Dysphagia DOI 10.1007/s00455-013-9500-y
ORIGINAL ARTICLE
Changes in Swallowing Physiology and Patient Perception of Swallowing Function Following Chemoradiation for Head and Neck Cancer Nicole M. Rogus-Pulia • Margaret C. Pierce Bharat B. Mittal • Steven G. Zecker • Jeri A. Logemann
•
Received: 8 May 2013 / Accepted: 22 November 2013 Ó Springer Science+Business Media New York (outside the USA) 2014
Abstract Patients treated with chemoradiation for head and neck cancer often report difficulty with swallowing and are frequently diagnosed with dysphagia. The extent to which patient awareness of dysphagia corresponds to observed physiologic changes in swallowing is unclear. The purpose of this study was to determine how both patient awareness of swallowing function and swallowing physiology individually change following chemoradiation and then to clarify the relationship between them. Twentyone patients with head and neck cancer treated with chemoradiation were assessed before and after treatment and matched with twenty-one control subjects. The modified barium swallow test was utilized to examine swallowing physiology. Each subject was also given a series of items regarding awareness of specific dysphagia symptoms. N. M. Rogus-Pulia (&) William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison GRECC (11G), Room D5216, Madison, WI 53705, USA e-mail: [email protected] N. M. Rogus-Pulia Department of Medicine, School of Medicine and Public Health, Speech, Swallowing, and Dining Enhancement Program, University of Wisconsin-Madison, Madison, WI, USA M. C. Pierce Radiation Oncology, Northwestern Memorial Hospital, Chicago, IL, USA B. B. Mittal Department of Radiation Oncology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA S. G. Zecker J. A. Logemann Department of Communication Sciences and Disorders, Northwestern University, Frances Searle Building, Evanston, IL 60208, USA
Results showed decreased swallow efficiencies, higher percentages of residue, and more occurrences of penetration and aspiration following chemoradiation. Patients also had significantly higher ratings for 4 of the 12 items (‘‘dry mouth,’’ ‘‘food sticking in my mouth,’’ ‘‘need water to help food go down,’’ and ‘‘change in sense of taste’’). Only one strong and significant correlation was found between ratings for ‘‘I have difficulty swallowing’’ and swallow efficiency values. Based on these findings, it appears that patients sense a general difficulty with swallowing but have less awareness of specific symptoms of dysphagia. Keywords Deglutition Deglutition disorders Dysphagia Chemoradiation Head and neck cancer Perception Swallow efficiency
Introduction Patients with head and neck cancer often report symptoms of dysphagia following chemoradiation treatment [1–4]. Patient perception of illness is a well-established determinant of adherence to medical treatment recommendations [5]. However, difficulties with patient nonadherence to dietary and liquid modifications for dysphagia have been linked to poor patient awareness of their condition [6–8]. Nonadherence with therapeutic recommendations is associated with a significantly increased mortality risk related to the development of aspiration pneumonia [9]. A clearer understanding of the relationships among specific aspects of patient perception and physiologic dysfunction is critical to future development of educational interventions that may improve patient adherence. The degree to which patient perception of swallow function agrees with objective measures of swallow
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N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
physiology has not been well-defined. Results of studies that examined patient perception of swallowing difficulty include information about the level of agreement between physiology and a global awareness of swallowing [1–4] but no data on which specific aspects of swallowing patients perceive to be problematic. The impact of chemoradiation treatment on the quality of life of patients with head and neck cancer has been examined extensively [10]. Current quality-of-life rating scales focus on the functional impact of dysphagia on the patient’s life as a whole [11]. Although there are subscales included within these comprehensive quality-of-life scales with questions related to specific dysphagia symptoms, these items comprise a relatively small part of the overall measure. Results from studies in other patient populations that examined the relationship between patient perception and objective measures of swallowing have yielded conflicting results. Several authors reported a discord between patient perception and actual swallow function [12–15]. Others have found a more consistent match between subjective complaints and objective measures of swallowing [16–22]. The few studies that examined patients with head and neck cancer have mixed findings. Walther and Deroover [4] and Rhodus et al. [16] found a link between perception and motility disturbances. A study by Pauloski et al. [23] concluded that patients with complaints of difficulty swallowing had lower swallow efficiency scores, longer oral and pharyngeal transit times, greater oral and pharyngeal residue, and more swallows with aspiration than those without complaints. In contrast, Hughes et al. [24] reported no significant relationship between patient complaint of dysphagia and videofluoroscopic findings. A limitation of this previous work has been the use of perception questionnaires with yes/no responses [20, 23– 26]. In order to find direct correlations with objective measures taken from videofluoroscopic recordings of swallowing, it is necessary to quantify the degree to which patients perceive each problem. Therefore, we have utilized Likertscale responses to a series of questions taken partly from a previously used questionnaire by Pauloski et al. [23] and Logemann et al. [25, 26] as well as another commonly used questionnaire developed by Wallace et al. [27]. This study was designed to provide new insights into the complex relationship between patient awareness of dysphagia and swallowing physiology in post-chemoradiation patients with head and neck cancer. The objectives of this study were (1) to more clearly define changes in patient perception of swallowing function following chemoradiation treatment by administering a series of questions about specific dysphagia symptoms requiring Likert-scale responses and (2) to clarify relationships among patient perception of swallowing function and swallowing physiology. Our hypothesis, based on previous work that examined changes in patient perception of
123
swallowing following chemoradiation treatment [23], was that patients would perceive more difficulty with swallowing overall and that these perception ratings would correlate highly with measures of physiology.
Methodology Subjects There were two groups of subjects: (1) 21 patients diagnosed with head and neck cancer and treated with chemoradiation treatment and (2) 21 age- and gender-matched control subjects. Patients were recruited through referrals from the Radiation Oncology and Medical Oncology centers and the Speech and Swallowing Clinic at Northwestern Memorial Hospital. Cooperating radiation oncologists, medical oncologists, and head and neck surgeons helped to identify patients suitable for the study. The patient group consisted of individuals who were from 36 to 80 years of age (average age = 56 years). These patients were diagnosed with oral, oropharyngeal, nasopharyngeal, or laryngeal tumors and treated with a full course of radiotherapy and chemotherapy. All patients received at least 66 Gy over an average of 7 weeks with concurrent and/or induction chemotherapy. The radiation delivery was intensity-modulated for all the patients except one who received conventional external-beam radiation (see Table 1 for patient characteristics). Inclusion criteria for the patient group were (1) diagnosis of head and neck cancer by a medical doctor, (2) age 30–80 years, and (3) planned total radiation dosage of at least 50 Gy with concurrent chemotherapy. Exclusion criteria were (1) other medical problems known to cause dysphagia (e.g., neurological problems, gastroenterological problems), (2) prior swallowing treatment, and (3) prescribed medication that could affect swallowing. The control group consisted of 21 normal subjects ranging in age from 31 to 77 years (average age = 56 years). These subjects were eligible for participation if they (1) matched with a patient with respect to gender and age (±5 years), (2) did not complain of or have a history of dry mouth, (3) did not have a history of dysphagia, or (4) were not taking any medication that could affect swallowing. Study Procedures The protocol was approved by the Institutional Review Board and all subjects signed informed consent statements. Each patient with head and neck cancer was evaluated twice, once prior to initiation of chemoradiation treatment and once after completion of treatment. The pre-treatment assessment took place an average of 3.5 weeks before treatment began. The post-treatment assessment for the majority of patients
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 1 Patient characteristics Subject Age Sex Tumor site
Tumor stage
Total RT Induction Concurrent Surgery dose (Gy) chemo chemo (Y/N) (Y/N)
Smoking/ alcohol abuse
1
36
M
Nasopharynx
T2bN3bM0
70
Y
Y
None
No/No
2
48
F
Nasopharynx
T1N3M0
70
Y
Y
None
No/No
3
80
M
Hypopharynx, epiglottis T4N1M0, T1N1M0
70
N
Y
None
Yes/No
4
53
M
Left base of tongue
T2N2bM0
70
N
Y
None
No/No
5
66
M
Left tonsil
T2N2bM0
66
N
Y
Tonsillectomy
Yes/Yes
6
59
M
Nasopharynx
T4N2M0
70
Y
Y
None
No/No
7
55
M
Right tonsil
T1N2bM0
70
N
Y
Tonsillectomy
Yes/No
8
47
M
Right oral tongue
T1N0M0
70
N
Y
Partial glossectomy
No/No
9
48
M
Left base of tongue
T0N2bM0
70
Y
Y
Neck dissection
No/No
10
54
M
Base of tongue
T4aN2cM0
70
N
Y
None
No/Yes
11
59
M
Left base of tongue
T1N2bM0
70
N
Y
None
Yes/Yes
12
45
M
Right tonsil
T2N2bM0
66
Y
Y
Neck dissection and tonsillectomy No/No
13
76
M
Right vocal fold
T4N0M0
70
N
Y
None
14
56
M
Unknown primary
T0N1M0
70
N
Y
Tonsillectomy
Yes/No
15
61
F
Right tonsil
T2N2bMX
70
N
Y
Tumor debulking
Yes/Yes
16
50
M
Right tonsil
T2N2b/cM0 70
Y
Y
None
Yes/Yes
17 18
67 65
M F
Base of tongue Right base of tongue
T1N2cM0 T2N2bM0
70 70
N N
Y Y
None None
No/Yes Yes/Yes
19
63
M
Left base of tongue
T2N2bM0
72
N
Y
None
No/Yes
20
55
F
Right base of tongue
T1N2cM0
70
N
Y
Right neck dissection
Yes/No
21
42
M
Left palatine tonsil
T2N2bM0
70
N
Y
None
No/No
Yes/No
RT radiation treatment, Chemo chemotherapy, Y yes, N no, M male, F female, T tumor, N node, M metastasis
was between 3 months and 1 year after treatment (an average of 5 months). Three patients were assessed up to 2 years post-treatment due to difficulty with follow-up. The control subjects were evaluated only once and underwent the same procedures as the patient group. Data collection procedures at each assessment point included responses to a series of questions about specific dysphagia symptoms and the modified barium swallow test. Patient Perception of Swallow Function There were 12 questions regarding swallowing function that were administered to each subject (see Table 2 for a list of questions). These items were taken from a questionnaire used in previous studies by Logemann et al. [28]. However, in this study, the required responses were on a 7-point Likert scale versus yes/no responses used previously. Most of these questions also were similar to those included in a tool developed by Wallace et al. [27], except this questionnaire included a question about the severity of dry mouth, a common symptom for patients following chemoradiation treatment that likely affects swallowing. Also, the tool developed by Wallace et al.
