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Laryngeal Penetration and Aspiration During Swallowing After the Treatment of Advanced Oropharyngeal Cancer
M. Boyd Gillespie, MD;
Martin B. Brodsky, MA;
Terry A. Day, MD;
Anand K. Sharma, MD;
Fu-shing Lee, PhD;
Bonnie Martin-Harris, PhD
Arch Otolaryngol Head Neck Surg. 2005;131:615-619.
ABSTRACT
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Objective To determine whether laryngeal penetration and aspiration in oropharyngeal cancer survivors differ by treatment group.
Design Cross-sectional study of patients with stage III or IV oropharyngeal squamous cell carcinoma who were at least 12 months removed from combined modality therapy and clinically free of disease.
Subjects Potential subjects were stratified by tumor site and tumor T stage to achieve a similar comparison between chemoradiotherapy (n = 10) and surgery/radiotherapy (n = 11) groups. Validated instruments used to evaluate swallowing included the Penetration-Aspiration Scale and the M. D. Anderson Dysphagia Inventory.
Results Patients with oropharyngeal cancer treated with chemoradiotherapy demonstrated greater airway protection according to Penetration-Aspiration Scale scores than those treated with surgery and radiotherapy on 5-mL (P = .02), 10-mL (P = .04), and 20-mL (P = .04) liquid barium swallows. Also, the oropharyngeal chemoradiotherapy group had better self-perceived swallowing ability than the surgery-radiotherapy group on the basis of the M. D. Anderson Dysphagia Inventory (P = .02).
Conclusion The present study suggests that patients with oropharyngeal cancer who successfully complete chemoradiotherapy protocols without surgical salvage retain greater airway protection during swallowing and better swallowing-related quality of life than patients treated with primary surgery and radiotherapy.
INTRODUCTION
Dysphagia, or impairment of swallowing function, is a frequent consequence of head and neck cancer and its treatment that can result in decreased quality of life and nutritional deficiency. Dysphagia is present in up to 50% of head and neck cancer survivors, especially those with advanced-stage disease.1 Approximately half of the 40 000 cases of head and neck cancer diagnosed in the United States in 2002 presented with stage III or IV disease.2 Therefore, the incidence of head and neck cancer–related dysphagia is estimated to be 10 000 to 20 000 new cases per year.
The treatment of advanced squamous cell carcinoma of the head and neck has evolved over the last decade to include combination chemotherapy and external beam radiotherapy. Comparable survival rates have been achieved with chemoradiotherapy (CRT) with surgical salvage vs surgery and radiation therapy (SRT) for multiple head and neck sites.3-5 Chemoradiotherapy is commonly referred to as the organ-preservation approach because it allows a certain percentage of individuals to avoid surgical extirpation of cancerous tissues. Although the detrimental effects of both SRT and CRT on swallowing have been well documented in a number of case series,6-10 few studies have directly compared the swallowing outcomes of patients who undergo SRT with those who undergo CRT. This lack of information may in part be a result of a lack of agreement as to which components of swallowing are most highly associated with important patient outcomes, such as airway protection, dietary intake, nutritional status, and quality of life. Given the comparable survival rates of CRT and SRT, information concerning the swallowing consequences of treatment would be helpful to patients and clinicians who must decide between competing treatment strategies.11 We therefore sought to determine whether airway protection during swallowing differs by treatment group in a limited set of oropharyngeal cancer survivors.
METHODS
The present study was a 2-institution, cross-sectional survey of adult patients ( 18 years of age) at least 12 months after treatment of a stage III or IV squamous cell carcinoma of the oropharynx. Evidence suggests that swallowing function after treatment of head and neck cancer reaches a steady state that is representative of long-term outcome at approximately 12 months after therapy.9, 12-13 Swallowing continues to evolve during the first 12 months after therapy owing to the delayed effects of radiotherapy, including gradual fibrosis of the pharyngeal muscles and soft tissues.12 The 12-month period was chosen to maximize potential recruitment, while allowing the effects of delayed fibrosis to become manifest. The institutional review board of the Medical University of South Carolina, Charleston, approved the study design and the informed consent process.
