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Speech and swallowing in irradiated and nonirradiated postsurgical oral cancer patients
Speech and swallowing in irradiated and nonirradiated postsurgical oral cancer patients BARBARA ROA PAULOSKI, PhD, ALFRED W. RADEMAKER, PhD, JERILYN A. LOGEMANN, PhD, and LAURA A. COLANGELO, MS,
Evanston, Illinois The effect of radiation on speech and swallowing function was assessed for 18 patients surgically treated for oral and oropharyngeal cancer. Nine patients received surgical intervention and postoperative radiation therapy, and nine received surgery only. Patients were matched regarding percentage of oral tongue resected, percentage of tongue base resected, locus of resection, and method of reconstruction. Speech and swallowing function was assessed before and at 1, 3, 6, and 12 months after surgery following a standardized protocol. Speech tasks included an audio recording of a brief conversation and of a standard articulation test; swallowing function was examined with videofluoroscopy. Statistical testing indicated that overall speech function did not differ between the irradiated and nonirradiated patients. Irradiated patients had significantly reduced oral and pharyngeal swallowing performance, specifically, longer oral transit times on paste boluses, lower oropharyngeal swallow efficiency, increased pharyngeal residue, and reduced cricopharyngeal opening duration. Impaired function may be the result of radiation effects such as edema, fibrosis, and reduced salivary flow. Increased use of tongue range-ofmotion exercises during and after radiation treatment may reduce the formation of fibrotic tissue in the oral cavity and may improve pharyngeal clearance by maintaining adequate tongue base-to–pharyngeal wall contact. (Otolaryngol Head Neck Surg 1998;118:616-24.)
T
he presence of speech and swallowing problems in surgically treated head and neck cancer patients has been well documented in the literature.1-11 Speech and swallowing function in postsurgical head and neck cancer patients may be affected by the degree of resection and the nature of reconstruction. Articulation and the oral stage of the swallow are generally more severely impaired, although the pharyngeal stage of the swallow may be affected if resection includes the tongue base.7,8 Radiation therapy is often used in conjunction with surgical resection of oral and oropharyngeal tumors to control the spread of disease. In addition to the desired antitumor effects, however, radiation therapy to the head and neck induces damage in normal tissues that may From the Departments of Communication Sciences and Disorders (Drs. Pauloski and Logemann), Preventive Medicine (Dr. Rademaker and Ms. Colangelo), and Otolaryngology–Head and Neck Surgery (Dr. Logemann), Northwestern University. Funded by NIH/NCI grant no. P01CA40007. Presented in part at the Fourth Research Workshop on the Biology, Prevention, and Treatment of Head and Neck Cancer, Arlington, Va., Sept. 8-11, 1994, and the annual convention of the American Speech-Language-Hearing Association, New Orleans, La., Nov. 17-21, 1994. Reprint requests: Barbara Roa Pauloski, PhD, Northwestern University, 2299 N. Campus Dr., Evanston, IL 60208. Copyright © 1998 by the American Academy of Otolaryngology– Head and Neck Surgery Foundation, Inc. 0194-5998/98/$5.00 + 0 23/1/85014 616
result in side effects such as mucositis, hyposalivation, radiation caries, trismus, soft tissue necrosis, and osteoradionecrosis of the mandible.12,13 Radiotherapy with or without chemotherapy as a primary treatment modality may result in immediate and long-term changes in swallowing function. Irradiated patients demonstrate pharyngeal swallow disorders, including reduced tongue base contact to the posterior pharyngeal wall, reduced laryngeal elevation, and reduced vestibule and true vocal cord closure during the swallow.14,15 The effect of postoperative radiotherapy on oral functions in surgically treated patients with head and neck cancer has not been well documented in the literature. This study was designed to examine the impact of postoperative radiation therapy on speech and swallowing function in two groups of irradiated and nonirradiated patients with oral and oropharyngeal resections carefully matched on key surgical variables.16 METHODS Subjects
Eighteen patients participated in this study. Nine patients (5 men and 4 women; average age, 62 years) received surgical intervention and postoperative radiation therapy for treatment of their tumors, whereas nine (8 men and 1 woman; average age, 58 years) received surgery only. These patients were selected from a prospectively collected database of surgically treated
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Table 1. Summary of resection and reconstruction types received by patients in this study Resection reconstruction group
1 2 3 4 5 6 7 8
Description of surgical procedure
Anterior tongue only with primary closure Anterior tongue, FOM, segmental mandibular resection with primary closure Anterior tongue, FOM, mandible preserved with distal flap closure Soft palate resection only with primary closure ≤1 cm tongue base, tonsil, mandible preserved with primary closure >1 cm tongue base, tonsil, mandible preserved with primary closure >1 cm tongue base, tonsil, mandible preserved with skin graft closure >1 cm tongue base, tonsil, segmental mandibular resection with primary closure
No. of patient pairs/group
1 1 1 1 1 1 1 2
FOM, Floor of mouth.
patients with oral and oropharyngeal cancer. Subjects were matched regarding surgical resection site, percentage of oral tongue resected (±10%), percentage of tongue base resected (±20%), and method of reconstruction. The amounts of oral tongue and tongue base resected have been demonstrated to be the primary correlates of speech and swallowing impairment in postsurgical patients with oral and oropharyngeal cancer,16-18 so it was important to match on these variables. Patients were not matched regarding total volume of resected tissue because previous research has indicated that resection volume does not correlate with postoperative oral function.16 The nine pairs of patients fell into eight resection/ reconstruction categories. Table 1 summarizes these groups. For each pair of patients, Table 2 summarizes the resection/reconstruction group, tumor stage, radiation dosage and fields when applicable, and status of neck dissection. Although the patients in each pair had primary tumors of similar size, the patients who received postoperative radiotherapy tended to have more advanced disease, as evidenced by greater nodal involvement. Six patient pairs had the same degree of neck dissection; in two pairs, the irradiated patient had a greater amount of neck dissected, and in one pair the nonirradiated patient had a larger neck dissection. Irradiated patients in general began their postoperative radiotherapy within the first month after surgery, although several began in their second month. All subjects began radiotherapy before the 3-month posthealing evaluation. Data Collection, Reduction, and Analysis
The study protocol for this project was approved by the Institutional Review Board at Northwestern University for use in human subjects; informed consent was obtained from all patients. Speech and swallowing performance were assessed before surgery and 1, 3, 6,
and 12 months after healing. Healing was defined as the time when the patient’s surgeon indicated that the suture lines could withstand oral functions, generally 10 to 12 days after surgery. No patient in whom a fistula or other complication in healing developed was included in the study. Therefore the date of healing was chosen as a comparable point across patients. Speech tasks consisted of an audio recording of a 6to 7-minute conversation and the sentence version of the Fisher-Logemann Test of Articulation Competence.19 Swallowing function was examined with the modified barium swallow procedure20 by use of videofluoroscopy. Each patient attempted to complete two swallows each of 1 ml of barium liquid and 1 ml of barium paste. All boluses were administered from a teaspoon. These bolus types are part of the standard clinical protocol for assessing patient behavior with various food consistencies. The bolus sizes were chosen for ease of administration and to reduce the likelihood of aspiration of large amounts. Not all patients were able to swallow two trials of each food consistency at each evaluation point. A patient may have refused to attempt one or both trials of a consistency because of known or suspected difficulty with it; the speech-language pathologist also may have judged it a clinical risk to introduce or continue with a specific consistency during the videofluorographic evaluation. Fluoroscopic data were recorded on 3/4-inch videotape at 30 frames per second. During the study, the fluoroscopy tube was focused on the lips anteriorly, the cervical vertebrae posteriorly, the soft palate superiorly, and the bifurcation of the esophagus and airway inferiorly. Data reduction was completed according to the methods described by Pauloski et al.,7 resulting in the following speech and swallowing measures: percentage of perceived correct production of consonant phonemes, percentage of conversational understandability, oral transit time, pharyngeal transit time, pha-
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Table 2. Summary of patient characteristics by matched pairs
Pair
Resection/ reconstruction group
1
1
2
2
3
3
4
4
5
5
6
6
7
7
8
8
9
8
Sex
M M M F F M M F M M M M M M M F M F
Age (yr)
72 59 54 64 54 69 76 61 54 45 60 75 27 69 50 66 71 50
Volume resected (ml)
7.2 3.0 35 63 140 36.75 72 13.05 1.08 10.0 210.00 34.83 84.0 50.0 42 119 8.8 27
% Oral tongue resected
10 15 0 10 10 0 0 0 0 5 5 0 17.5 10 2 8 5 10
% Tongue base resected
Tumor stage
0 0 0 0 0 0 0 0 15 0 5 20 20 10 5 25 0 10
T2N1M0 T2N3bM0 T2N2bM0 T2N0M0 T2N1M0 T2N2bM0 T3N0M0 T3N0M0 T2N0M0 T2N0M0 T3N1M0 T2N0M0 T3N1M0 T3N2bM0 T2N1M0 T3N2aM0 T3N0M0 T3N1M0
Resection/reconstruction groups are summarized in Table 1. NA, Not applicable.