[27] utilized a visual analog scale. A Likert-scale design was preferred in this study due to its ease of administration and interpretation [29]. Each item required a rating of 1–7 (1 indicating no difficulty with the perceived problem and 7 indicating the most severe difficulty). This perception assessment had a minimum summated score of 12 and a maximum of 84. Inter-item correlations were determined to examine potential overlap between the 12 items on the questionnaire (Table 3). Correlations were calculated for the patient group at both the pre-treatment and the posttreatment assessment points and for the control group. As is seen in Table 3, the items that were both strongly and significantly correlated differed based on group as well as assessment point, suggesting that the perception measured by each item may vary depending on disease and treatment status. Therefore, all items were retained for use in this study. The Modified Barium Swallow Test (MBST) Each subject’s swallowing was examined using a modified barium swallow test. The MBST enables visualization and
123
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 2 Items administered for perception of swallowing assessment 1
I have difficulty swallowing
2
I have a dry mouth
3
Food sticks in my mouth
4
Food sticks in my throat
5
I find that food won’t go down
6
I need to drink water to help food go down
7
I choke on food/liquid
8
I have found that I cough when eating and/or drinking
9
I experience food/liquid coming back up after I swallow
10
I experience heartburn
11
I wake up at night coughing and/or gagging
12
I have experienced a change in my sense of taste
measurement of the critical movements of the oropharyngeal swallow. Each subject was administered two 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 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 placed into the patient’s mouth via syringe or spoon. The patient was instructed to hold the bolus in his/her mouth until directed to swallow. 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 swallowing physiology on particular bolus types could be attributed more accurately to effects of chemoradiation. If a patient aspirated [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 Three types of measures and observations were made from videofluoroscopy: (1) approximate amount (percentage) of residue, (2) frequency of penetration and aspiration, and (3) selected temporal measurements of structural and bolus movement. Data from the videofluoroscopic studies were recorded on 0.5-inch. videotape. The measures and observations were made through visual inspection of the recordings at regular speed, slow motion, and frame-byframe using a DVC-PRO machine. Intrarater and interrater reliabilities were calculated for 10 % of all swallows and were found to be high (95–99 % agreement) for all measures and observations.
123
Approximate Percent Residue 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 that examined the correlations between oral residue measured with scintigraphy and estimations of the amount of oral residue from the modified barium swallow indicate that observations of approximate percent residue from videofluoroscopy can be accurate when done by well-trained staff [28]. The presence or absence and the amount of residue if present in the oral and pharyngeal cavities were determined. Values for each measure were averaged across trials in order to obtain a value per bolus type for each subject. Then, overall measures were obtained by averaging measures across bolus types for each subject. Frequency of Penetration and Aspiration For each swallow, the presence or absence of penetration and aspiration was recorded. The time point (before, during, or after the swallow) was also noted. The total number of penetration or aspiration occurrences at each time point was calculated by summing frequencies across all swallows within each group. Temporal Measures of Bolus Movement Using frame-by-frame analysis and slow motion, specific video frames 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 tongue base, which is 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), and (d) end of cricopharyngeal opening (the tail of the 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, b-a), the time it takes the bolus to move through the oral cavity; pharyngeal delay time (PDT, c-b), the time from when the bolus head passes the posterior edge of the ramus of the mandible until the initial observation of laryngeal elevation; pharyngeal response time (PRT, d-c), the time from the onset of laryngeal elevation until the bolus tail passes through the cricopharyngeal sphincter; and pharyngeal transit time (PTT, d-b), the time
0.32
Controls
-0.18
0.34
Controls
0.445*
Pre-tx patients
0.41
Controls
Post-tx patients
0.808* 0.438*
Pre-tx patients
Post-tx patients
0.07 0.11
Post-tx patients Controls
0.08
Controls 0.124
0.3
Post-tx patients
Pre-tx patients
0.405*
0.36
Controls
Pre-tx patients
0.3
Post-tx patients
0.41 0.783
Controls
Pre-tx patients
0.36
Post-tx patients
0.460*
Controls 0.193
0.448*
Post-tx patients
Pre-tx patients
0.280
-0.22
Pre-tx patients
Controls
0.111 0.44*
0.434*
Post-tx patients
Pre-tx patients Post-tx patients
0.330
Pre-tx patients
Controls
*The asterisk denotes statistical significance
Change in taste
Wake at night cough/gag
Heartburn
Food comes back up
Cough
Choke
Need water
Food won’t go down
Food sticks in throat
0.36 0.15
Post-tx patients
0.493* -0.057
Controls
Pre-tx patients
0.485*
Post-tx patients
Food sticks in mouth
0.291
Pre-tx patients
Dry mouth
Difficulty swallowing
Group and/or assessment point
Items on perception assessment
-0.29
0.23
0.377
0.666*
0.739*
0.251
0 0.11
0.169
-0.18
0.33
0.571*
0.736*
0.528*
0.045
0.736*
0.3
-0.134
0.29
0.41
0.700*
0.19
0.563* 0.556*
0.703*
0.31
0.506*
0.24
0.39
0.12
–
Dry mouth
Table 3 Interitem correlational matrix for patient and control groups
-0.149
0.26
0.39
0.284
0.515*
-0.119
0.02 0.062
0.313
0.274
0.559*
0.134
0.031
0.25
-0.045
-0.051
0.36
0.134
-0.030
0.12
0.364
0.031
0.397 0.556*
0.098
0.717*
0.316
–
–
Food sticks in mouth
0.01
0.29
0.389
0.893*
0.28
0.111
0.14 0.27
-0.168
-0.14
0.503*
0.228
0.777*
0.09
0.173
0.819*
0.41
-0.091
0.11
0.16
0.795
0.2
0.909 0.38
–
–
–
Food sticks in throat
0.559*
0.25
0.486*
0.18
0.512*
-0.006
-0.07 0.491*
-0.086
0.3
0.784*
0.273
0.28
0.698*
-0.054
0.26
0.800*
-0.064
0.2
-0.14
0.885*
–
–
–
–
Food won’t go down
-0.143
0.367
0.549*
0.095
0.368
0.136
0.178 -0.047
0.01
0.092
-0.315
0.689*
0.431
-0.007
0.024
0.106
-0.204
-0.073
–
–
–
–
–
Need water
-0.03
0.127
-0.118
0.759*
0.275
0.103
0.073 0.43
0.751*
-0.13
0.867*
-0.050
0.821*
0.534*
0.368
–
–
–
–
–
–
Choke
-0.17
0.075
0.095
0.732*
0.397
0.669*
-0.183 0.13
0.280
-0.23
0.520
0.134
–
–
–
–
–
–
–
Cough
0.057
-0.121
0.379
-0.262
0.261
0.290
0.121 0.542*
0.156
–
–
–
–
–
–
–
–
Food comes back up
0.297
-0.161
0.028
0.183
-0.195
-0.013
–
–
–
–
–
–
–
–
–
Heartburn
0.143
0.323
0.624*
–
–
–
–
–
–
–
–
–
–
Wake at night cough/gag
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
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N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
required for the bolus to move through the pharynx. For each measure, values were averaged across trials to obtain a value for each bolus type per subject. Then, overall measures were obtained by averaging each measure across all bolus types for each subject. Oropharyngeal Swallow Efficiency The oropharyngeal swallow efficiency (OPSE) for each swallow was also calculated. The OPSE attempts to quantify the interaction of bolus speed and clearance of material from the oropharynx [30]. OPSE is calculated using the following equation:
the perception assessment and measures of swallow physiology (oral residue, pharyngeal residue, and OPSE). If a subject had missing data, which occurred when subjects aspirated more than 5 % of the initial bolus and in rare cases of difficulties with equipment or image clarity, then missing data specific to each analysis were excluded from that analysis. Correlations between the demographic variables of continuous nature (age, radiation total dose, time to pre-treatment assessment, time to post-treatment assessment) and the dependent variables in this study were also calculated. Since there were no strong or significant correlations present, these variables were not included as covariates in the analyses.
