Functional Outcome Swallowing Scale (FOSS) score 0 to 5 distribution as frequency and percentage.
Best swallowing scores (BSS) based on a Functional Outcome Swallowing Scale (FOSS) score of 0 to 5 were broken down by the 5 general resection and reconstruction sites. A, Cervical esophagus with or without the hypopharynx; B, hypopharynx (>60% resected) with or without the oropharynx/nasopharynx; C, partial laryngopharyngectomy (partial larynx with >60% resection of the hypopharynx); D, base of tongue with supraglottic laryngectomy; E, base of tongue with either additional resection of the hypopharynx or the oropharynx without supraglottic laryngectomy.
The probability of achieving best swallowing over time. The solid line represents the probability and dotted lines, 95% confidence intervals.
Sumer BD, Gastman BR, Nussenbaum B, Gao F, Haughey BH. Microvascular Flap Reconstruction of Major Pharyngeal Resections With the Intent of Laryngeal Preservation. Arch Otolaryngol Head Neck Surg. 2009;135(8):801-806. doi:10.1001/archoto.2009.84
To determine the functional outcome in patients undergoing pharyngeal reconstruction with free tissue transfer with the intent of functional laryngeal preservation.
Retrospective medical record review.
Academic tertiary care hospital.
The study population comprised 45 patients who underwent a major pharyngeal resection with or without a partial laryngeal resection (2 patients died perioperatively, leaving 43 to evaluate). The majority (n = 35 [81%]) had advanced (T3 or T4) primary tumors at presentation and underwent subsequent reconstruction using free tissue transfer at a tertiary care hospital.
Main Outcome Measures
The rate of functional larynx preservation, best swallow score based on the Functional Outcome Swallowing Scale, and need for tracheostomy. Thirteen independent variables relevant to function and 6 postoperative outcome variables were studied following treatment, and their correlation with laryngeal function was determined.
Of the 43 patients, 35 (81%) had T3 (n = 9) or T4 (n = 26) squamous cell carcinoma at presentation. There was 100% flap survival. Thirty-one patients (72%) tolerated an oral diet, with 24 (56%) achieving an exclusively oral diet. Only a history of gastroesophageal reflux disease had a statistically significant correlation with poor swallowing; having had a cranial nerve removed did not achieve statistical significance (P = .06). The majority of patients had their best swallow by 10 months. Of the 43 patients, 42 (97%) achieved native laryngeal speech and 36 (84%) were decannulated. The need for a tracheostomy did not correlate with any of the preoperative independent variables.
Free tissue transfer allows for successful reconstruction of complex pharyngeal defects that functionally threaten the remaining larynx. In properly selected patients, functional laryngeal preservation, decannulation, and use of laryngeal speech can be reliably achieved. Excellent swallowing function can less reliably be predicted.
Laryngeal organ preservation is increasingly becoming a realistic goal in locally advanced cancers of the upper aerodigestive tract. Recent efforts in this regard have centered on chemoradiation. In addition, however, surgical options for larynx preservation exist. Less-advanced tumors can often be resected and reconstructed primarily with open partial laryngectomy procedures, preserving laryngeal function. Transoral laser surgery is also an excellent surgical option for many cancers of the larynx, oropharynx, and hypopharynx, allowing organ preservation and the full range of postoperative or salvage options. Resection of locally advanced squamous cell carcinoma of the pharynx that oncologically or functionally involves the larynx, however, often adversely affects laryngeal function.
Advances in primary site reconstruction with the use of local and pedicled flaps have allowed for increasingly larger pharyngeal resections while anatomically preserving the larynx.1 Larger lesions that oncologically or functionally affect the larynx, however, could necessitate a total laryngectomy owing to concerns with aspiration.1 Thus, even when anatomic preservation of the larynx is possible oncologically, functionally it cannot be preserved.2,3 The ability to contour pedicled flaps for bulk such as in base of tongue reconstructions and for pliability in the oropharyngeal wall, palatal and hypopharyngeal reconstruction has been found to be limited.4
As reconstructive options have expanded with the use of free tissue transfer, the goal of preserving laryngopharyngeal function after major open pharyngectomies has become more realistic. Studies assessing functional preservation of the larynx after resection of advanced lesions of the pharynx and reconstruction with free tissue transfer, however, are lacking. Therefore, the hypothesis that the use of free tissue transfer techniques allows for functional (swallowing, airway protection, laryngeal speech) laryngeal preservation after open resection of locally advanced oropharyngeal and/or hypopharyngeal cancers was tested.