Table 3. Means and standard deviations (in parentheses) for patient demographics by radiation treatment group and paired Student’s t test p values No postoperative radiation
% Oral tongue resected % Tongue base resected Resection volume (ml) Age (yr)
5.5 5.0 66.7 56.4
(6.0) (7.5) (69.9) (14.0)
ryngeal delay time, duration of laryngeal closure, duration of cricopharyngeal opening, percentage of oral residue, percentage of pharyngeal residue, percentage of aspiration, and oropharyngeal swallow efficiency (OPSE). OPSE, defined as the approximate percentage of the bolus swallowed into the esophagus divided by total transit time, is a global measure that describes the interaction of the speed of movement of the bolus and the safety and efficiency of the mechanism in clearing material from the oropharynx while preventing aspiration.6,21,22 The notation of the percentage swallowed is a clinical judgment based on the proportion of the bolus passing through the cricopharyngeus versus that remaining in the oropharynx. This index is a convenient measure for comparing various clinical populations that may have different impairments in the oropharyngeal swallow.22 To verify the reliability of measures used in this study, we reanalyzed 10% of the speech and swallow data. Pearson correlation coefficients for interobserver reliability ranged from 0.83 to 1.00, with a mean relia-
Postoperative radiation
6.4 7.2 39.6 62.1
(5.5) (9.7) (35.5) (9.5)
p Value
0.69 0.57 0.32 0.41
bility measure of 0.94. Pearson correlation coefficients for intraobserver reliability between the first and second measures ranged from 0.93 to 1.00, with an average reliability measure of 0.98. Patients were not required to receive speech and swallowing therapy as part of the study protocol; provision of therapy was at the discretion of the participating clinician. When therapy was provided, data were collected on the number and duration of speech/swallowing therapy sessions, as well as the individual therapy techniques instructed and practiced at each session with a standard form prepared for this study. Statistical analyses were conducted to assess the effect of radiation on postsurgical speech and swallowing function. Paired Student’s t tests revealed that the irradiated and nonirradiated patients did not differ significantly before surgery regarding any speech or swallow outcome measure except OPSE. However, to ensure that any postoperative differences observed between the groups were attributable to radiation effects and not differences in baseline performance, we
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No. days RT started after surgery
RT dose (cGy)
NA 33 NA 27 NA 25 NA 27 NA 25 NA 52 NA 60 NA 26 NA 21
0 6400 0 6000 0 5580 0 4500 0 6000 0 6000 0 6000 0 6000 0 6000
Field(s)
NA Primary, left neck, right neck NA Left neck, right neck, anterior neck NA Right neck NA Primary, left neck, right neck NA Primary NA Primary, right neck NA Primary, left neck, right neck NA Primary, left neck, right neck NA Left neck, right neck, anterior neck
used each patient’s preoperative function as a covariate in an analysis of covariance. For speech measures, the interaction of the radiation treatment group (no postoperative radiation versus postoperative radiation) and evaluation point (1, 3, 6, and 12 months after healing) was tested first; for swallow variables, the interactions among radiation treatment group (no postoperative radiation versus postoperative radiation), evaluation point (1, 3, 6, and 12 months after healing), and bolus consistency (liquid, paste) were tested first. When a significant interaction was found, the effect of radiation was analyzed by subgroup (either evaluation point or bolus consistency as appropriate). If no significant interactions were found, a test of the main effect of radiation was performed. Analysis was conducted with the general linear model procedure of SAS statistical software.23 All 18 patients received preoperative, 6-month posthealing, and 12-month posthealing evaluations, whereas 15 also received a 1-month evaluation, and 16 also received a 3-month evaluation. RESULTS
Paired Student’s t tests revealed that the irradiated and nonirradiated patients did not differ significantly regarding the percentage of oral tongue and tongue base resected, total volume resected, or age (Table 3). On average, the irradiated patients began their radiotherapy 33 days after surgery and received an average dose of 5276 cGy. As stated previously, each patient’s preoper-
Neck dissection?
Right radical Bilateral radical Right radical Right modified radical Bilateral supraomohyoid Right radical No No Right radical Left radical Left radical Right radical Left radical Left radical Right radical Left radical Right radical Left radical
ative function was used as a covariate to adjust for any differences in baseline function between the irradiated and nonirradiated patients. Therefore the data reported here reflect the mean adjusted for preoperative levels. Speech Data
Table 4 summarizes the significance test results for the interaction of the radiation treatment group and the evaluation point for speech variables. Because there were no significant interactions, the data were pooled over the evaluation point to test for the main effect of the radiation treatment group. These results are also listed in Table 4. Only the percentage of correct production of /h/ had a significant main effect, with irradiated patients having significantly lower correct articulation of that phoneme. Swallowing Data
Not all patients were able to swallow two trials of each consistency at all evaluation points. A patient may have refused to attempt one or both trials of a consistency because of known or suspected difficulty with it; the speech-language pathologist also may have judged it a clinical risk to introduce or continue with a specific consistency during the videofluoroscopy evaluation. Therefore the number of trials of each consistency at each evaluation point varied. Interaction effects. Table 5 summarizes the significance levels for interactions that include the radiation treatment group for the swallow measures. None of
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Table 4. Significance test results for the interaction of radiation status and evaluation point, means and standard errors (in parentheses) by radiation treatment group pooled across evaluation point, and significance test results for the main effect of radiation status for speech outcome measures Radiation by evaluation p value
% Conversational understandability n % Correct phonemes All phonemes /p, b/ /t, d/ /k, g/ /f, v/ /θ, δ/ /s, z/ /S, Z/ /h/ /T, D/ /r, l, w, j/ n
Radiation main effect p value
No postoperative radiation
Postoperative radiation
0.97
73.7 (2.6) 32
73.0 (2.4) 31
0.85
0.69 0.68 0.88 0.76 0.74 0.55 0.82 0.99 0.48 0.55 0.31
73.8 94.4 70.9 73.7 88.3 75.7 46.3 41.9 99.6 50.6 87.6 33
69.1 83.8 64.1 62.1 83.1 75.8 39.2 31.1 86.5 35.6 84.5 32
0.40 0.07 0.47 0.16 0.35 0.99 0.51 0.25 0.03* 0.23 0.47
(3.6) (3.9) (6.1) (5.7) (3.8) (4.5) (6.9) (6.0) (4.0) (7.7) (2.9)
(3.7) (4.1) (6.3) (5.8) (3.9) (4.5) (7.1) (5.6) (4.0) (7.9) (3.0)
n, Number of speech evaluations pooled over 1, 3, 6, and 12 months. *p ≤ 0.05.