Eligible subjects were identified and stratified by tumor subsite, T stage, and treatment modality using information available from the cancer registries of the Medical University of South Carolina–Hollings Cancer Center and the Ralph H. Johnson Veterans Affairs Medical Center, Charleston. Eligible subjects included surviving adult patients (18 years of age) at least 12 months after treatment of a stage III or IV squamous cell carcinoma of the oropharynx with either CRT with or without neck dissection or surgery followed by postoperative irradiation (SRT). Chemotherapy had to be delivered as a primary modality with curative intent. Patients receiving triple therapy (chemotherapy, surgery, and irradiation) and patients with neurologic conditions (eg, stroke or neurodegenerative disease) that would affect swallowing were excluded. Potential subjects were contacted via telephone to ask them to participate in the study. When a subject agreed to participate, an attempt was made to recruit a subject matched for tumor site and T stage from the other treatment group to maximize balance between treatment groups.
The study was performed in the Otolaryngology–Head and Neck Surgery Clinic and the Evelyn Trammell Center for Voice and Swallowing at the Medical University of South Carolina. A complete head and neck examination with flexible laryngoscopy was performed on all subjects to rule out persistent or recurrent tumor. Subjects completed the M. D. Anderson Dysphagia Inventory (MDADI),14 a validated instrument to assess the effects of dysphagia on swallowing-related quality of life in the head and neck population, and underwent a modified barium swallow (MBS) under the direction of a speech-language pathologist and radiologist. The MBS protocol consisted of a series of two 5-, 10-, and 20-mL swallows of thin liquid barium. The MBS was concluded early if the patient demonstrated evidence of aspiration with decreased airway clearance or if the patient refused to proceed. The results of all MBS examinations were stored on a digital recording device (60 images per second) that allows rapid retrieval and review (Digital Swallowing Workstation Model 7200; Kay Elemetrics Corp, Lincoln Park, NJ). All results were recorded with a subject research number only, without the patient information being identified on the viewing screen.
Two speech-language pathologists (M.B.B. and B.M.-H.) who were blinded to patient history and treatment group scored each swallowing trial using the previously validated Penetration-Aspiration Scale (PAS).15
The PAS score is assigned based on the level of penetration or aspiration and on the patient response to airway contamination during videofluoroscopy. The mean PAS scores for each volume were calculated and compared between treatment groups.
The MDADI scores were obtained on all subjects. Similar to many quality-of-life instruments, the MDADI is divided into several subscales (ie, global, emotional, functional, and physical) to capture to full breadth of the disorder’s impact on quality of life. The global subscale consists of a single question to assess the patient’s perception of the degree of swallowing impairment. The emotional subscale consists of 6 questions that assess the degree to which the patient is upset or embarrassed by his or her swallowing problem. The functional subscale includes 5 questions that are designed to assess ease of food preparation and eating in public. The 8 questions on the physical subscale assess the effects of dysphagia on the patient’s reports of dietary consistency, aspiration, maintenance of weight, and fatigue. The mean of the MDADI subscale scores (MDADI total) was calculated for each subject to produce a single numerical value that is representative of overall swallowing ability, with a score of 100 indicating no dysphagia and a score of 20 representing severe dysphagia.
Treatment groups were compared with regard to the number of swallows performed vs the number of swallows intended per the protocol using a  2 test. The PAS scores were analyzed between groups using the Wilcoxon rank sum test for ordinal data. The MDADI scores did not differ significantly from the normal distribution when tested (P=.80); therefore, these scores were treated as a continuous variable that allowed comparison using a t test. Spearman correlation was used to determine whether there was an association between the MDADI scores and the PAS scores. Because of the pilot nature of the study, the  level for all comparisons was set at .05 using a standard statistical software package (Stata version 7.0; Stata Corp, College Station, Tex).
RESULTS
A total of 21 subjects with oropharyngeal cancer entered the study: 11 in the SRT group and 10 in the CRT group. Comparisons between the 2 groups revealed no significant differences in mean age of the subjects, sex distribution, and mean time since treatment or oropharyngeal subsite (Table 1). When the T stages of the 2 groups were compared by tumor site, the CRT group had slightly higher-stage tumors than the SRT group.
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Table 1. Baseline Characteristics of Treatment Groups
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Surgery for oropharyngeal cancer consisted of wide excision with primary closure or skin graft in 7 subjects, wide excision with radial forearm free flap in 3 subjects, and wide excision with levator scapula flap in 1 subject. Three of the patients who underwent oropharyngeal surgery had a transoral resection, with the remaining 8 requiring mandibulotomy or pharyngotomy approaches. Chemotherapy consisted of concomitant CRT with cisplatin and fluorouracil in 7 subjects, cisplatin and paclitaxel in 2 subjects, and cisplatin, fluorouracil, and paclitaxel in 1 subject.