This study was approved by the Washington University Human Studies Committee, St Louis, Missouri. Forty-five patients meeting the inclusion criteria who were treated between October 1989 and November 2002 at Barnes Jewish Hospital in St Louis were identified (2 patients died perioperatively, leaving 43 to evaluate). The surgical entry criterion was to have undergone a larynx-sparing extended pharyngectomy reconstructed using free tissue transfer. Of the 43 patients evaluated, 26 (60%) had T4 and 35 (81%) had either T3 or T4 disease. There were 5 categories of resection sites: cervical esophagus with or without the hypopharynx (site A), hypopharynx with or without oropharynx/nasopharynx (site B), partial laryngopharyngectomy (site C), base of tongue with supraglottic laryngectomy (site D), and base of tongue with either additional resection of hypopharynx or oropharynx without a supraglottic laryngectomy (site E). Regarding sites D and E, it is our policy5 at Washington University to perform free flap reconstruction of base of tongue defects if two-thirds or more of that structure has been resected, and that policy was followed in the patients described herein.
Independent variables relevant to demographics, functional outcomes, and postoperative morbidity included age, sex, stage, site and type of resection, race, history of gastroesophageal reflux disease (GERD), intentional cranial nerve removal for tumor clearance, concurrent neck dissection(s), preoperative or postoperative radiation (and chemotherapy), donor tissue, and presence of a postoperative fistula.
The following 6 outcome variables were measured following treatment: flap survival, the Functional Outcome Swallowing Scale (FOSS) score, rate of decannulation, method of vocalization, documented aspiration, and the presence of major complications. Aspiration was documented either by fiberoptic examination while swallowing or with a modified barium swallow study. Major complications were defined as those that required reoperation or a prolongation of hospitalization. Swallowing was assessed using the FOSS.6 The best swallowing score (BSS) was defined as the best swallow based on the FOSS that they achieved postoperatively. Postoperative voice was divided into 2 categories: the native larynx with understandable speech or nonlaryngeal speech.
Statistical analyses were performed using SAS software (version 9; SAS Institute Inc, Cary, North Carolina). Six outcome variables were measured following treatment. However, because the majority of the outcomes had relatively homogeneous results, the data analysis of this study was mainly focused on the outcome to achieve the BSS. The probability of achieving a BSS over time was calculated by the Kaplan-Meier method with 95% Greenwood confidence intervals. The association between achieving a BSS of 0 to 3 vs a BSS of 4 to 5 and each of the independent variables was assessed by Fisher exact tests and described using odds ratios. Because of the relatively small sample size, all the data analyses were descriptive in nature, and no multivariate analysis was performed. All statistical tests were 2-sided, and P ≤ .05 was considered statistically significant.
The 45 patients in this study included 32 men and 13 women. Two patients died perioperatively after discharge from the hospital, one from a major gastrointestinal tract bleed and the other from tracheostomy tube dislodgement, leaving 43 patients to evaluate. The mean (range) age was 59.2 (39-82) years. All patients were treated for head and neck squamous cell carcinomas; 26 patients had T4 lesions (60%), 9 patients had T3 lesions (21%), and the 8 remaining patients had T2 lesions at the time of surgery. Thirty-one patients had overall stage 4 disease (69%) and 10 had stage 3 disease (22%).
There was 100% flap survival. Flaps included the radial forearm (n = 35) and jejunum flap (n = 8). Ten of the forearm flaps were made sensate with a direct nerve anastomosis.
Figure 1 illustrates the FOSS score distribution. Of 43 patients, 24 (56%) did not require a feeding tube and another 7 (16%) achieved the ability to have some of their diet through an oral route. Of the 14 independent variables, only a history of GERD had a statistically significant correlation with poor swallowing (P = .04), with an odds ratio of 6.54. Having had any cranial nerve removed did not achieve statistical significance (P = .06) in terms of poor swallowing (Table 1). Sites that involved partial resection of the supraglottis or larynx (C + D) had a significantly worse swallowing outcome than sites that did not involve resection of the larynx (sites A + B + E) (Table 1). The number of patients requiring a permanent feeding tube by site were 2 each for sites A and B and 5 each for sites C, D, and E.
