Total Glossectomy With Laryngeal Preservation and Free Flap Reconstruction: Objective Functional Outcomes and Systematic Review of the Literature

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1 The Laryngoscope VC 2012 The American Laryngological, Rhinological and Otological Society, Inc. Total Glossectomy With Laryngeal Preservation and Free Flap Reconstruction: Objective Functional Outcomes and Systematic Review of the Literature Peter T. Dziegielewski, MD; Michael L. Ho, BSc; Jana Rieger, PhD; Prabhjyot Singh, MD; Morgan Langille, MD; Jeffrey R. Harris, MD, FRCS(C); Hadi Seikaly, MD, FRCS(C) Objective: Advanced tongue cancer is a devastating diagnosis with potential for significant morbidity after treatment. This is especially true for patients undergoing total glossectomy with laryngeal preservation (TGLP), free flap reconstruction and adjuvant radiotherapy. The goals of this study were to: 1) determine long-term objective functional and quality of life outcomes, 2) investigate the influence of rehabilitation on functional recovery and 3) determine swallowing ability in patients with TGLP. Study Design: Prospective cohort study and systematic review of the literature. Methods: Functional outcomes data were collected from Outcomes were measured pre- and 12 months post-surgery and included: gastrostomy-tube (G-Tube) rates, swallowing transit times on video fluoroscopic swallowing studies, speech intelligibility and EORTC-H&N 35 quality of life scores. A systematic review of the literature was conducted to determine comprehensive long term G-Tube rates. Results: Twelve patients were included and eight were still living at 12 months post-surgery. Fifty percent of patients in this study and 24% with systematic review used G-Tubes at 1 year post-surgery. Patients who could swallow did not aspirate, but more than doubled swallowing transit times. Spoken sentence intelligibility averaged 66% and mean quality of life scores improved 8.9 points 12 months post-surgery. Patients who attended >80% of swallowing and speech rehabilitation sessions demonstrated superior swallowing and speech functional outcomes. Conclusions: Although a potentially morbid treatment, TGLP and free flap reconstruction can provide good swallowing and speech outcomes as well as meaningful long-term quality of life. Regular attendance of rehabilitation sessions is imperative to optimize functional outcomes. Key Words: Total glossectomy, total glossectomy with laryngeal preservation, anterolateral thigh free flap, functional outcomes, quality of life, oral cancer, swallowing rehabilitation. Level of Evidence: 4 Laryngoscope, 123: , 2013 INTRODUCTION Historically, patients with advanced tongue cancers were treated with a primary aim of preserving life. While aggressive resections improved survival, patients were rendered orally disabled. Once effortless, functions such as speech, chewing, and swallowing became distant From the Department of Surgery, Division of Otolaryngology Head and Neck Surgery, (P.T.D., P.S., M.L., H.S.) University of Alberta, Edmonton, AB, Canada; Faculty of Medicine and Dentistry, (M.L.H.) University of Alberta, Edmonton, AB, Canada, Institute for Reconstructive Sciences in Medicine, (J.R.) Caritas Health Group, Edmonton, AB, Canada. Editor s Note: This Manuscript was accepted for publication May 21, This study was presented at the AHNS 2010 Research Workshop on Biology, Prevention & Treatment of Head & Neck Cancer, on October 28 30, The authors have no funding, financial relationships, or conflicts of interest to disclose. Ethics approval was granted by the University of Alberta s Health Research Ethics Board. Informed consent was obtained from each patient for data usage. Send correspondence to Hadi Seikaly, MD, FRCSC, 1E4.29 Walter C Mackenzie Center, Street NW, Edmonton, Alberta, T6G 2B7 Canada. hadi.seikaly@albertahealthservices.ca DOI: /lary memories. Eventually patients and their physicians begged the question: is the extension of life, actually worth living? Consequently a modern paradigm of head and neck surgery arose, where surgeons strive to balance survival, function, and quality of life. 1,2 In the era of organ preservation, this balance has shifted towards decreasing morbidity. 3 5 However, many institutions are finding unacceptable compromises of survival with organ preservation. 3,6 Emerging evidence suggests that primary surgery with postoperative radiotherapy (RT) may provide an improved balance for advanced oral cancer. 1,3,7 While this has been shown for lesions requiring hemiglossectomy, there is a paucity of data for lesions necessitating total glossectomy. 4,8 Moreover, the debate of whether laryngectomy should be included to improve postoperative function ensues Thus, the question still remains: how does total glossectomy with laryngeal preservation (TGLP) fit in with modern head and neck oncology? The purpose of this study was to examine prospectively collected objective swallowing, speech, and quality of life data in patients undergoing TGLP, free flap reconstruction, and postoperative RT, and to determine the 140