Subjects were assessed for the consistency of their present diet compared with their diet at the time of their cancer diagnosis. At diagnosis, 20 subjects (95%) consumed a complex diet of all solids and liquids, and 1 subject (5%) consumed only soft solids and liquids. At the time of the study, 10 patients (48%) consumed a complex diet of all solids and liquids, 7 patients (33%) consumed only soft solids and liquids, 3 patients (14%) were limited to ground solids and purees with liquids, and 1 patient (5%) received only tube feedings. Significantly fewer patients in the SRT group (2/11) than in the CRT group (8/10) were able to consume a complex diet of all solids and liquids after treatment (Table 2). There was no history of aspiration pneumonia in any study subject.
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Table 2. Comparisons of Diet, MDADI Scores, and PAS Scores by Treatment
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A total of 20 patients underwent MBS testing under the supervision of a speech-language pathologist. One patient in the CRT oropharyngeal group was unable to participate because of transportation issues. Each subject performed 2 swallows of 5, 10, and 20 mL of thin liquid barium in a progressive fashion, for a total of 6 swallows. All subjects in the CRT oropharyngeal group completed the entire MBS examination, whereas 2 patients in the SRT oropharyngeal group were unable to complete the full examination because of repeated aspiration that could not be cleared with compensatory maneuvers. When the PAS and MDADI scores were compared between groups, the CRT group demonstrated greater airway protection during swallowing and better swallowing-related quality of life (Table 2).
The association between the MDADI scores and the PAS scores was investigated to determine whether greater levels of laryngeal penetration and aspiration were associated with a reduction in swallowing-related quality of life. Using the Spearman correlation coefficient, no significant associations were found between the PAS scores and the MDADI scores for the 5-mL (P = .11), 10-mL (P = .22), or 20-mL (P = .16) liquid barium swallows. Although laryngeal penetration and aspiration are associated with potentially severe medical consequences (eg, aspiration pneumonia), this finding suggests that there may be little association between airway protection during swallowing and swallowing-related quality of life.
COMMENT
Dysphagia, which is a frequent consequence of head and neck cancer and its treatment, may result in poor health and reduced quality of life. To assess the impact of dysphagia in oropharygeal cancer survivors, we used 2 validated instruments, the MDADI and the PAS. The MDADI has been shown to be sensitive and reliable in regard to swallowing-related quality-of-life items in the head and neck cancer population.14 In our experience, the MDADI is a patient-friendly, easy-to-use questionnaire that usually takes less than 5 minutes to complete. Scaled 20 to 100, with 100 representing no dysphagia, the instrument is easy to score and interpret. Before the introduction of the MDADI, dysphagia was largely inferred by the consistency of diet. A recently published phase 3 trial of concurrent CRT for laryngeal cancer found that 16% of patients had dysphagia at 2 years on the basis of dietary consistency.16 In a previous study, we found that 35 (88%) of 40 patients with head and neck cancer were on either a normal or a soft solid diet after therapy; however, only 4 patients (10%) had a composite MDADI score of 90 or more.17 This finding suggests that scales of dietary consistency are poor indicators of dysphagia, because many patients continue to eat a normal diet, albeit with considerable difficulty. Therefore, the use of sensitive instruments such as the MDADI may improve our ability to recognize patients with dysphagia.
The MBS, which is performed under the supervision of a speech-language pathologist and a radiologist, is the radiographic tool most commonly used for the evaluation and treatment of dysphagia. It provides visualization of the structural movements of the upper aerodigestive tract during bolus passage18 and allows the identification and characterization of specific deviations in the timing and coordination of swallowing. Also, the speech-language pathologist can institute and evaluate compensatory swallowing strategies in real time during the examination. The clinical utility of the MBS in the evaluation and treatment of dysphagia is supported by a retrospective study of 608 MBS examinations performed on dysphagic patients.18 The MBS examination identified swallowing abnormalities in 90% of the patients and led to therapeutic recommendations in 50% of the patients.18
Although the clinical utility of the MBS in the evaluation of dysphagia is well accepted, the relationship of specific MBS findings to specific patient outcomes is less well established. The PAS was introduced in 1996 as a way to quantify the presence and degree of airway penetration (the bolus enters the vestibule but stays above the glottis) and aspiration (the bolus passes below the glottis) on MBS examination.15 The straightforward 8-point scale is reliable when performed by experienced swallowing clinicians and is valid because it is predictive of patient risk of aspiration pneumonia.19
On the basis of the PAS, the present study found better airway protection during swallowing among patients with oropharyngeal cancer who were treated with CRT than among patients with oropharyngeal cancer who were treated with SRT. Although the study predicted a greater risk of aspiration in the SRT oropharyngeal group, the clinical significance of this finding is uncertain, because no patient in the study suffered a documented case of aspiration pneumonia. Also, the PAS only quantifies 1 parameter of swallowing (airway protection), while failing to quantify other parameters, such as bolus preparation and transportation. Fewer than a third of dysphagic patients in a large, retrospective series had aspiration on MBS; however, close to 60% had other noted abnormalities.18 Therefore, further study is needed to determine whether treatment groups differ in other important swallowing parameters that can be measured by the MBS.