Figure 2 illustrates the BSS for the 5 general resection sites. Although the individual resection site numbers were small, the extended base of tongue resection without supraglottic laryngectomy did not achieve statistical significance as having a better BSS vs the rest of the groups (P = .08) despite being the slowest group to achieve BSS (Table 2). However, in absolute terms, the site with the highest proportion of patients with superior FOSS scores was site B (hypopharynx with or without oropharynx/nasopharynx; Table 1), with 4 of 5 patients (80%) achieving a FOSS score of 0 to 3. Neither preoperative nor postoperative radiation nor chemoradiotherapy had a significant impact on swallowing (P = .76 and P = .33, respectively). The use of a sensate flap did not statistically significantly improve swallowing function.
Figure 3 demonstrates the time to reach the patient's BSS. Most patients stabilized their best swallow by 10 months. Table 2 illustrates the time to BSS based on resection and reconstruction site. The extended base of tongue resection without supraglottic laryngectomy had the best swallow results but required the longest time to reach this time point. This group also demonstrated the most variability in time to BSS. For patients who received postoperative radiotherapy, the mean time to BSS was 7.8 months vs 4.5 months for patients who did not receive postoperative radiation.
Of the 43 patients, 42 (97%) achieved native laryngeal speech, and 1 patient went on to have a total laryngectomy for severe dysphagia. Thirty-six patients (84%) were successfully decannulated. None of the perioperative variables correlated with the need for a long-term tracheostomy.
A total of 13 major complications occurred in the 45 patients. These complications included 3 fistulas, 2 hematomas, 2 wound infections, and 1 patient with a postoperative cardiac arrhythmia requiring pacemaker placement. One patient had a stroke. One patient required a subsequent pectoralis flap owing to native neck skin breakdown. One patient had a mild gastrointestinal tract bleed. There were 2 perioperative deaths, with one from a massive gastrointestinal tract bleed and the other from a dislodged tracheostomy device at a rehabilitation facility.
Resection of advanced pharyngeal lesions with laryngeal preservation has historically been limited by the ability to functionally reconstruct the resultant defect and maintain airway protection. The introduction of local reconstruction techniques and the use of regional pedicled flaps allowed resection of these lesions while maintaining separation of the aerodigestive tract from the neck. Schuller et al7 reported using the pectoralis major flap to reconstruct partial laryngopharyngeal defects. In this series, only 1 of 21 patients had to be converted to a total laryngectomy owing to aspiration, and 31 of 43 patients (72%) had some oral intake.
Even with local and regional flap reconstruction, however, resection of locally advanced pharyngeal lesions can lead to profound functional deficits involving the larynx including aspiration, poor airway caliber, difficulty swallowing due to laryngeal fixation, and poor voice. To address these functional defects of the larynx, adjunctive total laryngectomy with partial pharyngectomy has been a surgical standard treatment for extensive cancers involving the pharynx with or without extension into adjacent structures. Advantages associated with a total laryngectomy include lack of aspiration and reliable recovery of swallowing after surgery. With the introduction of prosthetic tracheoesophageal speech, postlaryngectomy voice restoration has been significantly improved even in patients who had extended laryngectomies with a free flap reconstruction.8 Disadvantages of total laryngectomy include the psychosocial stigmata, cosmetic deformity, loss of the sense of smell, and general patient aversion to having a tracheostoma.
The reliability and importance of free tissue transfer in oncologic surgical reconstruction has been well characterized in the head and neck.9 Free tissue transfer has become the reconstruction method of choice for treating defects of the hypopharynx and oropharynx.10 Hagen11 described 30 patients who underwent free flap reconstruction of partial laryngopharyngectomy defects, all of whom had at least part of their larynx preserved. Of these patients, only 1 required a subsequent laryngectomy, 25 were decannulated, and 25 were reported as having a usable to excellent voice.