these variables had a significant three-way interaction of radiation treatment group by evaluation point by bolus consistency. Three measures, oral transit time, pharyngeal transit time, and percentage of pharyngeal residue, had a significant two-way interaction. Oral transit time and pharyngeal transit time demonstrated significant interactions between the radiation treatment group and bolus consistency, indicating that the two groups functioned differently regarding these variables depending on bolus consistency. Because of the significant interaction, the main effect of the radiation treatment group was tested separately for each consistency. Means and standard errors, as well as the test for the main effect of the treatment group pooled over the evaluation point, are summarized in Table 6 for these variables. Oral transit time for liquid did not differ significantly between the radiation treatment groups; however, the irradiated patients had significantly longer oral transit times for paste boluses than did the nonirradiated patients (Fig. 1). Pharyngeal transit time did not differ significantly between radiation treatment groups regarding either liquid or paste boluses. The percentage of pharyngeal residue demonstrated a significant radiation by evaluation point interaction, indicating that the irradiated and nonirradiated patients differed regarding this measure as a function of time, pooled over bolus consistency. Table 7 and Fig. 2 summarize the mean percentage of pharyngeal residue as a function of the radiation treatment group and evaluation point, pooled over bolus consistency. At the 1-month posthealing evaluation, the patient groups did not dif-
fer; however, at the 3-, 6-, and 12-month evaluations, the irradiated patients had significantly more pharyngeal residue than did the nonirradiated patients. Main effect of radiation treatment group. The percentage of oral residue, pharyngeal delay time, OPSE, duration of laryngeal closure, and duration of cricopharyngeal opening did not demonstrate any significant interactions; therefore bolus consistencies and evaluation points were pooled to test the main effect of the radiation treatment group for these variables. Both OPSE and duration of cricopharyngeal opening demonstrated a significant main effect for radiation treatment group (Fig. 3). Means, standard errors, and significant post hoc test results are summarized in Table 8. Irradiated patients had significantly lower swallow efficiency and significantly shorter cricopharyngeal opening duration. Speech and Swallowing Therapy Data
Table 9 summarizes the number of speech and/or swallow therapy sessions the patients received relative to their posthealing speech and swallow assessments. Six (66.7%) of the nine patients in each treatment group received some kind of speech and/or swallowing therapy. For the nonirradiated patients, 59% of all therapy was provided before the 1-month posthealing evaluation, 6% between 1 and 3 months after healing, 23% between 3 and 6 months after healing, and 12% between 6 months and 1 year after healing. Treatment focused on increasing mobility in oral structures and improving articulation.
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Table 5. Significance test results (p values) for interactions involving radiation status for swallow function variables Radiation by consistency by evaluation
Measure
Oral transit time (sec) Pharyngeal transit time (sec) Pharyngeal delay time (sec) % Oral residue % Pharyngeal residue Oropharyngeal swallow efficiency Laryngeal closure duration (sec) Cricopharyngeal opening duration (sec) *p
0.59 0.16 0.35 0.35 0.49 0.16 0.66 0.96
Radiation by evaluation
0.44 0.09 0.48 0.41 0.0009* 0.61 0.43 0.49
Radiation by consistency
0.04* 0.049* 0.19 0.48 0.22 0.46 0.06 0.81
≤ 0.05.
Table 6. Means and standard errors (in parentheses) by radiation treatment group and bolus consistency, and significance testing results for the effect of radiation treatment group for oral transit time and pharyngeal transit time Measure
Oral transit time (sec)
Consistency
Liquid Paste
Pharyngeal transit time (sec)
Liquid Paste
No postoperative radiation
Postoperative radiation
0.48 (0.07) n = 61 1.23 (0.40) n = 63 0.86 (0.05) n = 60 1.60 (0.19) n = 64
0.67 (0.07) n = 62 3.26 (0.44) n = 59 0.90 (0.05) n = 62 1.14 (0.18) n = 57
p Value
0.053 0.0009* 0.53 0.10
n, Number of swallows pooled over 1, 3, 6, and 12 months. * p ≤ 0.05.
Table 7. Means and standard errors (in parentheses) by evaluation point and radiation status pooled over bolus consistency and significance testing results for the effect of radiation treatment group for percentage of pharyngeal residue
No postoperative radiation n Postoperative radiation n Radiation effect p value
1 Mo
3 Mo
6 Mo
12 Mo
14.6 (1.9) 30 9.1 (2.5) 28 0.09
5.8 (2.3) 31 16.1 (2.2) 32 0.002
4.0 (3.6) 36 29.2 (4.1) 31 <0.0001
7.8 (2.2) 36 20.8 (2.4) 32 0.0002
n, Number of swallows pooled over liquid and paste boluses.
For the irradiated patients, 75% of all therapy was provided before the 1-month posthealing evaluation, 18% between 1 and 3 months after healing, and 7% between 3 and 6 months after healing. The focus of therapy was similar to that of the nonirradiated group, with more emphasis on postures and maneuvers to improve swallowing function. DISCUSSION
This study demonstrates that radiation treatment in postsurgical patients with oral and oropharyngeal cancer did not influence articulation or speech intelligibil-
ity but affected aspects of both the oral and pharyngeal stages of the swallow. Hamlet et al.24 studied the recovery of tongue mobility for speech in five partial glossectomy patients before surgery, between 2 and 7 weeks after surgery, and between 4 and 10 weeks after subsequent radiotherapy (approximately 4 to 5 months after surgery). They concluded that radiotherapy after surgery did not prevent continued recovery of tongue function for speech in the early postradiation period. In this study speech function also was not negatively influenced by postoperative radiotherapy. Only production of the phoneme /h/ was
622 PAULOSKI et al.
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Fig. 1. Means and standard errors for oral transit time in seconds for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer as a function of bolus consistency pooled over evaluation point.
Fig. 3. Means and standard errors for OPSE and cricopharyngeal opening duration in seconds for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer pooled over evaluation point and bolus consistency.
Fig. 2. Means and standard errors for percentage of pharyngeal residue for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer as a function of evaluation point pooled over bolus consistency.
significantly worse for the irradiated patients. This result may reflect the impact of radiation treatment on laryngeal function rather than on articulation. Changes in the irradiated voice are associated with the reversal of the mechanical effects of the tumor and the effects of radiation on the laryngeal tissues, including both edema during treatment and fibrosis after treatment.25 All of the irradiated patients in this study had a portion of the neck in the field of radiation. This locus of treatment would certainly provide radiation to the larynx, which may have had an impact on production of the glottal fricative /h/.