2 influence of rehabilitation on those outcomes. The secondary goal of the study was to conduct a systematic review of the literature for similar patients and to combine data for swallowing ability in this cohort. PATIENTS AND METHODS Ethics approval was granted by the University of Alberta Health Research Ethics Board (HREB) committee. This study was conducted at a tertiary care academic referral center. Patient Selection Inclusion criteria Cancer of the tongue: oral tongue, base of tongue or both Primary treatment: TGLP and free flap reconstruction Adjuvant treatment: RT 6 Chemotherapy Exclusion criteria Previous RT to the head and neck Previous head and neck malignancy Resections extending outside the tongue base in the oropharynx Research Questions What proportion of patients will achieve adequate swallowing function to sustain caloric needs without the aid of a gastrostomy-tube (G-Tube)? If swallowing is achieved, how efficient and safe is it? How intelligible is speech of these patients? How compromised is quality of life in this group? What effect does attendance of speech and swallowing rehabilitation sessions have on functional recovery? What is the overall literature-combined rate of G-tube use in this population? Treatment Patients with head and neck cancers at the University of Alberta underwent a metastatic workup, including full body positron emission tomography-computed tomography (PET-CT) and panendoscopy, prior to establishing a treatment regime. Those who chose primary surgery were booked for a single-staged procedure including tumor extirpation and defect reconstruction. Preoperatively all patients were evaluated in a preadmission clinic by an intensive care unit physician, an anesthetist as well as an internist. Those with significant pulmonary disease (e.g., chronic obstructive pulmonary disease), on home oxygen, or with poor functional capacity underwent pulmonary function testing at the discretion of the medical team in the clinic. Results were used to optimize pulmonary function perioperatively. Resection. Surgery included a perioperative tracheostomy, which was reversed and sutured closed prior to discharge or after RT, 14 bilateral neck dissections, lip-splitting mandibulotomy approach 15 and TGLP. Total glossectomy was defined as resection of 100% of the tongue (tip to vallecular floor) as well as >75% of the floor of mouth. Two patients underwent a hemimandibulectomy as part of a composite resection, which was reconstructed with a fibular free flap (FF). Flap reinnervation was performed when possible. 16 The superior laryngeal nerve was identified and preserved. Laryngeal suspension was performed for all resections. 13,17 21 Tongue reconstruction. A neo tongue was constructed from an anterolateral thigh free flap (ALTF). The flap was raised with substantial subcutaneous bulk, including fat and vastus lateralis muscle. 12,13,22 Adjuvant treatment. RT was initiated 4 6 weeks postoperatively, with patients receiving fractions of Gy of conventional RT five times per week for 6 weeks. Four patients also received concomitant chemotherapy consisting of a standard cis-platin-based regimen. Rehabilitation. Patients were enrolled in postoperative speech and swallowing rehabilitation with an advanced practitioner. Therapy was patient-specific and included private and group sessions on a weekly basis until adequate function was achieved or the patient self-discontinued sessions. Maintenance therapy was conducted on a monthly basis. Data Collection Cases of advanced tongue carcinoma from January 2000 to September 2010 were assessed in a prospective functional outcomes program. 23 Data collection included patient age, gender, TNM staging, 24 diagnosis, site of lesion, percent of oral tongue and tongue base excised, type of free flap used, adjuvant treatment, attendance of speech and swallowing rehabilitation sessions, as well as quality-of-life questionnaire and functional outcomes data. Data on postoperative complications was also collected including: timing, type, and treatment of complication. Functional Outcome Measures: Swallowing and speech functions were measured and prospectively recorded preoperatively and 12 months postoperatively at the Head and Neck Surgery Functional Assessment Laboratory at the Institute for Reconstructive Sciences in Medicine. Furthermore, patients completed quality of life questionnaires during these visits. Swallowing. Patients were nasogastric tube-fed postoperatively. Once their tracheostomy had been reversed, they underwent swallowing evaluation by a speech pathologist. A videofluoroscopic swallowing study (VFSS) was used to evaluate readiness for oral intake. Patients who could maintain >75% of their diet orally, had the feeding tube discontinued. Those who failed the swallowing test were given 1 week of intensive swallowing therapy and were reevaluated. If they did not improve a G-Tube was installed. Moreover, at any point postoperatively if the patient could not maintain adequate oral nutrition, a G- Tube was instituted. Swallowing was assessed in terms of ability, safety, and efficiency. Swallowing ability was the primary outcome and was defined as complete independence from a G-Tube to maintain daily caloric requirements. Swallowing safety and efficiency were evaluated via VFSS, completed in the presence of a radiologist within the diagnostic imaging department. Pudding mixed with barium paste (Esobar, barium sulfate cream, Therapex) in a 3:1 ratio was presented as a calibrated bolus on a teaspoon to the patients, who cleared the material from the spoon and swallowed it. Two trials of the swallow were made and the video was saved to disc. The clearest and most complete of the 2 VFSS was analyzed in frame-by-frame slow motion using the Digital Swallowing Workstation (Model 7200, KayPentax, Lincoln Park, NJ) Swallowing safety was determined using a Penetration-Aspiration Scale. 28 This eight-level scale was simplified to a two-point clinically applicable system: 0 ¼ level 1 5 (no penetration of the glottis) and 1 ¼ Levels 6 8 (penetration of the glottis). Swallowing efficiency was defined as the time it took to complete one swallow (i.e., swallowing transit time). This was measured on the VFSS as the time from the start of the swallow to the time of the radio-opaque bolus passing the cricopharyngeus muscle. To establish interrater reliability, 50% of the VFSS films were randomly chosen for reanalysis