100 ðoral residue þ pharyngeal residue þ aspiration before swallow þ aspiration during swallowÞ : oral transit time + pharyngeal delay time + pharyngeal response time
OPSE scores typically range from 100 (100 % of the bolus is swallowed in 1 s) to 140 in normal subjects as the bolus becomes thicker. With disordered swallowing, the OPSE drops lower as the percentage of bolus swallowed decreases and the time increases. Scores for the two swallows for each bolus type were averaged in order to obtain one value of each measure per bolus type for each subject. A measure of overall OPSE was determined by averaging this measure across all bolus types for each subject. Statistical Analysis Repeated-measures analyses of variance (ANOVA) were conducted to examine changes in summated scores as well as ratings for each individual item on the perception assessment and all measures of swallow physiology (OTT, PDT, PRT, PTT, oral residue, pharyngeal residue, and OPSE) from pretreatment to post-treatment. One-way between-groups ANOVA were conducted to compare the control group to the patient group at each time point separately on each of these same dependent variables. McNemar’s test was used to test for differences in the frequencies of penetration during the swallow from pre- to posttreatment. Due to low numbers per cell, McNemar’s exact test was used to determine changes in the frequencies of aspiration during and after the swallow from pre- to post-treatment. v2 or Fisher’s exact test was used to test for differences in the frequencies of penetration and aspiration between the patient group at both assessment points and the control group. Pearson product-moment correlation coefficients were calculated within the patient group post-treatment to examine the relationships between ratings for the items on
123
Results Item Analysis and Summated Scores for Perception Questionnaire Summated scores increased significantly from pre- to posttreatment [Wilks’ lambda = 0.632, F(1,20) = 11.66, p \ 0.005]. Scores were also significantly higher for the patient group post-treatment than for the control group [F(1,40) = 16.8, p \ 0.001]. Significant increases in ratings were found from pre- to post-treatment for the following items: ‘‘dry mouth’’ [Wilks’ lambda = 0.404, F(1,20) = 6.56, p \ 0.001], ‘‘food sticks in my mouth’’ [Wilks’ lambda = 0.753, F(1,20) = 6.56, p \ 0.002], ‘‘need water to help food go down’’ (Wilks’ lambda = 0.575, F(1,20) = 14.75, p \ 0.002], and ‘‘change in sense of taste’’ [Wilks’ lambda = 0.684, F(1,20) = 9.22, p \ 0.01]. These same items, as well as ‘‘difficulty swallowing’’ [F(1,40) = 22.04, p \ 0.0001], were rated significantly higher in the patient group at the posttreatment assessment point compared to the control group. The item with the highest rating overall post-treatment was ‘‘I have a dry mouth’’ (see Fig. 1 for illustration of these results). Only one item, ‘‘difficulty swallowing,’’ was rated significantly higher in the patient group at the pre-treatment assessment point compared to the control group [F(1,40) = 6.88, p \ 0.02]. Measures of Swallowing Physiology Residue There were significantly greater amounts of oral residue posttreatment as compared to pre-treatment [Wilks’ lambda =
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Fig. 1 Ratings for each individual item given as part of the perception assessment before and after chemoradiation treatment
Table 4 Mean and standard deviation for measures of swallowing physiology
Items that correspond to numbers on x-axis: 1. Difficulty swallowing 2. Dry mouth 3. Food stick mouth 4. Food stick throat 5. Food won’t go down 6. Need water 7. Choke 8. Cough 9. Comes back up 10. Heartburn 11. Wake at night 12. Change in taste
Measure Oral transit time
Pharyngeal delay time
Pharyngeal response time
Pharyngeal transit time
Oral residue
Pharyngeal residue
0.421, F(1,20) = 27.45, p \ 0.001]. There were also significant differences in oral residue between the post-treatment patient group and the control group [F(1,40) = 21.62, p \ 0.001]. Pharyngeal residue overall increased significantly from pre-treatment to post-treatment [Wilks’ lambda = 0.629, F(1,20) = 11.79, p \ 0.005]. Again, there were significant differences between the post-treatment patient group and the control group [F(1,40) = 11.65, p \ 0.002]. Means and standard deviations are displayed in Table 4. Frequency of Penetration and Aspiration There were no instances of penetration or aspiration before the swallow in either group. Following treatment, six patients
Group
Mean
Standard deviation
Control
0.478
0.169
Patient (pre-treatment)
0.496
0.210
Patient (post-treatment)
0.666
0.535
Control
0.120
0.314
Patient (pre-treatment)
0.062
0.285
Patient (post-treatment)
0.077
0.196
Control
0.819
0.114
Patient (pre-treatment)
0.754
0.083
Patient (post-treatment)
0.816
0.112
Control
0.933
0.332
Patient (pre-treatment) Patient (post-treatment)
0.817 0.891
0.265 0.191
Control
2.28
1.56
Patient (pre-treatment)
2.81
2.83
Patient (post-treatment)
5.73
3.01
Control
2.56
1.85
Patient (pre-treatment)
2.88
1.90
Patient (post-treatment)
11.77
12.22
were found to have penetration during the swallow compared to two patients before treatment. As a group, the patients at post-treatment had significantly more occurrences of penetration during the swallow (25 occurrences out of 149 swallows, p \ 0.0001) than at pre-treatment (3 occurrences). One patient was found to aspirate during the swallow and two were found to aspirate after the swallow post-treatment compared to none pre-treatment. There was a nonsignificant increase in frequency of aspiration during the swallow from before (no occurrences) to after (3 occurrences) treatment. Aspiration after the swallow occurred significantly more frequently (6 occurrences) after treatment than before (no occurrences, p \ 0.05). The patients at post-treatment also had significantly more occurrences of penetration during the swallow
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N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
treatment, correlations were calculated between the specific measures that influence the swallow efficiency calculation (oral transit time, pharyngeal delay time, pharyngeal response time, oral residue, and pharyngeal residue) and the ratings for the items on the PPSFQ that were found to increase significantly following treatment. The only significant correlation was between the item ‘‘Need water to help food go down’’ and oral residue overall (r = -0.457, p \ 0.05) (see Table 5 for these correlations). Fig. 2 Temporal measures for patients before and after chemoradiation treatment. HN head and neck cancer, Pre before chemoradiation treatment, Post after chemoradiation treatment, OTT oral transit time, PDT pharyngeal delay time, PRT pharyngeal response time, PTT pharyngeal transit time
(p \ 0.001) and aspiration after the swallow (p \ 0.03) than the control group (no occurrences of penetration or aspiration). All occurrences of aspiration during the swallow and 83 % of occurrences of aspiration after the swallow were ‘‘silent’’ (no throat clear or cough in response). Individual Temporal Measures Pharyngeal response time was the only measure found to be significantly longer post-treatment [Wilks’ lambda = 0.677, F(1,20) = 9.54, p \ 0.01] as compared to pre-treatment within the patient group (Fig. 2). Oropharyngeal Swallow Efficiency Within the patient group, overall OPSE values decreased significantly from pre-treatment to post-treatment [Wilks’ lambda = 0.542, F(1,20) = 16.88, p \ 0.002]. There were also lower swallow efficiency values in the post-treatment patient group than in the control group [F(1,39) = 5.36, p \ 0.05]. There were two instances where the OPSE values actually increased from pre-treatment to post-treatment and both patients had tonsillar tumors. Relationships Between Individual Perception Questionnaire Items and OPSE At the post-treatment assessment point in the patient group, there was a significant negative correlation between the ‘‘difficulty swallowing’’ item and OPSE overall (r = 0–0.652, p \ 0.002). Summated scores from the questionnaire were not found to be significantly correlated with any measure of swallow physiology. In order to determine which specific aspects of physiology may underlie the change in perception post-
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Exclusion of Patients with Tonsillar Tumors Based on observed increases in OPSE values from pre- to post-treatment for two of the five patients in this study with tonsillar tumors, it is possible that patients with tonsillar tumors may respond differently to chemoradiation treatment. Therefore, data also were analyzed after exclusion of those with tonsillar tumors. This smaller sample size (n = 16) required use of the nonparametric Wilcoxon signed-rank test for continuous data and McNemar’s test for binary data. Differences in results after exclusion of those with tonsillar tumors were significant increases in oral transit time (p = 0.008) and pharyngeal transit time (p = 0.014) following treatment. Surgical Versus Nonsurgical Intervention A number of those in the patient group received some type of surgical intervention in addition to chemoradiation treatment. The effects of surgery on changes from before to after treatment were examined by subdividing the overall patient group into those who received surgical intervention (n = 8) and those who did not (n = 13). Changes in all dependent variables were examined for both subgroups separately using nonparametric statistics due to the smaller group sizes. For the surgical subgroup, significant increases in ratings for ‘‘dry mouth’’ (p B 0.01), ‘‘food sticks in my mouth’’ (p \ 0.05), ‘‘need water to help food go down’’ (p \ 0.02), and ‘‘change in sense of taste’’ (p \ 0.05) on the perception assessment were consistent with findings for the overall patient group. However, only ratings for ‘‘dry mouth’’ (p \ 0.05) and ‘‘need water to help food go down’’ (p \ 0.05) increased significantly for the nonsurgical subgroup. For measures of swallow physiology in the surgical subgroup, oral transit time (p \ 0.01), pharyngeal response time (p \ 0.02), pharyngeal transit time (p \ 0.02), amounts of oral residue (p \ 0.002), and pharyngeal residue (p \ 0.002) increased significantly following treatment. OPSE values also decreased significantly (p \ 0.001). In the nonsurgical subgroup, the only significant finding was an increase in oral residue (p \ 0.05).