In this study, irradiated patients had significantly increased oral transit time with paste boluses, greater pharyngeal residue, lower swallow efficiency, and shorter cricopharyngeal opening duration when compared with matched patients who received surgery only for treatment of their cancer. Radiotherapy produces mucositis (an inflammation of the mucous membranes of the oral cavity) and reduced salivary flow or hyposalivation during the course of treatment. The initial signs of mucositis and a significant decrease in the flow of saliva may occur as early as the end of the first week of radiotherapy. Mucositis persists through the course of radiation treatment and continues for several weeks after completion; oral erythema or redness may persist for up to 6 months after completion of radiotherapy, whereas hyposalivation is usually irreversible when the radiation dosage exceeds 40 Gy. After radiotherapy, tissues become increasingly fibrotic over time, resulting in reduced mobility of the oral musculature.12,13 The increase in oral transit time with paste boluses, as observed in the irradiated patients in this study, may be the result of hyposalivation. Difficulty with oral
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Table 8. Means and standard errors (in parentheses) by radiation treatment group pooled over evaluation point and bolus consistency, and significance testing results for the effect of radiation treatment group for swallow measures with no significant interactions Measure
No postoperative radiation
Postoperative radiation
p Value
21.90 (1.80) 133 0.26 (0.08) 127 58.20 (2.80) 119 0.46 (0.06) 131 0.41 (0.01) 130
24.30 (1.90) 123 0.13 (0.08) 120 36.70 (2.80) 120 0.46 (0.06) 116 0.35 (0.01) 120
0.37
% Oral residue n Pharyngeal delay time (sec) n Oropharyngeal swallow efficiency n Laryngeal closure duration (sec) n Cricopharyngeal opening duration (sec) n
0.27 <0.0001* 0.91 <0.0001*
n, Number of swallows pooled over 1, 3, 6, and 12 months and over liquid and paste boluses. *p ≤ 0.05.
Table 9. Number and timing relative to postoperative evaluations of speech and/or swallowing therapy sessions for each patient by radiation group No. of therapy sessions
Pair no.
Patients with no postoperative radiotherapy 1 2 3 4 5 6 7 8 9 Total sessions Patients with postoperative radiotherapy 1 2 3 4 5 6 7 8 9 Total sessions
Resection/ Before reconstruction 1 mo group evaluation
Between 1 and 3 mo evaluations
Between 3 and 6 mo evaluations
Between 6 and 12 mo evaluations
Total by 12 mo evaluation
1 2 3 4 5 6 7 8 8
0 0 0 0 0 4 4 1 1 10
0 0 0 0 0 1 0 0 0 1
0 1 1 0 0 2 0 0 0 4
0 1 0 0 0 1 0 0 0 2
0 2 1 0 0 8 4 1 1 17
1 2 3 4 5 6 7 8 8
1 0 0 4 0 7 1 7 1 21
0 0 0 0 0 4 0 1 0 5
0 1 0 0 0 0 0 1 0 2
0 0 0 0 0 0 0 0 0 0
1 1 0 4 0 11 1 9 1 28
transport of more viscous consistencies also may be the result of pain from mucositis during radiation treatment as well as increased fibrosis of the oral musculature after completion of radiotherapy causing a disruption in the ability of the tongue to produce sufficient bolus driving pressure. Increased pharyngeal residue and shortened cricopharyngeal opening duration in the irradiated patients also are indications of a reduction in pharyngeal bolus driving pressure, perhaps resulting from reduced tongue base retraction. Movement of the
tongue base and posterior pharyngeal wall toward each other until full contact is achieved is a key element in producing pharyngeal bolus driving pressure.26,27 Discomfort from mucositis and later fibrosis of the irradiated tissue may result in decreased range of motion of the oral tongue and tongue base, thereby affecting both the oral and pharyngeal swallows. Six of the nine subjects in each group received some amount of speech and swallowing therapy, with three in each group receiving tongue range-of-motion exercises.
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The irradiated patients received 75% of their therapy before the 1-month posthealing evaluation, most before the onset of radiation treatment. Only two patients received a total of one therapy session each after the completion of radiotherapy. Increased use of tongue range-of-motion exercises during and after radiation treatment may help reduce the formation of fibrotic tissue in the oral cavity and improve pharyngeal clearance by maintaining adequate contact of the tongue base to the pharyngeal wall. In summary, the irradiated subjects demonstrated difficulty with both the oral and pharyngeal stages of the swallow after radiation treatment but no change in speech function. Radiotherapy may produce edema and pain from mucositis during the course of treatment and reduced salivary flow and fibrosis of the irradiated tissue after completion. Increased use of tongue range-ofmotion exercises may help counteract the negative impact of radiation therapy on swallowing function. More research concerning the influence of radiotherapy on postsurgical patients as well as the impact of the amount, type, and timing of speech and swallowing therapy in these patients needs to be performed. REFERENCES 1. Logemann JA, Bytell DE. Swallowing disorders in three types of head and neck surgical patients. Cancer 1979;81: 469-78. 2. Logemann J. Evaluation and treatment of swallowing disorders. San Diego: College Hill; 1983. 3. Sessions D, Zill R, Schwartz S. Deglutition after conservation surgery for cancer of the larynx and pharynx. Otolaryngol Head Neck Surg 1979;87:779-6. 4. Hamlet S, Jones L, Mathog R, Bolton M, Patterson R. Bolus propulsive activity of the tongue in dysphagic cancer patients. Dysphagia 1989;3:18-23. 5. Cerenko D, McConnel F, Jackson R. Quantitative assessment of pharyngeal bolus driving forces. Otolaryngol Head Neck Surg 1989;100:57-63. 6. Logemann J. Swallowing physiology and pathophysiology. Otolaryngol Clin North Am 1988;21:613-23. 7. Pauloski BR, Logemann JA, Rademaker AW, et al. Speech and swallowing function after anterior tongue and floor of mouth resection with distal flap reconstruction. J Speech Hear Res 1993;36:267-76. 8. Logemann JA, Pauloski BR, Rademaker AW, et al. Speech and swallow function after tonsil/base of tongue resection with primary closure. Clinics in Communication Disorders J Speech Hear Res 1993;36:918-26.