Although the PAS can help to quantify a given patient’s risk of aspiration pneumonia, it has not been shown to be predictive of other important patient outcomes such as dietary intake, nutritional status, and swallowing-related quality of life. Although the present study demonstrated better PAS and MDADI scores in the CRT group than in the SRT group, there was poor correlation between the PAS scores and the MDADI scores overall. This finding may indicate that laryngeal penetration and aspiration have little impact on swallowing-related quality of life. It is also consistent with anecdotal cases in which head and neck patients with no complaint of dysphagia were found to have significant laryngeal penetration and/or aspiration on barium swallow. Because subjective symptoms of dysphagia may not correlate with underlying swallowing dysfunction, our head and neck group routinely performs an MBS on all patients with advanced head and neck cancer, preferably before and after therapy, to ensure adequate airway protection and to identify patients who may benefit from further swallowing therapy. Also, measures of laryngeal penetration and aspiration only look at one aspect of swallowing and therefore fail to capture the overall physiologic functions of swallowing. Further study is needed to identify parameters of swallowing that are associated with important patient-based outcomes.
The assumption that organ preservation translates into functional preservation appears to be true in this small sample of patients with oropharyngeal carcinoma. These findings lend objective support to head and neck tumor boards that are increasingly recommending concurrent CRT as a first-line treatment for stage III and IV oropharyngeal carcinoma. Several study limitations, however, deserve mention. A cross-sectional study does not permit an assessment of differences in airway-protection mechanisms and swallowing-related quality of life between groups at baseline. A multi-institutional, longitudinal study of swallowing in patients with head and neck cancer would be helpful to determine if certain baseline characteristics predict better swallowing with one treatment as opposed to another. Also, the best estimate of functional outcomes requires an intent-to-treat analysis that includes surgical salvage patients within the chemotherapy cohort and adjuvant chemotherapy patients in the surgical cohort. It is possible that surgical and chemotherapeutic salvage results in worse functional outcome than dual-modality therapy alone. Fewer patients (3/11) in the oropharyngeal SRT group underwent free-flap reconstruction of the oropharynx than might be expected given current surgical practice; however, the patients in this cohort who underwent free flap reconstruction did not demonstrate a better swallowing outcome than those who underwent primary reconstruction alone. Also, the majority (8/11) of the oropharyngeal surgery patients underwent mandibulotomy and/or pharyngotomy, which might compromise function to a greater degree than transoral approaches (eg, laser). Finally, the majority of patients in the CRT group received high-dose cisplatin and fluorouracil and standard radiotherapy therapy instead of the less-toxic low-dose cisplatin and paclitaxel regimen and intensity-modulated radiotherapy that is currently favored at our institution. Therefore, the functional outcomes of the patients whom we are currently treating may ultimately be vastly different from those of the patients whom we have treated in the past.
CONCLUSIONS
Dysphagia is a frequent sequela of head and neck cancer and its treatment. Chemoradiotherapy appears to result in better airway protection during swallowing and in better swallowing-related quality of life than SRT for patients with oropharyngeal cancer. Further characterization of swallowing differences among head and neck cancer treatment groups will require additional research to identify and validate critical parameters of swallowing, other than airway-protection mechanisms, that are reliable and predictive of important patient-based outcomes.
AUTHOR INFORMATION
Correspondence: M. Boyd Gillespie, MD, Department of Otolaryngology–Head and Neck Surgery, Medical University of South Carolina, 135 Rutledge Ave, Charleston, SC 29425 (gillesmb{at}musc.edu).
Submitted for Publication: August 31, 2004; accepted March 22, 2005.
Previous Presentation: This study was presented at the Sixth International Head and Neck Conference; August 10, 2004; Washington, DC.
Financial Disclosure: None.
Author Affiliations: Department of Otolaryngology–Head and Neck Surgery, Medical University of South Carolina, Charleston.
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