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 5 Correlations between perception questions and measures of swallow physiology Individual items
Oral transit time
Pharyngeal delay time
Pharyngeal response time
Oral residue
Pharyngeal residue
Dry mouth
r = 0.231
r = 0.07
r = -0.139
r = -0.129
r = 0.09
p = 0.314
p = 0.763
p = 0.549
p = 0.576
p = 0.679
Food sticks in mouth
r = -0.232
r = 0.184
r = 0.206
r = -0.429
r = -0.096
p = 0.311
p = 0.424
p = 0.371
p = 0.052
p = 0.679
Need water
r = 0.104
r = -0.093
r = -0.320
r = -0.457
r = -0.274
p = 0.653
p = 0.687
p = 0.158
p = 0.037*
p = -0.230
r = 0.228 p = 0.320
r = 0.357 p = 0.112
r = -0.239 p = 0.297
r = -0.122 p = 0.599
r = -0.273 p = 0.232
Change in taste
*The asterisk denotes statistical significance
Discussion This study provides new insight into patient awareness of specific dysphagia symptoms following chemoradiation for head and neck cancer. Results suggest a disconnect between patient awareness of swallowing difficulty and findings of the Modified Barium Swallow Test. Summated scores on the perception questionnaire increased significantly for patients from pre- to post-treatment. These scores represent a type of patient symptom profile that appears to have commonality across patients. Higher ratings for the ‘‘difficulty swallowing’’ item on the perception assessment for the patient group represent a level of overall awareness of difficulty swallowing. Ratings of ‘‘difficulty swallowing’’ at both assessment points were significantly higher than for the control group. These ratings did increase from pre- to post-treatment but the changes were not significant. This awareness of a general decrease in swallowing function already at the pre-treatment point is likely due to the presence of the tumor and may account for the lack of significant changes in ratings from pre- to post-treatment. Of the 12 items on the perception assessment questionnaire, patients rated only four significantly higher following treatment. Yet, consistent with previous studies, multiple aspects of swallow physiology changed after treatment. Increases in residue and the frequency of penetration and aspiration as well as longer pharyngeal response times and decreased OPSE scores all likely reflect fibrotic changes resulting in reduced strength of the head and neck musculature. The observed decreases in swallow efficiency are consistent with previous findings of swallowing dysfunction following chemoradiation [23, 24, 31–40]. Interestingly, there were two instances where swallow efficiency increased after treatment and both of these patients had tonsillar tumors. This suggests that for those with tonsillar tumors, eradication of the tumor could lead to overall improvement in swallowing. For this reason, additional
analyses were conducted after exclusion of the five patients in the study with tonsillar tumor sites. Without these patients, pharyngeal response times were still longer after treatment but additional measures of oral and pharyngeal transit times also were significantly longer. This supports the idea that patients with tonsillar tumors may not experience as many changes in swallow function as patients with other tumor sites. This requires further examination of larger numbers of subjects with varying tumor sites. Another important variable to consider when interpreting the results of this study was surgical history. Patients treated surgically experienced more changes in perception ratings as well as measures of swallow physiology than those who received chemoradiation only. The OPSE values were found to decrease significantly in the surgical group but not in the nonsurgical group. Overall changes in both perception and physiology following treatment observed in our combined patient group were likely driven by those patients who had surgery combined with chemoradiation. In a clinical setting, more severe changes in swallow function may be expected when surgery is combined with chemoradiation treatment. When considering how the patients’ report of symptoms relates to physiology, the summated scores from the questionnaire were not found to correlate significantly or strongly with any measure of swallow physiology. However, certain items on the perception questionnaire were found to have more value than others in relation to physical findings. For the patients following treatment, the only strong and significant correlation between perception scores and measures of swallow physiology after treatment was between ratings for the item ‘‘I have difficulty swallowing’’ and overall OPSE values. This supports the findings of Pauloski et al. [23] that patients who responded ‘‘yes’’ to this statement had lower swallow efficiency values. The item ‘‘need water to help food go down’’ also significantly correlated with overall amounts of oral residue. The need to drink water more frequently while eating may reflect weakness in the
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oral tongue or poor lubrication of the oral cavity resulting in higher amounts of oral residue. The lack of other strong correlations between perception and physiologic measures may indicate patient difficulty in identifying the specific problematic aspects of their swallow. This supports the disconnect between patient awareness and more discrete physiology reported in other studies [12, 15, 22, 24]. Specifically, this group of patients was found to have more occurrences of both penetration and aspiration following treatment completion. All occurrences of penetration and 83 % of aspiration occurrences were ‘‘silent.’’ In addition, ratings for the items ‘‘cough when eating and/or drinking’’ and ‘‘choke on food/liquid’’ were not found to increase after treatment. These findings reflect decreased patient awareness of airway invasion and support concern over ‘‘silent’’ aspiration in this patient population. In addition, higher amounts of pharyngeal residue were found post-treatment but patients did not rate the item ‘‘food sticks in my throat’’ higher. Previous studies have reported decreased intraoral, perioral, pharyngeal, and laryngeal sensation following chemoradiation treatment, which may lead to poor patient awareness of airway invasion and pharyngeal residue [35, 36, 41, 42]. In addition, perceptual changes following chemoradiation yielded higher ratings for items that could be related to salivation (‘‘dry mouth,’’ ‘‘food sticks in my mouth,’’ ‘‘need water to help food go down,’’ and ‘‘change in sense of taste’’). The significant correlation between the item ‘‘need water to help food go down’’ and oral residue suggests that patients have the perception of a need for more water while eating due to higher levels of material remaining in their oral cavity after the swallow. However, the fact that this correlation was only moderate indicates that another factor, possibly saliva production or thickness, may influence this particular perception. This hypothesis is also supported by the item ‘‘I have a dry mouth’’ yielding the highest ratings post-treatment. It is known that salivary flow and quality is affected by radiation treatment since the salivary glands are usually included in the radiation field. In addition, changes in taste sensation have been documented in this patient population and may relate to salivary alterations [43]. The degree to which a decrease in salivary flow along with changes in the thickness and composition of saliva affects swallowing remains to be elucidated. It also is important to note the items that did not yield higher ratings post-treatment, including ‘‘food/liquid come back up after I swallow,’’ ‘‘heartburn,’’ and ‘‘wake at night coughing/gagging.’’ As such, it may not be particularly useful to include these symptoms in a post-treatment dysphagia symptom questionnaire. However, further study with a larger group of patients is necessary before drawing such a conclusion. There were several limitations to our study. The number of patients with head and neck cancer was small and differed
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some in terms of tumor site, prior surgery, exact chemoradiation treatment protocol, and smoking or alcohol history. The time from completion of treatment to post-treatment assessment varied for our patients as well. Due to difficulty with follow-up closer to treatment completion secondary to acute effects, several patients were assessed at a later point than the rest of the group. Also, cognitive status and the presence of depression may have influenced patient responses on the perception assessment. Although all patients were determined to be cognitively able to participate in the study, a measure of cognitive level as well as the presence and severity of depression should be included and considered in relation to patient awareness of swallowing difficulty in future studies. Finally, in this study, we looked at overall values averaged across bolus type for all measures of physiology, so the effects specific to bolus type were not examined. To increase statistical power and validity of findings, multicenter trials to examine effects of chemoradiation on various aspects of perception and swallow physiology are needed. 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 work was performed at Northwestern University, Department of Communication Sciences and Disorders in Evanston, IL as well as Northwestern Memorial Hospital in Chicago, IL. The manuscript was partially prepared at the William S. Middleton Veteran Affairs Hospital in Madison, WI; GRECC manuscript #2013-04. 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 the U.S. government. Conflict of interest declare.