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9. Lazarus C, Logemann J, Gibbons P. Effects of maneuvers on swallow functioning in a dysphagic oral cancer patient. Head Neck 1993:15:419-24. 10. McConnel FMS, Mendelsohn MS, Logemann JA. Manofluorography of deglutition after supraglottic laryngectomy. Head Neck Surg 1987;9:142-50. 11. Pauloski BR, Logemann JA, Rademaker AW, et al. Speech and swallowing function after oral and oropharyngeal resections: one-year follow-up. Head Neck 1994;16:313-22. 12. Jansma J, Vissink A, Bouma J, Vermey A, Panders AK, Gravenmade EJ. A survey of prevention and treatment regimens for oral sequelae resulting from head and neck radiotherapy used in Dutch radiotherapy institutes. International Journal of Radiation Oncology, Biology, Physics 1992;24:359-67. 13. Jansma J, Vissink A, Spijkervet FK, Roodenburg JL, Panders AK, Vermey A, Szabo BG. Protocol for the prevention and treatment of oral sequelae resulting from head and neck radiotherapy. Cancer 1992;70:2171-80. 14. Lazarus CL. Effects of radiation therapy and voluntary maneuvers on swallow function in head and neck cancer patients. Clin Comm Disord 1993;3:11-20. 15. Lazarus CL, Logemann JA, Pauloski BR, Colangelo LA, Kahrilas PJ, Mittal BB, et al. Swallowing disorders in head and neck cancer patients treated with radiotherapy and adjuvant chemotherapy. Laryngoscope 1996;160:1157-66. 16. McConnel FMS, Logemann JA, Rademaker AW, et al. Surgical variables affecting postoperative swallowing efficiency in oral cancer patients: a pilot study. Laryngoscope 1994;104:87-90. 17. Massengill R, Maxwell S, Pickrell K. An analysis of articulation following partial and total glossectomy. J Speech Hear Dis 1970;35:170-3. 18. Skelly M. Glossectomy speech rehabilitation. Springfield (IL): Charles C. Thomas; 1973. 19. Fisher HB, Logemann JA. The Fisher-Logemann test of articulation competence. Boston: Houghton Mifflin; 1971. 20. Logemann J. A manual for videofluoroscopic evaluation of swallowing. 2nd ed. Austin (TX): Pro-Ed; 1993. 21. Logemann JA, Kahrilas PJ, Kobara M, Vakil NB. Benefit of head rotation on pharyngoesophageal dysphagia. Arch Phys Med Rehabil 1989;70:767-71. 22. Rademaker AW, Pauloski BR, Logemann JA, Shanahan TK. Oropharyngeal swallow efficiency as a representative measure of swallowing function. J Speech Hear Res 1994;37:314-25. 23. SAS/STAT user’s guide. Version 6. 4th ed. Vol 2. Cary (NC): SAS Institute; 1989. 24. Hamlet SL, Mathog RH, Patterson RL, Fleming SM. Tongue mobility in speech after partial glossectomy. Head Neck 1990;12:210-7. 25. Miller S, Harrison LB, Solomon B, Sessions RB. Vocal changes in patients undergoing radiation therapy for glottic carcinoma. Laryngoscope 1990;100:603-6. 26. Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology 1989;97:1469-78. 27. Shawker TH, Sonies BC, Stone M, Baum BJ. Real-time ultrasound visualization of tongue movements during swallowing. J Clin Ultrasound 1983;11:485-90.
Evanston, Illinois The effect of radiation on speech and swallowing function was assessed for 18 patients surgically treated for oral and oropharyngeal cancer. Nine patients received surgical intervention and postoperative radiation therapy, and nine received surgery only. Patients were matched regarding percentage of oral tongue resected, percentage of tongue base resected, locus of resection, and method of reconstruction. Speech and swallowing function was assessed before and at 1, 3, 6, and 12 months after surgery following a standardized protocol. Speech tasks included an audio recording of a brief conversation and of a standard articulation test; swallowing function was examined with videofluoroscopy. Statistical testing indicated that overall speech function did not differ between the irradiated and nonirradiated patients. Irradiated patients had significantly reduced oral and pharyngeal swallowing performance, specifically, longer oral transit times on paste boluses, lower oropharyngeal swallow efficiency, increased pharyngeal residue, and reduced cricopharyngeal opening duration. Impaired function may be the result of radiation effects such as edema, fibrosis, and reduced salivary flow. Increased use of tongue range-ofmotion exercises during and after radiation treatment may reduce the formation of fibrotic tissue in the oral cavity and may improve pharyngeal clearance by maintaining adequate tongue base-to–pharyngeal wall contact. (Otolaryngol Head Neck Surg 1998;118:616-24.)
T
he presence of speech and swallowing problems in surgically treated head and neck cancer patients has been well documented in the literature.1-11 Speech and swallowing function in postsurgical head and neck cancer patients may be affected by the degree of resection and the nature of reconstruction. Articulation and the oral stage of the swallow are generally more severely impaired, although the pharyngeal stage of the swallow may be affected if resection includes the tongue base.7,8 Radiation therapy is often used in conjunction with surgical resection of oral and oropharyngeal tumors to control the spread of disease. In addition to the desired antitumor effects, however, radiation therapy to the head and neck induces damage in normal tissues that may From the Departments of Communication Sciences and Disorders (Drs. Pauloski and Logemann), Preventive Medicine (Dr. Rademaker and Ms. Colangelo), and Otolaryngology–Head and Neck Surgery (Dr. Logemann), Northwestern University. Funded by NIH/NCI grant no. P01CA40007. Presented in part at the Fourth Research Workshop on the Biology, Prevention, and Treatment of Head and Neck Cancer, Arlington, Va., Sept. 8-11, 1994, and the annual convention of the American Speech-Language-Hearing Association, New Orleans, La., Nov. 17-21, 1994. Reprint requests: Barbara Roa Pauloski, PhD, Northwestern University, 2299 N. Campus Dr., Evanston, IL 60208. Copyright © 1998 by the American Academy of Otolaryngology– Head and Neck Surgery Foundation, Inc. 0194-5998/98/$5.00 + 0 23/1/85014 616
result in side effects such as mucositis, hyposalivation, radiation caries, trismus, soft tissue necrosis, and osteoradionecrosis of the mandible.12,13 Radiotherapy with or without chemotherapy as a primary treatment modality may result in immediate and long-term changes in swallowing function. Irradiated patients demonstrate pharyngeal swallow disorders, including reduced tongue base contact to the posterior pharyngeal wall, reduced laryngeal elevation, and reduced vestibule and true vocal cord closure during the swallow.14,15 The effect of postoperative radiotherapy on oral functions in surgically treated patients with head and neck cancer has not been well documented in the literature. This study was designed to examine the impact of postoperative radiation therapy on speech and swallowing function in two groups of irradiated and nonirradiated patients with oral and oropharyngeal resections carefully matched on key surgical variables.16 METHODS Subjects
Eighteen patients participated in this study. Nine patients (5 men and 4 women; average age, 62 years) received surgical intervention and postoperative radiation therapy for treatment of their tumors, whereas nine (8 men and 1 woman; average age, 58 years) received surgery only. These patients were selected from a prospectively collected database of surgically treated
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Table 1. Summary of resection and reconstruction types received by patients in this study Resection reconstruction group
1 2 3 4 5 6 7 8
Description of surgical procedure
Anterior tongue only with primary closure Anterior tongue, FOM, segmental mandibular resection with primary closure Anterior tongue, FOM, mandible preserved with distal flap closure Soft palate resection only with primary closure ≤1 cm tongue base, tonsil, mandible preserved with primary closure >1 cm tongue base, tonsil, mandible preserved with primary closure >1 cm tongue base, tonsil, mandible preserved with skin graft closure >1 cm tongue base, tonsil, segmental mandibular resection with primary closure
No. of patient pairs/group
1 1 1 1 1 1 1 2
FOM, Floor of mouth.