Weber et al12 reported 27 cases of near total or total glossectomy in which the larynx was preserved and long-term oral feeding was achieved in 44% of patients. Fujimoto et al13 recently reported that 85.5% of 62 patients who underwent resections involving the bilateral suprahyoid muscles or greater than 50% of the base of tongue had some oral intake. Of these patients, 52 underwent reconstruction with free flaps vs 10 who underwent reconstruction with pedicled flaps, with the free flap group achieving better swallowing than the pedicled flap group.
The patients in the present study underwent extensive pharyngeal, pharyngoesophageal, and laryngopharyngeal resections. These are sites likely to adversely affect swallowing function, but the patients still had good laryngeal functional outcomes. The larynx preservation in 42 of 43 patients (97%) compares favorably with nonsurgical methods of anatomic laryngeal preservation.14 In addition, the majority of patients went on to have at least some oral intake, with 24 (56%) having a FOSS of 0 or 1 and an exclusively oral diet. Also, 36 patients (84%) were decannulated. In contrast, a prior study showed that patients undergoing an extended supraglottic laryngectomy that included a significant tongue base resection but without flap reconstruction had a 21% rate of being converted to a total laryngectomy because of swallowing and aspiration problems and only a 50% rate of decannulation.3 These results indicate that reconstructive techniques with free tissue transfer can functionally improve patients' ability to swallow and protect their airway. The majority of patients achieved their BSS by 10 months. This is important prognostic information, emphasizing to the patient and caregivers that the postoperative swallowing rehabilitation requires an extended period. Postoperative radiation delayed the average time to BSS from 4.5 to 7.8 months, highlighting the acute and subacute adverse effects radiation can have on swallowing.
When the resection included portions of the larynx as with a partial laryngopharyngectomy, or the supraglottis, swallowing outcomes were, not surprisingly, worse than when the resection was confined to the pharynx or hypopharynx. Because the larynx and supraglottis play an essential role in the prevention of aspiration, it is not surprising that these sites were detrimentally affected, as judged by FOSS scores. Therefore, resections that will probably involve these anatomic sites need to be approached with caution. This study also demonstrates the importance of GERD for recovery of swallowing. The impact of GERD may be due to delayed wound healing, abnormal motility of the cricopharyngeus or esophagus, or effects on the physiologic function of reconstructed anatomy.15 This impact and the pathophysiologic mechanisms of GERD affecting the recovery of swallowing after undergoing major reconstructive surgery of the upper aerodigestive tract needs further study. The emphasis the FOSS scale places on aspiration also may have led to the observed correlation between GERD and poor swallowing.
In conclusion, free flap reconstruction of complex extended pharyngeal defects reliably allows avoidance of total laryngectomy. In properly selected patients, those seeking a surgical approach to functional laryngeal preservation that are not candidates for transoral laser microsurgical resection can expect excellent functional recovery regarding decannulation and laryngeal speech. Prediction of swallowing outcomes is less reliable but may be better if the defect does not involve resection of a portion of the larynx. This alternative may be an important option for patients, as it is becoming increasingly clear that chemoradiation may offer anatomic organ salvage without necessarily functional preservation.16 Future analysis of larger groups of patients in a multi-institutional study may delineate who will have an excellent vs a poor functional outcome using these reconstructive options.
Correspondence: Bruce H. Haughey, MBChB, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, 660 S Euclid Ave, Campus Box 8115, St Louis, MO 63110 (firstname.lastname@example.org).
Submitted for Publication: July 10, 2008; final revision received December 12, 2008; accepted December 22, 2008.
Author Contributions: Dr Haughey had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Sumer, Gastman, Nussenbaum, and Haughey. Acquisition of data: Gastman, Nussenbaum, and Haughey. Analysis and interpretation of data: Sumer, Gastman, Nussenbaum, Gao, and Haughey. Drafting of the manuscript: Sumer, Gastman, Nussenbaum, and Haughey. Critical revision of the manuscript for important intellectual content: Sumer, Gastman, Nussenbaum, Gao, and Haughey. Statistical analysis: Gao. Obtained funding: Haughey. Administrative, technical, and material support: Sumer, Gastman, and Haughey. Study supervision: Nussenbaum and Haughey.
Financial Disclosure: None reported.
Previous Presentation: This work was presented at the Sixth International Conference on Head and Neck Cancer; August 8, 2004; Washington, DC.