The authors have no conflicts of interest to
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Nicole M. Rogus-Pulia
PhD, CCC-SLP
Margaret C. Pierce RN, BSN, OCN Bharat B. Mittal
MD
Steven G. Zecker
PhD
Jeri A. Logemann PhD, CCC-SLP
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ORIGINAL ARTICLE
Changes in Swallowing Physiology and Patient Perception of Swallowing Function Following Chemoradiation for Head and Neck Cancer Nicole M. Rogus-Pulia • Margaret C. Pierce Bharat B. Mittal • Steven G. Zecker • Jeri A. Logemann
•
Received: 8 May 2013 / Accepted: 22 November 2013 Ó Springer Science+Business Media New York (outside the USA) 2014
Abstract Patients treated with chemoradiation for head and neck cancer often report difficulty with swallowing and are frequently diagnosed with dysphagia. The extent to which patient awareness of dysphagia corresponds to observed physiologic changes in swallowing is unclear. The purpose of this study was to determine how both patient awareness of swallowing function and swallowing physiology individually change following chemoradiation and then to clarify the relationship between them. Twentyone patients with head and neck cancer treated with chemoradiation were assessed before and after treatment and matched with twenty-one control subjects. The modified barium swallow test was utilized to examine swallowing physiology. Each subject was also given a series of items regarding awareness of specific dysphagia symptoms. N. M. Rogus-Pulia (&) William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison GRECC (11G), Room D5216, Madison, WI 53705, USA e-mail: [email protected] N. M. Rogus-Pulia Department of Medicine, School of Medicine and Public Health, Speech, Swallowing, and Dining Enhancement Program, University of Wisconsin-Madison, Madison, WI, USA M. C. Pierce Radiation Oncology, Northwestern Memorial Hospital, Chicago, IL, USA B. B. Mittal Department of Radiation Oncology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA S. G. Zecker J. A. Logemann Department of Communication Sciences and Disorders, Northwestern University, Frances Searle Building, Evanston, IL 60208, USA
Results showed decreased swallow efficiencies, higher percentages of residue, and more occurrences of penetration and aspiration following chemoradiation. Patients also had significantly higher ratings for 4 of the 12 items (‘‘dry mouth,’’ ‘‘food sticking in my mouth,’’ ‘‘need water to help food go down,’’ and ‘‘change in sense of taste’’). Only one strong and significant correlation was found between ratings for ‘‘I have difficulty swallowing’’ and swallow efficiency values. Based on these findings, it appears that patients sense a general difficulty with swallowing but have less awareness of specific symptoms of dysphagia. Keywords Deglutition Deglutition disorders Dysphagia Chemoradiation Head and neck cancer Perception Swallow efficiency
Introduction Patients with head and neck cancer often report symptoms of dysphagia following chemoradiation treatment [1–4]. Patient perception of illness is a well-established determinant of adherence to medical treatment recommendations [5]. However, difficulties with patient nonadherence to dietary and liquid modifications for dysphagia have been linked to poor patient awareness of their condition [6–8]. Nonadherence with therapeutic recommendations is associated with a significantly increased mortality risk related to the development of aspiration pneumonia [9]. A clearer understanding of the relationships among specific aspects of patient perception and physiologic dysfunction is critical to future development of educational interventions that may improve patient adherence. The degree to which patient perception of swallow function agrees with objective measures of swallow
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physiology has not been well-defined. Results of studies that examined patient perception of swallowing difficulty include information about the level of agreement between physiology and a global awareness of swallowing [1–4] but no data on which specific aspects of swallowing patients perceive to be problematic. The impact of chemoradiation treatment on the quality of life of patients with head and neck cancer has been examined extensively [10]. Current quality-of-life rating scales focus on the functional impact of dysphagia on the patient’s life as a whole [11]. Although there are subscales included within these comprehensive quality-of-life scales with questions related to specific dysphagia symptoms, these items comprise a relatively small part of the overall measure. Results from studies in other patient populations that examined the relationship between patient perception and objective measures of swallowing have yielded conflicting results. Several authors reported a discord between patient perception and actual swallow function [12–15]. Others have found a more consistent match between subjective complaints and objective measures of swallowing [16–22]. The few studies that examined patients with head and neck cancer have mixed findings. Walther and Deroover [4] and Rhodus et al. [16] found a link between perception and motility disturbances. A study by Pauloski et al. [23] concluded that patients with complaints of difficulty swallowing had lower swallow efficiency scores, longer oral and pharyngeal transit times, greater oral and pharyngeal residue, and more swallows with aspiration than those without complaints. In contrast, Hughes et al. [24] reported no significant relationship between patient complaint of dysphagia and videofluoroscopic findings. A limitation of this previous work has been the use of perception questionnaires with yes/no responses [20, 23– 26]. In order to find direct correlations with objective measures taken from videofluoroscopic recordings of swallowing, it is necessary to quantify the degree to which patients perceive each problem. Therefore, we have utilized Likertscale responses to a series of questions taken partly from a previously used questionnaire by Pauloski et al. [23] and Logemann et al. [25, 26] as well as another commonly used questionnaire developed by Wallace et al. [27]. This study was designed to provide new insights into the complex relationship between patient awareness of dysphagia and swallowing physiology in post-chemoradiation patients with head and neck cancer. The objectives of this study were (1) to more clearly define changes in patient perception of swallowing function following chemoradiation treatment by administering a series of questions about specific dysphagia symptoms requiring Likert-scale responses and (2) to clarify relationships among patient perception of swallowing function and swallowing physiology. Our hypothesis, based on previous work that examined changes in patient perception of
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swallowing following chemoradiation treatment [23], was that patients would perceive more difficulty with swallowing overall and that these perception ratings would correlate highly with measures of physiology.
Methodology Subjects There were two groups of subjects: (1) 21 patients diagnosed with head and neck cancer and treated with chemoradiation treatment and (2) 21 age- and gender-matched control subjects. Patients were recruited through referrals from the Radiation Oncology and Medical Oncology centers and the Speech and Swallowing Clinic at Northwestern Memorial Hospital. Cooperating radiation oncologists, medical oncologists, and head and neck surgeons helped to identify patients suitable for the study. The patient group consisted of individuals who were from 36 to 80 years of age (average age = 56 years). These patients were diagnosed with oral, oropharyngeal, nasopharyngeal, or laryngeal tumors and treated with a full course of radiotherapy and chemotherapy. All patients received at least 66 Gy over an average of 7 weeks with concurrent and/or induction chemotherapy. The radiation delivery was intensity-modulated for all the patients except one who received conventional external-beam radiation (see Table 1 for patient characteristics). Inclusion criteria for the patient group were (1) diagnosis of head and neck cancer by a medical doctor, (2) age 30–80 years, and (3) planned total radiation dosage of at least 50 Gy with concurrent chemotherapy. Exclusion criteria were (1) other medical problems known to cause dysphagia (e.g., neurological problems, gastroenterological problems), (2) prior swallowing treatment, and (3) prescribed medication that could affect swallowing. The control group consisted of 21 normal subjects ranging in age from 31 to 77 years (average age = 56 years). These subjects were eligible for participation if they (1) matched with a patient with respect to gender and age (±5 years), (2) did not complain of or have a history of dry mouth, (3) did not have a history of dysphagia, or (4) were not taking any medication that could affect swallowing. Study Procedures The protocol was approved by the Institutional Review Board and all subjects signed informed consent statements. Each patient with head and neck cancer was evaluated twice, once prior to initiation of chemoradiation treatment and once after completion of treatment. The pre-treatment assessment took place an average of 3.5 weeks before treatment began. The post-treatment assessment for the majority of patients
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 1 Patient characteristics Subject Age Sex Tumor site
Tumor stage
Total RT Induction Concurrent Surgery dose (Gy) chemo chemo (Y/N) (Y/N)
Smoking/ alcohol abuse
1
36
M
Nasopharynx
T2bN3bM0
70
Y
Y
None
No/No
2
48
F
Nasopharynx
T1N3M0
70
Y
Y
None
No/No
3
80
M
Hypopharynx, epiglottis T4N1M0, T1N1M0
70
N
Y
None
Yes/No
4
53
M
Left base of tongue
T2N2bM0
70
N
Y
None
No/No
5
66
M
Left tonsil
T2N2bM0
66
N
Y
Tonsillectomy
Yes/Yes
6
59
M
Nasopharynx
T4N2M0
70
Y
Y
None
No/No
7
55
M
Right tonsil
T1N2bM0
70
N
Y
Tonsillectomy
Yes/No
8
47
M
Right oral tongue
T1N0M0
70
N
Y
Partial glossectomy
No/No
9
48
M
Left base of tongue
T0N2bM0
70
Y
Y
Neck dissection
No/No
10
54
M
Base of tongue
T4aN2cM0
70
N
Y
None
No/Yes
11
59
M
Left base of tongue
T1N2bM0
70
N
Y
None
Yes/Yes
12
45
M
Right tonsil
T2N2bM0
66
Y
Y
Neck dissection and tonsillectomy No/No
13
76
M
Right vocal fold
T4N0M0
70
N
Y
None
14
56
M
Unknown primary
T0N1M0
70
N
Y
Tonsillectomy
Yes/No
15
61
F
Right tonsil
T2N2bMX
70
N
Y
Tumor debulking
Yes/Yes
16
50
M
Right tonsil
T2N2b/cM0 70
Y
Y
None
Yes/Yes
17 18
67 65
M F
Base of tongue Right base of tongue
T1N2cM0 T2N2bM0
70 70
N N
Y Y
None None
No/Yes Yes/Yes
19
63
M
Left base of tongue
T2N2bM0
72
N
Y
None
No/Yes
20
55
F
Right base of tongue
T1N2cM0
70
N
Y
Right neck dissection
Yes/No
21
42
M
Left palatine tonsil
T2N2bM0
70
N
Y
None
No/No
Yes/No
RT radiation treatment, Chemo chemotherapy, Y yes, N no, M male, F female, T tumor, N node, M metastasis
was between 3 months and 1 year after treatment (an average of 5 months). Three patients were assessed up to 2 years post-treatment due to difficulty with follow-up. The control subjects were evaluated only once and underwent the same procedures as the patient group. Data collection procedures at each assessment point included responses to a series of questions about specific dysphagia symptoms and the modified barium swallow test. Patient Perception of Swallow Function There were 12 questions regarding swallowing function that were administered to each subject (see Table 2 for a list of questions). These items were taken from a questionnaire used in previous studies by Logemann et al. [28]. However, in this study, the required responses were on a 7-point Likert scale versus yes/no responses used previously. Most of these questions also were similar to those included in a tool developed by Wallace et al. [27], except this questionnaire included a question about the severity of dry mouth, a common symptom for patients following chemoradiation treatment that likely affects swallowing. Also, the tool developed by Wallace et al.