patients with oral and oropharyngeal cancer. Subjects were matched regarding surgical resection site, percentage of oral tongue resected (±10%), percentage of tongue base resected (±20%), and method of reconstruction. The amounts of oral tongue and tongue base resected have been demonstrated to be the primary correlates of speech and swallowing impairment in postsurgical patients with oral and oropharyngeal cancer,16-18 so it was important to match on these variables. Patients were not matched regarding total volume of resected tissue because previous research has indicated that resection volume does not correlate with postoperative oral function.16 The nine pairs of patients fell into eight resection/ reconstruction categories. Table 1 summarizes these groups. For each pair of patients, Table 2 summarizes the resection/reconstruction group, tumor stage, radiation dosage and fields when applicable, and status of neck dissection. Although the patients in each pair had primary tumors of similar size, the patients who received postoperative radiotherapy tended to have more advanced disease, as evidenced by greater nodal involvement. Six patient pairs had the same degree of neck dissection; in two pairs, the irradiated patient had a greater amount of neck dissected, and in one pair the nonirradiated patient had a larger neck dissection. Irradiated patients in general began their postoperative radiotherapy within the first month after surgery, although several began in their second month. All subjects began radiotherapy before the 3-month posthealing evaluation. Data Collection, Reduction, and Analysis
The study protocol for this project was approved by the Institutional Review Board at Northwestern University for use in human subjects; informed consent was obtained from all patients. Speech and swallowing performance were assessed before surgery and 1, 3, 6,
and 12 months after healing. Healing was defined as the time when the patient’s surgeon indicated that the suture lines could withstand oral functions, generally 10 to 12 days after surgery. No patient in whom a fistula or other complication in healing developed was included in the study. Therefore the date of healing was chosen as a comparable point across patients. Speech tasks consisted of an audio recording of a 6to 7-minute conversation and the sentence version of the Fisher-Logemann Test of Articulation Competence.19 Swallowing function was examined with the modified barium swallow procedure20 by use of videofluoroscopy. Each patient attempted to complete two swallows each of 1 ml of barium liquid and 1 ml of barium paste. All boluses were administered from a teaspoon. These bolus types are part of the standard clinical protocol for assessing patient behavior with various food consistencies. The bolus sizes were chosen for ease of administration and to reduce the likelihood of aspiration of large amounts. Not all patients were able to swallow two trials of each food consistency at each evaluation point. A patient may have refused to attempt one or both trials of a consistency because of known or suspected difficulty with it; the speech-language pathologist also may have judged it a clinical risk to introduce or continue with a specific consistency during the videofluorographic evaluation. Fluoroscopic data were recorded on 3/4-inch videotape at 30 frames per second. During the study, the fluoroscopy tube was focused on the lips anteriorly, the cervical vertebrae posteriorly, the soft palate superiorly, and the bifurcation of the esophagus and airway inferiorly. Data reduction was completed according to the methods described by Pauloski et al.,7 resulting in the following speech and swallowing measures: percentage of perceived correct production of consonant phonemes, percentage of conversational understandability, oral transit time, pharyngeal transit time, pha-
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Table 2. Summary of patient characteristics by matched pairs
Pair
Resection/ reconstruction group
1
1
2
2
3
3
4
4
5
5
6
6
7
7
8
8
9
8
Sex
M M M F F M M F M M M M M M M F M F
Age (yr)
72 59 54 64 54 69 76 61 54 45 60 75 27 69 50 66 71 50
Volume resected (ml)
7.2 3.0 35 63 140 36.75 72 13.05 1.08 10.0 210.00 34.83 84.0 50.0 42 119 8.8 27
% Oral tongue resected
10 15 0 10 10 0 0 0 0 5 5 0 17.5 10 2 8 5 10
% Tongue base resected
Tumor stage
0 0 0 0 0 0 0 0 15 0 5 20 20 10 5 25 0 10
T2N1M0 T2N3bM0 T2N2bM0 T2N0M0 T2N1M0 T2N2bM0 T3N0M0 T3N0M0 T2N0M0 T2N0M0 T3N1M0 T2N0M0 T3N1M0 T3N2bM0 T2N1M0 T3N2aM0 T3N0M0 T3N1M0
Resection/reconstruction groups are summarized in Table 1. NA, Not applicable.
Table 3. Means and standard deviations (in parentheses) for patient demographics by radiation treatment group and paired Student’s t test p values No postoperative radiation
% Oral tongue resected % Tongue base resected Resection volume (ml) Age (yr)
5.5 5.0 66.7 56.4
(6.0) (7.5) (69.9) (14.0)
ryngeal delay time, duration of laryngeal closure, duration of cricopharyngeal opening, percentage of oral residue, percentage of pharyngeal residue, percentage of aspiration, and oropharyngeal swallow efficiency (OPSE). OPSE, defined as the approximate percentage of the bolus swallowed into the esophagus divided by total transit time, is a global measure that describes the interaction of the speed of movement of the bolus and the safety and efficiency of the mechanism in clearing material from the oropharynx while preventing aspiration.6,21,22 The notation of the percentage swallowed is a clinical judgment based on the proportion of the bolus passing through the cricopharyngeus versus that remaining in the oropharynx. This index is a convenient measure for comparing various clinical populations that may have different impairments in the oropharyngeal swallow.22 To verify the reliability of measures used in this study, we reanalyzed 10% of the speech and swallow data. Pearson correlation coefficients for interobserver reliability ranged from 0.83 to 1.00, with a mean relia-
Postoperative radiation
6.4 7.2 39.6 62.1
(5.5) (9.7) (35.5) (9.5)
p Value
0.69 0.57 0.32 0.41
bility measure of 0.94. Pearson correlation coefficients for intraobserver reliability between the first and second measures ranged from 0.93 to 1.00, with an average reliability measure of 0.98. Patients were not required to receive speech and swallowing therapy as part of the study protocol; provision of therapy was at the discretion of the participating clinician. When therapy was provided, data were collected on the number and duration of speech/swallowing therapy sessions, as well as the individual therapy techniques instructed and practiced at each session with a standard form prepared for this study. Statistical analyses were conducted to assess the effect of radiation on postsurgical speech and swallowing function. Paired Student’s t tests revealed that the irradiated and nonirradiated patients did not differ significantly before surgery regarding any speech or swallow outcome measure except OPSE. However, to ensure that any postoperative differences observed between the groups were attributable to radiation effects and not differences in baseline performance, we
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No. days RT started after surgery
RT dose (cGy)
NA 33 NA 27 NA 25 NA 27 NA 25 NA 52 NA 60 NA 26 NA 21
0 6400 0 6000 0 5580 0 4500 0 6000 0 6000 0 6000 0 6000 0 6000
Field(s)
NA Primary, left neck, right neck NA Left neck, right neck, anterior neck NA Right neck NA Primary, left neck, right neck NA Primary NA Primary, right neck NA Primary, left neck, right neck NA Primary, left neck, right neck NA Left neck, right neck, anterior neck
used each patient’s preoperative function as a covariate in an analysis of covariance. For speech measures, the interaction of the radiation treatment group (no postoperative radiation versus postoperative radiation) and evaluation point (1, 3, 6, and 12 months after healing) was tested first; for swallow variables, the interactions among radiation treatment group (no postoperative radiation versus postoperative radiation), evaluation point (1, 3, 6, and 12 months after healing), and bolus consistency (liquid, paste) were tested first. When a significant interaction was found, the effect of radiation was analyzed by subgroup (either evaluation point or bolus consistency as appropriate). If no significant interactions were found, a test of the main effect of radiation was performed. Analysis was conducted with the general linear model procedure of SAS statistical software.23 All 18 patients received preoperative, 6-month posthealing, and 12-month posthealing evaluations, whereas 15 also received a 1-month evaluation, and 16 also received a 3-month evaluation. RESULTS
Paired Student’s t tests revealed that the irradiated and nonirradiated patients did not differ significantly regarding the percentage of oral tongue and tongue base resected, total volume resected, or age (Table 3). On average, the irradiated patients began their radiotherapy 33 days after surgery and received an average dose of 5276 cGy. As stated previously, each patient’s preoper-
Neck dissection?
