequencies of penetration with the higher (10 ml) volume nectar-thick bolus type as compared to a lower volume (3 ml) nectar-thick bolus type conflict with previous research findings that suggest more frequent occurrences of penetration with increased bolus volumes. 38 It may be that the combination of a larger and slightly thicker bolus (as compared to thin liquid) provides increased sensory input during the swallow that results in improved airway protection. This emphasizes the clinical need to examine the effect of thickened liquids in these patients as one cannot assume that thickened liquids will continue to reduce penetration without examining their effect across volumes. Although the increase in number of aspiration occurrences posttreatment was nonsignificant, the majority of occurrences were silent (no throat clear or cough in response). These findings reflect sensory deficits that result in decreased patient awareness and support the concern over silent aspiration in this patient population. Although nonsignificant, there were trends toward higher HEAD & NECK DOI 10.1002/HED AUGUST 2015 1127

ROGUS-PULIA ET AL. amounts of oral and pharyngeal residue for pudding and cookie boluses than for other bolus types at the posttreatment point. This is consistent with previous work showing higher levels of residue for thicker boluses. 39 41 Another nonsignificant trend toward higher patient ratings of swallowing difficulty for pudding and cookie boluses also was observed. It is possible that, with a larger sample size, the relatively larger increases in percentages of residue and perception ratings observed with pudding and cookie boluses would reach significance. There were several limitations to this study. Patients with head and neck cancer varied in terms of tumor site and location as well as size of radiation field, exact chemoradiation treatment protocol, and smoking or alcohol history. A subset of the patients received some type of surgical intervention followed by chemoradiation. Due to varying types of surgery (tonsillectomy, partial glossectomy, and neck dissection) and the small number of patients in this category, it was not possible to determine differential effects of specific types of surgery. This is an important area for future research with a larger overall sample size. The time from completion of treatment to posttreatment assessment varied in our patient group as well. Several patients were assessed at a later point as compared to the rest of the group due to difficulty with follow-up closer to treatment completion secondary to acute effects. Despite nonsignificant trends of higher patient perception ratings and amounts of residue with pudding and cookie bolus, only one correlation between percentages of pharyngeal residue and patient perception ratings for a pudding bolus was significant. If patient awareness of swallowing closely reflects changes in swallow physiology, more correlations that are positive would be expected. Therefore, the lack of significant correlations observed in this study suggests some level of disconnect between patient awareness of swallowing and swallowing function. Pauloski et al 31 reported general agreement between perception and physiology for multiple bolus types; however, perceptions of swallowing difficulty in this study were not bolus-specific. When patients were asked to rate difficulty of swallowing for each bolus type in our study, this consistent level of agreement was not observed. Overall, patient ratings of difficulty were low (<3). It may be that patients do not observe as much difficulty swallowing as would be expected from the observed changes in swallowing physiology. This relatively poor awareness of any swallowing difficulty may be the reason patients often continue to swallow foods that are not safe or efficient for them. Future research should focus on other potential mediating factors of this relationship between patient awareness of swallowing difficulty and physiology, such as salivary hypofunction and oropharyngeal sensation. Acknowledgments The authors thank Muveddet Harris for assistance with data reduction; Kristin Larsen, Sharon Veis, Cory Atkinson, and Megan Schliep for assistance with subject recruitment; and Charles Larson for editorial feedback. This manuscript was partially prepared within the Geriatric Research Education and Clinical Center (GRECC Manuscript #2014-014) at the William S. Middleton Veteran Affairs Hospital in Madison, WI. The views and content expressed in this article are solely the responsibility of the authors and do not necessarily reflect the position, policy, or official views of the Department of Veteran Affairs or U.S. government. REFERENCES 1. Manikantan K, Khode S, Sayed SI, et al. Dysphagia in head and neck cancer. Cancer Treat Rev 2009;35:724 732. 2. 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