[27] utilized a visual analog scale. A Likert-scale design was preferred in this study due to its ease of administration and interpretation [29]. Each item required a rating of 1–7 (1 indicating no difficulty with the perceived problem and 7 indicating the most severe difficulty). This perception assessment had a minimum summated score of 12 and a maximum of 84. Inter-item correlations were determined to examine potential overlap between the 12 items on the questionnaire (Table 3). Correlations were calculated for the patient group at both the pre-treatment and the posttreatment assessment points and for the control group. As is seen in Table 3, the items that were both strongly and significantly correlated differed based on group as well as assessment point, suggesting that the perception measured by each item may vary depending on disease and treatment status. Therefore, all items were retained for use in this study. The Modified Barium Swallow Test (MBST) Each subject’s swallowing was examined using a modified barium swallow test. The MBST enables visualization and
123
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 2 Items administered for perception of swallowing assessment 1
I have difficulty swallowing
2
I have a dry mouth
3
Food sticks in my mouth
4
Food sticks in my throat
5
I find that food won’t go down
6
I need to drink water to help food go down
7
I choke on food/liquid
8
I have found that I cough when eating and/or drinking
9
I experience food/liquid coming back up after I swallow
10
I experience heartburn
11
I wake up at night coughing and/or gagging
12
I have experienced a change in my sense of taste
measurement of the critical movements of the oropharyngeal swallow. Each subject was administered two 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 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 placed into the patient’s mouth via syringe or spoon. The patient was instructed to hold the bolus in his/her mouth until directed to swallow. 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 swallowing physiology on particular bolus types could be attributed more accurately to effects of chemoradiation. If a patient aspirated [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 Three types of measures and observations were made from videofluoroscopy: (1) approximate amount (percentage) of residue, (2) frequency of penetration and aspiration, and (3) selected temporal measurements of structural and bolus movement. Data from the videofluoroscopic studies were recorded on 0.5-inch. videotape. The measures and observations were made through visual inspection of the recordings at regular speed, slow motion, and frame-byframe using a DVC-PRO machine. Intrarater and interrater reliabilities were calculated for 10 % of all swallows and were found to be high (95–99 % agreement) for all measures and observations.
123
Approximate Percent Residue 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 that examined the correlations between oral residue measured with scintigraphy and estimations of the amount of oral residue from the modified barium swallow indicate that observations of approximate percent residue from videofluoroscopy can be accurate when done by well-trained staff [28]. The presence or absence and the amount of residue if present in the oral and pharyngeal cavities were determined. Values for each measure were averaged across trials in order to obtain a value per bolus type for each subject. Then, overall measures were obtained by averaging measures across bolus types for each subject. Frequency of Penetration and Aspiration For each swallow, the presence or absence of penetration and aspiration was recorded. The time point (before, during, or after the swallow) was also noted. The total number of penetration or aspiration occurrences at each time point was calculated by summing frequencies across all swallows within each group. Temporal Measures of Bolus Movement Using frame-by-frame analysis and slow motion, specific video frames 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 tongue base, which is 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), and (d) end of cricopharyngeal opening (the tail of the 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, b-a), the time it takes the bolus to move through the oral cavity; pharyngeal delay time (PDT, c-b), the time from when the bolus head passes the posterior edge of the ramus of the mandible until the initial observation of laryngeal elevation; pharyngeal response time (PRT, d-c), the time from the onset of laryngeal elevation until the bolus tail passes through the cricopharyngeal sphincter; and pharyngeal transit time (PTT, d-b), the time
0.32
Controls
-0.18
0.34
Controls
0.445*
Pre-tx patients
0.41
Controls
Post-tx patients
0.808* 0.438*
Pre-tx patients
Post-tx patients
0.07 0.11
Post-tx patients Controls
0.08
Controls 0.124
0.3
Post-tx patients
Pre-tx patients
0.405*
0.36
Controls
Pre-tx patients
0.3
Post-tx patients
0.41 0.783
Controls
Pre-tx patients
0.36
Post-tx patients
0.460*
Controls 0.193
0.448*
Post-tx patients
Pre-tx patients
0.280
-0.22
Pre-tx patients
Controls
0.111 0.44*
0.434*
Post-tx patients
Pre-tx patients Post-tx patients
0.330
Pre-tx patients
Controls
*The asterisk denotes statistical significance
Change in taste
Wake at night cough/gag
Heartburn
Food comes back up
Cough
Choke
Need water
Food won’t go down
Food sticks in throat
0.36 0.15
Post-tx patients
0.493* -0.057
Controls
Pre-tx patients
0.485*
Post-tx patients
Food sticks in mouth
0.291
Pre-tx patients
Dry mouth
Difficulty swallowing
Group and/or assessment point
Items on perception assessment
-0.29
0.23
0.377
0.666*
0.739*
0.251
0 0.11
0.169
-0.18
0.33
0.571*
0.736*
0.528*
0.045
0.736*
0.3
-0.134
0.29
0.41
0.700*
0.19
0.563* 0.556*
0.703*
0.31
0.506*
0.24
0.39
0.12
–
Dry mouth
Table 3 Interitem correlational matrix for patient and control groups
-0.149
0.26
0.39
0.284
0.515*
-0.119
0.02 0.062
0.313
0.274
0.559*
0.134
0.031
0.25
-0.045
-0.051
0.36
0.134
-0.030
0.12
0.364
0.031
0.397 0.556*
0.098
0.717*
0.316
–
–
Food sticks in mouth
0.01
0.29
0.389
0.893*
0.28
0.111
0.14 0.27
-0.168
-0.14
0.503*
0.228
0.777*
0.09
0.173
0.819*
0.41
-0.091
0.11
0.16
0.795
0.2
0.909 0.38
–
–
–
Food sticks in throat
0.559*
0.25
0.486*
0.18
0.512*
-0.006
-0.07 0.491*
-0.086
0.3
0.784*
0.273
0.28
0.698*
-0.054
0.26
0.800*
-0.064
0.2
-0.14
0.885*
–
–
–
–
Food won’t go down
-0.143
0.367
0.549*
0.095
0.368
0.136
0.178 -0.047
0.01
0.092
-0.315
0.689*
0.431
-0.007
0.024
0.106
-0.204
-0.073
–
–
–
–
–
Need water
-0.03
0.127
-0.118
0.759*
0.275
0.103
0.073 0.43
0.751*
-0.13
0.867*
-0.050
0.821*
0.534*
0.368
–
–
–
–
–
–
Choke
-0.17
0.075
0.095
0.732*
0.397
0.669*
-0.183 0.13
0.280
-0.23
0.520
0.134
–
–
–
–
–
–
–
Cough
0.057
-0.121
0.379
-0.262
0.261
0.290
0.121 0.542*
0.156
–
–
–
–
–
–
–
–
Food comes back up
0.297
-0.161
0.028
0.183
-0.195
-0.013
–
–
–
–
–
–
–
–
–
Heartburn
0.143
0.323
0.624*
–
–
–
–
–
–
–
–
–
–
Wake at night cough/gag
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
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N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
required for the bolus to move through the pharynx. For each measure, values were averaged across trials to obtain a value for each bolus type per subject. Then, overall measures were obtained by averaging each measure across all bolus types for each subject. Oropharyngeal Swallow Efficiency The oropharyngeal swallow efficiency (OPSE) for each swallow was also calculated. The OPSE attempts to quantify the interaction of bolus speed and clearance of material from the oropharynx [30]. OPSE is calculated using the following equation:
the perception assessment and measures of swallow physiology (oral residue, pharyngeal residue, and OPSE). If a subject had missing data, which occurred when subjects aspirated more than 5 % of the initial bolus and in rare cases of difficulties with equipment or image clarity, then missing data specific to each analysis were excluded from that analysis. Correlations between the demographic variables of continuous nature (age, radiation total dose, time to pre-treatment assessment, time to post-treatment assessment) and the dependent variables in this study were also calculated. Since there were no strong or significant correlations present, these variables were not included as covariates in the analyses.