Right radical Bilateral radical Right radical Right modified radical Bilateral supraomohyoid Right radical No No Right radical Left radical Left radical Right radical Left radical Left radical Right radical Left radical Right radical Left radical
ative function was used as a covariate to adjust for any differences in baseline function between the irradiated and nonirradiated patients. Therefore the data reported here reflect the mean adjusted for preoperative levels. Speech Data
Table 4 summarizes the significance test results for the interaction of the radiation treatment group and the evaluation point for speech variables. Because there were no significant interactions, the data were pooled over the evaluation point to test for the main effect of the radiation treatment group. These results are also listed in Table 4. Only the percentage of correct production of /h/ had a significant main effect, with irradiated patients having significantly lower correct articulation of that phoneme. Swallowing Data
Not all patients were able to swallow two trials of each consistency at all evaluation points. A patient may have refused to attempt one or both trials of a consistency because of known or suspected difficulty with it; the speech-language pathologist also may have judged it a clinical risk to introduce or continue with a specific consistency during the videofluoroscopy evaluation. Therefore the number of trials of each consistency at each evaluation point varied. Interaction effects. Table 5 summarizes the significance levels for interactions that include the radiation treatment group for the swallow measures. None of
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Table 4. Significance test results for the interaction of radiation status and evaluation point, means and standard errors (in parentheses) by radiation treatment group pooled across evaluation point, and significance test results for the main effect of radiation status for speech outcome measures Radiation by evaluation p value
% Conversational understandability n % Correct phonemes All phonemes /p, b/ /t, d/ /k, g/ /f, v/ /θ, δ/ /s, z/ /S, Z/ /h/ /T, D/ /r, l, w, j/ n
Radiation main effect p value
No postoperative radiation
Postoperative radiation
0.97
73.7 (2.6) 32
73.0 (2.4) 31
0.85
0.69 0.68 0.88 0.76 0.74 0.55 0.82 0.99 0.48 0.55 0.31
73.8 94.4 70.9 73.7 88.3 75.7 46.3 41.9 99.6 50.6 87.6 33
69.1 83.8 64.1 62.1 83.1 75.8 39.2 31.1 86.5 35.6 84.5 32
0.40 0.07 0.47 0.16 0.35 0.99 0.51 0.25 0.03* 0.23 0.47
(3.6) (3.9) (6.1) (5.7) (3.8) (4.5) (6.9) (6.0) (4.0) (7.7) (2.9)
(3.7) (4.1) (6.3) (5.8) (3.9) (4.5) (7.1) (5.6) (4.0) (7.9) (3.0)
n, Number of speech evaluations pooled over 1, 3, 6, and 12 months. *p ≤ 0.05.
these variables had a significant three-way interaction of radiation treatment group by evaluation point by bolus consistency. Three measures, oral transit time, pharyngeal transit time, and percentage of pharyngeal residue, had a significant two-way interaction. Oral transit time and pharyngeal transit time demonstrated significant interactions between the radiation treatment group and bolus consistency, indicating that the two groups functioned differently regarding these variables depending on bolus consistency. Because of the significant interaction, the main effect of the radiation treatment group was tested separately for each consistency. Means and standard errors, as well as the test for the main effect of the treatment group pooled over the evaluation point, are summarized in Table 6 for these variables. Oral transit time for liquid did not differ significantly between the radiation treatment groups; however, the irradiated patients had significantly longer oral transit times for paste boluses than did the nonirradiated patients (Fig. 1). Pharyngeal transit time did not differ significantly between radiation treatment groups regarding either liquid or paste boluses. The percentage of pharyngeal residue demonstrated a significant radiation by evaluation point interaction, indicating that the irradiated and nonirradiated patients differed regarding this measure as a function of time, pooled over bolus consistency. Table 7 and Fig. 2 summarize the mean percentage of pharyngeal residue as a function of the radiation treatment group and evaluation point, pooled over bolus consistency. At the 1-month posthealing evaluation, the patient groups did not dif-
fer; however, at the 3-, 6-, and 12-month evaluations, the irradiated patients had significantly more pharyngeal residue than did the nonirradiated patients. Main effect of radiation treatment group. The percentage of oral residue, pharyngeal delay time, OPSE, duration of laryngeal closure, and duration of cricopharyngeal opening did not demonstrate any significant interactions; therefore bolus consistencies and evaluation points were pooled to test the main effect of the radiation treatment group for these variables. Both OPSE and duration of cricopharyngeal opening demonstrated a significant main effect for radiation treatment group (Fig. 3). Means, standard errors, and significant post hoc test results are summarized in Table 8. Irradiated patients had significantly lower swallow efficiency and significantly shorter cricopharyngeal opening duration. Speech and Swallowing Therapy Data
Table 9 summarizes the number of speech and/or swallow therapy sessions the patients received relative to their posthealing speech and swallow assessments. Six (66.7%) of the nine patients in each treatment group received some kind of speech and/or swallowing therapy. For the nonirradiated patients, 59% of all therapy was provided before the 1-month posthealing evaluation, 6% between 1 and 3 months after healing, 23% between 3 and 6 months after healing, and 12% between 6 months and 1 year after healing. Treatment focused on increasing mobility in oral structures and improving articulation.
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Table 5. Significance test results (p values) for interactions involving radiation status for swallow function variables Radiation by consistency by evaluation
Measure
Oral transit time (sec) Pharyngeal transit time (sec) Pharyngeal delay time (sec) % Oral residue % Pharyngeal residue Oropharyngeal swallow efficiency Laryngeal closure duration (sec) Cricopharyngeal opening duration (sec) *p
0.59 0.16 0.35 0.35 0.49 0.16 0.66 0.96
Radiation by evaluation
0.44 0.09 0.48 0.41 0.0009* 0.61 0.43 0.49
Radiation by consistency
0.04* 0.049* 0.19 0.48 0.22 0.46 0.06 0.81
≤ 0.05.
Table 6. Means and standard errors (in parentheses) by radiation treatment group and bolus consistency, and significance testing results for the effect of radiation treatment group for oral transit time and pharyngeal transit time Measure
Oral transit time (sec)
Consistency
Liquid Paste
Pharyngeal transit time (sec)
Liquid Paste
No postoperative radiation
Postoperative radiation
0.48 (0.07) n = 61 1.23 (0.40) n = 63 0.86 (0.05) n = 60 1.60 (0.19) n = 64
0.67 (0.07) n = 62 3.26 (0.44) n = 59 0.90 (0.05) n = 62 1.14 (0.18) n = 57
p Value
0.053 0.0009* 0.53 0.10
n, Number of swallows pooled over 1, 3, 6, and 12 months. * p ≤ 0.05.
Table 7. Means and standard errors (in parentheses) by evaluation point and radiation status pooled over bolus consistency and significance testing results for the effect of radiation treatment group for percentage of pharyngeal residue
No postoperative radiation n Postoperative radiation n Radiation effect p value
1 Mo
3 Mo
6 Mo
12 Mo
14.6 (1.9) 30 9.1 (2.5) 28 0.09
5.8 (2.3) 31 16.1 (2.2) 32 0.002
4.0 (3.6) 36 29.2 (4.1) 31 <0.0001
7.8 (2.2) 36 20.8 (2.4) 32 0.0002
n, Number of swallows pooled over liquid and paste boluses.
For the irradiated patients, 75% of all therapy was provided before the 1-month posthealing evaluation, 18% between 1 and 3 months after healing, and 7% between 3 and 6 months after healing. The focus of therapy was similar to that of the nonirradiated group, with more emphasis on postures and maneuvers to improve swallowing function. DISCUSSION
This study demonstrates that radiation treatment in postsurgical patients with oral and oropharyngeal cancer did not influence articulation or speech intelligibil-
ity but affected aspects of both the oral and pharyngeal stages of the swallow. Hamlet et al.24 studied the recovery of tongue mobility for speech in five partial glossectomy patients before surgery, between 2 and 7 weeks after surgery, and between 4 and 10 weeks after subsequent radiotherapy (approximately 4 to 5 months after surgery). They concluded that radiotherapy after surgery did not prevent continued recovery of tongue function for speech in the early postradiation period. In this study speech function also was not negatively influenced by postoperative radiotherapy. Only production of the phoneme /h/ was
622 PAULOSKI et al.
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Fig. 1. Means and standard errors for oral transit time in seconds for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer as a function of bolus consistency pooled over evaluation point.
Fig. 3. Means and standard errors for OPSE and cricopharyngeal opening duration in seconds for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer pooled over evaluation point and bolus consistency.
Fig. 2. Means and standard errors for percentage of pharyngeal residue for irradiated and nonirradiated postsurgical patients with oral and oropharyngeal cancer as a function of evaluation point pooled over bolus consistency.
significantly worse for the irradiated patients. This result may reflect the impact of radiation treatment on laryngeal function rather than on articulation. Changes in the irradiated voice are associated with the reversal of the mechanical effects of the tumor and the effects of radiation on the laryngeal tissues, including both edema during treatment and fibrosis after treatment.25 All of the irradiated patients in this study had a portion of the neck in the field of radiation. This locus of treatment would certainly provide radiation to the larynx, which may have had an impact on production of the glottal fricative /h/.
In this study, irradiated patients had significantly increased oral transit time with paste boluses, greater pharyngeal residue, lower swallow efficiency, and shorter cricopharyngeal opening duration when compared with matched patients who received surgery only for treatment of their cancer. Radiotherapy produces mucositis (an inflammation of the mucous membranes of the oral cavity) and reduced salivary flow or hyposalivation during the course of treatment. The initial signs of mucositis and a significant decrease in the flow of saliva may occur as early as the end of the first week of radiotherapy. Mucositis persists through the course of radiation treatment and continues for several weeks after completion; oral erythema or redness may persist for up to 6 months after completion of radiotherapy, whereas hyposalivation is usually irreversible when the radiation dosage exceeds 40 Gy. After radiotherapy, tissues become increasingly fibrotic over time, resulting in reduced mobility of the oral musculature.12,13 The increase in oral transit time with paste boluses, as observed in the irradiated patients in this study, may be the result of hyposalivation. Difficulty with oral
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Table 8. Means and standard errors (in parentheses) by radiation treatment group pooled over evaluation point and bolus consistency, and significance testing results for the effect of radiation treatment group for swallow measures with no significant interactions Measure
No postoperative radiation
Postoperative radiation
p Value
21.90 (1.80) 133 0.26 (0.08) 127 58.20 (2.80) 119 0.46 (0.06) 131 0.41 (0.01) 130
24.30 (1.90) 123 0.13 (0.08) 120 36.70 (2.80) 120 0.46 (0.06) 116 0.35 (0.01) 120
0.37
% Oral residue n Pharyngeal delay time (sec) n Oropharyngeal swallow efficiency n Laryngeal closure duration (sec) n Cricopharyngeal opening duration (sec) n
0.27 <0.0001* 0.91 <0.0001*
n, Number of swallows pooled over 1, 3, 6, and 12 months and over liquid and paste boluses. *p ≤ 0.05.
Table 9. Number and timing relative to postoperative evaluations of speech and/or swallowing therapy sessions for each patient by radiation group No. of therapy sessions
Pair no.
Patients with no postoperative radiotherapy 1 2 3 4 5 6 7 8 9 Total sessions Patients with postoperative radiotherapy 1 2 3 4 5 6 7 8 9 Total sessions
Resection/ Before reconstruction 1 mo group evaluation
Between 1 and 3 mo evaluations
Between 3 and 6 mo evaluations
Between 6 and 12 mo evaluations
Total by 12 mo evaluation
1 2 3 4 5 6 7 8 8
0 0 0 0 0 4 4 1 1 10
0 0 0 0 0 1 0 0 0 1
0 1 1 0 0 2 0 0 0 4
0 1 0 0 0 1 0 0 0 2
0 2 1 0 0 8 4 1 1 17
1 2 3 4 5 6 7 8 8
1 0 0 4 0 7 1 7 1 21
0 0 0 0 0 4 0 1 0 5
0 1 0 0 0 0 0 1 0 2
0 0 0 0 0 0 0 0 0 0
1 1 0 4 0 11 1 9 1 28
transport of more viscous consistencies also may be the result of pain from mucositis during radiation treatment as well as increased fibrosis of the oral musculature after completion of radiotherapy causing a disruption in the ability of the tongue to produce sufficient bolus driving pressure. Increased pharyngeal residue and shortened cricopharyngeal opening duration in the irradiated patients also are indications of a reduction in pharyngeal bolus driving pressure, perhaps resulting from reduced tongue base retraction. Movement of the
tongue base and posterior pharyngeal wall toward each other until full contact is achieved is a key element in producing pharyngeal bolus driving pressure.26,27 Discomfort from mucositis and later fibrosis of the irradiated tissue may result in decreased range of motion of the oral tongue and tongue base, thereby affecting both the oral and pharyngeal swallows. Six of the nine subjects in each group received some amount of speech and swallowing therapy, with three in each group receiving tongue range-of-motion exercises.
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The irradiated patients received 75% of their therapy before the 1-month posthealing evaluation, most before the onset of radiation treatment. Only two patients received a total of one therapy session each after the completion of radiotherapy. Increased use of tongue range-of-motion exercises during and after radiation treatment may help reduce the formation of fibrotic tissue in the oral cavity and improve pharyngeal clearance by maintaining adequate contact of the tongue base to the pharyngeal wall. In summary, the irradiated subjects demonstrated difficulty with both the oral and pharyngeal stages of the swallow after radiation treatment but no change in speech function. Radiotherapy may produce edema and pain from mucositis during the course of treatment and reduced salivary flow and fibrosis of the irradiated tissue after completion. Increased use of tongue range-ofmotion exercises may help counteract the negative impact of radiation therapy on swallowing function. More research concerning the influence of radiotherapy on postsurgical patients as well as the impact of the amount, type, and timing of speech and swallowing therapy in these patients needs to be performed. REFERENCES 1. Logemann JA, Bytell DE. Swallowing disorders in three types of head and neck surgical patients. Cancer 1979;81: 469-78. 2. Logemann J. Evaluation and treatment of swallowing disorders. San Diego: College Hill; 1983. 3. Sessions D, Zill R, Schwartz S. Deglutition after conservation surgery for cancer of the larynx and pharynx. Otolaryngol Head Neck Surg 1979;87:779-6. 4. Hamlet S, Jones L, Mathog R, Bolton M, Patterson R. Bolus propulsive activity of the tongue in dysphagic cancer patients. Dysphagia 1989;3:18-23. 5. Cerenko D, McConnel F, Jackson R. Quantitative assessment of pharyngeal bolus driving forces. Otolaryngol Head Neck Surg 1989;100:57-63. 6. Logemann J. Swallowing physiology and pathophysiology. Otolaryngol Clin North Am 1988;21:613-23. 7. Pauloski BR, Logemann JA, Rademaker AW, et al. Speech and swallowing function after anterior tongue and floor of mouth resection with distal flap reconstruction. J Speech Hear Res 1993;36:267-76. 8. Logemann JA, Pauloski BR, Rademaker AW, et al. Speech and swallow function after tonsil/base of tongue resection with primary closure. Clinics in Communication Disorders J Speech Hear Res 1993;36:918-26.
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