100 ðoral residue þ pharyngeal residue þ aspiration before swallow þ aspiration during swallowÞ : oral transit time + pharyngeal delay time + pharyngeal response time
OPSE scores typically range from 100 (100 % of the bolus is swallowed in 1 s) to 140 in normal subjects as the bolus becomes thicker. With disordered swallowing, the OPSE drops lower as the percentage of bolus swallowed decreases and the time increases. Scores for the two swallows for each bolus type were averaged in order to obtain one value of each measure per bolus type for each subject. A measure of overall OPSE was determined by averaging this measure across all bolus types for each subject. Statistical Analysis Repeated-measures analyses of variance (ANOVA) were conducted to examine changes in summated scores as well as ratings for each individual item on the perception assessment and all measures of swallow physiology (OTT, PDT, PRT, PTT, oral residue, pharyngeal residue, and OPSE) from pretreatment to post-treatment. One-way between-groups ANOVA were conducted to compare the control group to the patient group at each time point separately on each of these same dependent variables. McNemar’s test was used to test for differences in the frequencies of penetration during the swallow from pre- to posttreatment. Due to low numbers per cell, McNemar’s exact test was used to determine changes in the frequencies of aspiration during and after the swallow from pre- to post-treatment. v2 or Fisher’s exact test was used to test for differences in the frequencies of penetration and aspiration between the patient group at both assessment points and the control group. Pearson product-moment correlation coefficients were calculated within the patient group post-treatment to examine the relationships between ratings for the items on
123
Results Item Analysis and Summated Scores for Perception Questionnaire Summated scores increased significantly from pre- to posttreatment [Wilks’ lambda = 0.632, F(1,20) = 11.66, p \ 0.005]. Scores were also significantly higher for the patient group post-treatment than for the control group [F(1,40) = 16.8, p \ 0.001]. Significant increases in ratings were found from pre- to post-treatment for the following items: ‘‘dry mouth’’ [Wilks’ lambda = 0.404, F(1,20) = 6.56, p \ 0.001], ‘‘food sticks in my mouth’’ [Wilks’ lambda = 0.753, F(1,20) = 6.56, p \ 0.002], ‘‘need water to help food go down’’ (Wilks’ lambda = 0.575, F(1,20) = 14.75, p \ 0.002], and ‘‘change in sense of taste’’ [Wilks’ lambda = 0.684, F(1,20) = 9.22, p \ 0.01]. These same items, as well as ‘‘difficulty swallowing’’ [F(1,40) = 22.04, p \ 0.0001], were rated significantly higher in the patient group at the posttreatment assessment point compared to the control group. The item with the highest rating overall post-treatment was ‘‘I have a dry mouth’’ (see Fig. 1 for illustration of these results). Only one item, ‘‘difficulty swallowing,’’ was rated significantly higher in the patient group at the pre-treatment assessment point compared to the control group [F(1,40) = 6.88, p \ 0.02]. Measures of Swallowing Physiology Residue There were significantly greater amounts of oral residue posttreatment as compared to pre-treatment [Wilks’ lambda =
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Fig. 1 Ratings for each individual item given as part of the perception assessment before and after chemoradiation treatment
Table 4 Mean and standard deviation for measures of swallowing physiology
Items that correspond to numbers on x-axis: 1. Difficulty swallowing 2. Dry mouth 3. Food stick mouth 4. Food stick throat 5. Food won’t go down 6. Need water 7. Choke 8. Cough 9. Comes back up 10. Heartburn 11. Wake at night 12. Change in taste
Measure Oral transit time
Pharyngeal delay time
Pharyngeal response time
Pharyngeal transit time
Oral residue
Pharyngeal residue
0.421, F(1,20) = 27.45, p \ 0.001]. There were also significant differences in oral residue between the post-treatment patient group and the control group [F(1,40) = 21.62, p \ 0.001]. Pharyngeal residue overall increased significantly from pre-treatment to post-treatment [Wilks’ lambda = 0.629, F(1,20) = 11.79, p \ 0.005]. Again, there were significant differences between the post-treatment patient group and the control group [F(1,40) = 11.65, p \ 0.002]. Means and standard deviations are displayed in Table 4. Frequency of Penetration and Aspiration There were no instances of penetration or aspiration before the swallow in either group. Following treatment, six patients
Group
Mean
Standard deviation
Control
0.478
0.169
Patient (pre-treatment)
0.496
0.210
Patient (post-treatment)
0.666
0.535
Control
0.120
0.314
Patient (pre-treatment)
0.062
0.285
Patient (post-treatment)
0.077
0.196
Control
0.819
0.114
Patient (pre-treatment)
0.754
0.083
Patient (post-treatment)
0.816
0.112
Control
0.933
0.332
Patient (pre-treatment) Patient (post-treatment)
0.817 0.891
0.265 0.191
Control
2.28
1.56
Patient (pre-treatment)
2.81
2.83
Patient (post-treatment)
5.73
3.01
Control
2.56
1.85
Patient (pre-treatment)
2.88
1.90
Patient (post-treatment)
11.77
12.22
were found to have penetration during the swallow compared to two patients before treatment. As a group, the patients at post-treatment had significantly more occurrences of penetration during the swallow (25 occurrences out of 149 swallows, p \ 0.0001) than at pre-treatment (3 occurrences). One patient was found to aspirate during the swallow and two were found to aspirate after the swallow post-treatment compared to none pre-treatment. There was a nonsignificant increase in frequency of aspiration during the swallow from before (no occurrences) to after (3 occurrences) treatment. Aspiration after the swallow occurred significantly more frequently (6 occurrences) after treatment than before (no occurrences, p \ 0.05). The patients at post-treatment also had significantly more occurrences of penetration during the swallow
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treatment, correlations were calculated between the specific measures that influence the swallow efficiency calculation (oral transit time, pharyngeal delay time, pharyngeal response time, oral residue, and pharyngeal residue) and the ratings for the items on the PPSFQ that were found to increase significantly following treatment. The only significant correlation was between the item ‘‘Need water to help food go down’’ and oral residue overall (r = -0.457, p \ 0.05) (see Table 5 for these correlations). Fig. 2 Temporal measures for patients before and after chemoradiation treatment. HN head and neck cancer, Pre before chemoradiation treatment, Post after chemoradiation treatment, OTT oral transit time, PDT pharyngeal delay time, PRT pharyngeal response time, PTT pharyngeal transit time
(p \ 0.001) and aspiration after the swallow (p \ 0.03) than the control group (no occurrences of penetration or aspiration). All occurrences of aspiration during the swallow and 83 % of occurrences of aspiration after the swallow were ‘‘silent’’ (no throat clear or cough in response). Individual Temporal Measures Pharyngeal response time was the only measure found to be significantly longer post-treatment [Wilks’ lambda = 0.677, F(1,20) = 9.54, p \ 0.01] as compared to pre-treatment within the patient group (Fig. 2). Oropharyngeal Swallow Efficiency Within the patient group, overall OPSE values decreased significantly from pre-treatment to post-treatment [Wilks’ lambda = 0.542, F(1,20) = 16.88, p \ 0.002]. There were also lower swallow efficiency values in the post-treatment patient group than in the control group [F(1,39) = 5.36, p \ 0.05]. There were two instances where the OPSE values actually increased from pre-treatment to post-treatment and both patients had tonsillar tumors. Relationships Between Individual Perception Questionnaire Items and OPSE At the post-treatment assessment point in the patient group, there was a significant negative correlation between the ‘‘difficulty swallowing’’ item and OPSE overall (r = 0–0.652, p \ 0.002). Summated scores from the questionnaire were not found to be significantly correlated with any measure of swallow physiology. In order to determine which specific aspects of physiology may underlie the change in perception post-
123
Exclusion of Patients with Tonsillar Tumors Based on observed increases in OPSE values from pre- to post-treatment for two of the five patients in this study with tonsillar tumors, it is possible that patients with tonsillar tumors may respond differently to chemoradiation treatment. Therefore, data also were analyzed after exclusion of those with tonsillar tumors. This smaller sample size (n = 16) required use of the nonparametric Wilcoxon signed-rank test for continuous data and McNemar’s test for binary data. Differences in results after exclusion of those with tonsillar tumors were significant increases in oral transit time (p = 0.008) and pharyngeal transit time (p = 0.014) following treatment. Surgical Versus Nonsurgical Intervention A number of those in the patient group received some type of surgical intervention in addition to chemoradiation treatment. The effects of surgery on changes from before to after treatment were examined by subdividing the overall patient group into those who received surgical intervention (n = 8) and those who did not (n = 13). Changes in all dependent variables were examined for both subgroups separately using nonparametric statistics due to the smaller group sizes. For the surgical subgroup, significant increases in ratings for ‘‘dry mouth’’ (p B 0.01), ‘‘food sticks in my mouth’’ (p \ 0.05), ‘‘need water to help food go down’’ (p \ 0.02), and ‘‘change in sense of taste’’ (p \ 0.05) on the perception assessment were consistent with findings for the overall patient group. However, only ratings for ‘‘dry mouth’’ (p \ 0.05) and ‘‘need water to help food go down’’ (p \ 0.05) increased significantly for the nonsurgical subgroup. For measures of swallow physiology in the surgical subgroup, oral transit time (p \ 0.01), pharyngeal response time (p \ 0.02), pharyngeal transit time (p \ 0.02), amounts of oral residue (p \ 0.002), and pharyngeal residue (p \ 0.002) increased significantly following treatment. OPSE values also decreased significantly (p \ 0.001). In the nonsurgical subgroup, the only significant finding was an increase in oral residue (p \ 0.05).
N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer Table 5 Correlations between perception questions and measures of swallow physiology Individual items
Oral transit time
Pharyngeal delay time
Pharyngeal response time
Oral residue
Pharyngeal residue
Dry mouth
r = 0.231
r = 0.07
r = -0.139
r = -0.129
r = 0.09
p = 0.314
p = 0.763
p = 0.549
p = 0.576
p = 0.679
Food sticks in mouth
r = -0.232
r = 0.184
r = 0.206
r = -0.429
r = -0.096
p = 0.311
p = 0.424
p = 0.371
p = 0.052
p = 0.679
Need water
r = 0.104
r = -0.093
r = -0.320
r = -0.457
r = -0.274
p = 0.653
p = 0.687
p = 0.158
p = 0.037*
p = -0.230
r = 0.228 p = 0.320
r = 0.357 p = 0.112
r = -0.239 p = 0.297
r = -0.122 p = 0.599
r = -0.273 p = 0.232
Change in taste
*The asterisk denotes statistical significance
Discussion This study provides new insight into patient awareness of specific dysphagia symptoms following chemoradiation for head and neck cancer. Results suggest a disconnect between patient awareness of swallowing difficulty and findings of the Modified Barium Swallow Test. Summated scores on the perception questionnaire increased significantly for patients from pre- to post-treatment. These scores represent a type of patient symptom profile that appears to have commonality across patients. Higher ratings for the ‘‘difficulty swallowing’’ item on the perception assessment for the patient group represent a level of overall awareness of difficulty swallowing. Ratings of ‘‘difficulty swallowing’’ at both assessment points were significantly higher than for the control group. These ratings did increase from pre- to post-treatment but the changes were not significant. This awareness of a general decrease in swallowing function already at the pre-treatment point is likely due to the presence of the tumor and may account for the lack of significant changes in ratings from pre- to post-treatment. Of the 12 items on the perception assessment questionnaire, patients rated only four significantly higher following treatment. Yet, consistent with previous studies, multiple aspects of swallow physiology changed after treatment. Increases in residue and the frequency of penetration and aspiration as well as longer pharyngeal response times and decreased OPSE scores all likely reflect fibrotic changes resulting in reduced strength of the head and neck musculature. The observed decreases in swallow efficiency are consistent with previous findings of swallowing dysfunction following chemoradiation [23, 24, 31–40]. Interestingly, there were two instances where swallow efficiency increased after treatment and both of these patients had tonsillar tumors. This suggests that for those with tonsillar tumors, eradication of the tumor could lead to overall improvement in swallowing. For this reason, additional
analyses were conducted after exclusion of the five patients in the study with tonsillar tumor sites. Without these patients, pharyngeal response times were still longer after treatment but additional measures of oral and pharyngeal transit times also were significantly longer. This supports the idea that patients with tonsillar tumors may not experience as many changes in swallow function as patients with other tumor sites. This requires further examination of larger numbers of subjects with varying tumor sites. Another important variable to consider when interpreting the results of this study was surgical history. Patients treated surgically experienced more changes in perception ratings as well as measures of swallow physiology than those who received chemoradiation only. The OPSE values were found to decrease significantly in the surgical group but not in the nonsurgical group. Overall changes in both perception and physiology following treatment observed in our combined patient group were likely driven by those patients who had surgery combined with chemoradiation. In a clinical setting, more severe changes in swallow function may be expected when surgery is combined with chemoradiation treatment. When considering how the patients’ report of symptoms relates to physiology, the summated scores from the questionnaire were not found to correlate significantly or strongly with any measure of swallow physiology. However, certain items on the perception questionnaire were found to have more value than others in relation to physical findings. For the patients following treatment, the only strong and significant correlation between perception scores and measures of swallow physiology after treatment was between ratings for the item ‘‘I have difficulty swallowing’’ and overall OPSE values. This supports the findings of Pauloski et al. [23] that patients who responded ‘‘yes’’ to this statement had lower swallow efficiency values. The item ‘‘need water to help food go down’’ also significantly correlated with overall amounts of oral residue. The need to drink water more frequently while eating may reflect weakness in the
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N. M. Rogus-Pulia et al.: Swallowing Function After Chemoradiation for Head and Neck Cancer
oral tongue or poor lubrication of the oral cavity resulting in higher amounts of oral residue. The lack of other strong correlations between perception and physiologic measures may indicate patient difficulty in identifying the specific problematic aspects of their swallow. This supports the disconnect between patient awareness and more discrete physiology reported in other studies [12, 15, 22, 24]. Specifically, this group of patients was found to have more occurrences of both penetration and aspiration following treatment completion. All occurrences of penetration and 83 % of aspiration occurrences were ‘‘silent.’’ In addition, ratings for the items ‘‘cough when eating and/or drinking’’ and ‘‘choke on food/liquid’’ were not found to increase after treatment. These findings reflect decreased patient awareness of airway invasion and support concern over ‘‘silent’’ aspiration in this patient population. In addition, higher amounts of pharyngeal residue were found post-treatment but patients did not rate the item ‘‘food sticks in my throat’’ higher. Previous studies have reported decreased intraoral, perioral, pharyngeal, and laryngeal sensation following chemoradiation treatment, which may lead to poor patient awareness of airway invasion and pharyngeal residue [35, 36, 41, 42]. In addition, perceptual changes following chemoradiation yielded higher ratings for items that could be related to salivation (‘‘dry mouth,’’ ‘‘food sticks in my mouth,’’ ‘‘need water to help food go down,’’ and ‘‘change in sense of taste’’). The significant correlation between the item ‘‘need water to help food go down’’ and oral residue suggests that patients have the perception of a need for more water while eating due to higher levels of material remaining in their oral cavity after the swallow. However, the fact that this correlation was only moderate indicates that another factor, possibly saliva production or thickness, may influence this particular perception. This hypothesis is also supported by the item ‘‘I have a dry mouth’’ yielding the highest ratings post-treatment. It is known that salivary flow and quality is affected by radiation treatment since the salivary glands are usually included in the radiation field. In addition, changes in taste sensation have been documented in this patient population and may relate to salivary alterations [43]. The degree to which a decrease in salivary flow along with changes in the thickness and composition of saliva affects swallowing remains to be elucidated. It also is important to note the items that did not yield higher ratings post-treatment, including ‘‘food/liquid come back up after I swallow,’’ ‘‘heartburn,’’ and ‘‘wake at night coughing/gagging.’’ As such, it may not be particularly useful to include these symptoms in a post-treatment dysphagia symptom questionnaire. However, further study with a larger group of patients is necessary before drawing such a conclusion. There were several limitations to our study. The number of patients with head and neck cancer was small and differed
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some in terms of tumor site, prior surgery, exact chemoradiation treatment protocol, and smoking or alcohol history. The time from completion of treatment to post-treatment assessment varied for our patients as well. Due to difficulty with follow-up closer to treatment completion secondary to acute effects, several patients were assessed at a later point than the rest of the group. Also, cognitive status and the presence of depression may have influenced patient responses on the perception assessment. Although all patients were determined to be cognitively able to participate in the study, a measure of cognitive level as well as the presence and severity of depression should be included and considered in relation to patient awareness of swallowing difficulty in future studies. Finally, in this study, we looked at overall values averaged across bolus type for all measures of physiology, so the effects specific to bolus type were not examined. To increase statistical power and validity of findings, multicenter trials to examine effects of chemoradiation on various aspects of perception and swallow physiology are needed. 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 work was performed at Northwestern University, Department of Communication Sciences and Disorders in Evanston, IL as well as Northwestern Memorial Hospital in Chicago, IL. The manuscript was partially prepared at the William S. Middleton Veteran Affairs Hospital in Madison, WI; GRECC manuscript #2013-04. 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 the U.S. government. Conflict of interest declare.
The authors have no conflicts of interest to
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Nicole M. Rogus-Pulia
PhD, CCC-SLP
Margaret C. Pierce RN, BSN, OCN Bharat B. Mittal
MD
Steven G. Zecker
PhD
Jeri A. Logemann PhD, CCC-SLP
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