3 TABLE I. Patient Characteristics. Characteristic N (%) Patients 12 (100) Male 10 (83) Female 2 (17) Mean Age (y) 64.3 SCC 12 (100) T-Stage T3 9 (75) T4 3 (25) AJCC Stage IVa 12 (100) Reconstruction ALTF 10 (83) ALTFþFFF 2 (17) Abbreviations: N, number of patients; y, years; SCC, squamous cell carcinoma; ALTF, anterolateral thigh free-flap; FFF, fibular free flap; AJCC, American Joint Committee on Cancer. Speech. Naïve listeners assessments of speech intelligibility were completed using Computerized Assessment of Intelligibility of Dysarthric Speech (CAIDS; Pro-Ed, Austin, TX). 30 Patients read a standardized passage, which was then recorded and played to naive listeners, who were neither a trained speech pathologist nor familiar with the patient. The listeners interpreted the recording, which was scored for single word and sentence intelligibility. To confirm interrater reliability, all recordings were reanalyzed by a second naive listener. 30 Quality of Life. Patients were administered questions of the European Organization for Research and Treatment of Cancer Head & Neck 35 Quality of Life Questionnaire (EORTC H&N 35). 31 This widely used and validated head and neck cancer-specific quality of life questionnaire is self-administered without the aid of a health care professional or questionnaire administrator. Scores are scaled to a minimal score of 30 and maximum of 100. A higher score indicates a worse quality of life. Systematic Review Literature review was conducted to determine G-Tube rates at 6 12 and 12 months post-surgery for patients undergoing primary TGLP and free flap reconstruction with adjuvant RT. Three independent reviewers identified relevant articles, using Pubmed, Medline, Embase, and Scopus. Abstracts were reviewed for appropriate content. If the abstract mentioned total glossectomy, major glossectomy, or extensive glossectomy, the article was pulled and fully reviewed. Any relevant articles referenced within the pulled article were also reviewed. Selected articles were reviewed by the authors to ensure patients met this study s criteria. Search strategies included: total glossectomy, complete glossectomy, extensive glossectomy, total tongue removal, total tongue resection, glossectomy, advanced oral cancer AND surgery, and advanced oral cancer AND glossectomy. The search included all literature published from 1809 to Mar 1, G Tube rates (per study and overall) were calculated as total number of patients with a G-Tube/total number of patients at that time point. Data were analyzed using SPSS Statistics 17.0 (2008, Chicago, IL). RESULTS One hundred eighty-nine patients with advanced tongue cancer were enrolled in the functional outcomes program. Twenty-one patients met study inclusion criteria. Two were excluded due to previous tongue RT and seven due to the resection extending into the tonsils, soft palate, or posterior pharyngeal wall. Both patients who had previous RT did not attend any functional outcomes sessions. All margins were clear by at least 5 mm. One patient died 3 weeks postoperatively of a pulmomary embolus and three others died of local recurrence 4 6 months post-surgery. No patients were lost to followup. Table I shows patient characteristics. Three patients experienced postoperative complications. Two surgical complications were encountered in separate patients: one neck hematoma, requiring evacuation on postoperative day 1 and venous congestion in a flap requiring microvascular anastamotic revision on postoperative day 2. The flap was salvaged with no further sequalae. The only medical complication encountered was aspiration pneumonia. Both instances occurred 12 months postoperatively, required hospital admission with intravenous antibiotic treatment and resulted in hospital discharge within 7 days. Both patients were G-Tube dependent and had attempted to resume oral diets without the supervision of a medical professional. One of these patients had the neck hematoma mentioned above. G-Tube rates are illustrated in Table II. Patients able to swallow were on thickened liquid diets. Of the four patients reliant on G-Tubes at 12 months, two tolerated an oral diet, but chose to continue with a G-Tube for convenience. Both could consume >90% of their caloric needs orally, but stated that it was too time consuming to rely on oral feeds. The other one could not safely swallow following RT and required a G-Tube. Table II also demonstrates results of the systematic review. Seventy-three potential studies were identified. Sixtyseven were excluded due to incomplete/unclear data and six remained. Patients who could complete a VFSS demonstrated swallowing safety scores and swallowing transit times as per Table III. All patients alive at 6 and 12 months attended speech testing with results as per Table IV. Overall 10 TABLE II. G-Tube Rates as Per Systematic Review of the Literature. Author Year N Reconstruction G-Tube rate, % 6-12 mos post-op 12 mos post-op Dziegielewski ALTF Yun ALTF, RA 0 0 Van Lierop RFFF, RA 0 Chien ALTF, FOCF, RFFF 20 Yu ALTF 75 Davidson RFFF 0 Urken RFFFþICF 0 Overall Rate: Abbreviations: N, number of patients; G-Tube, gastrostomy tube; mos, months; post-op, postoperative; ALTF, anterolateral thigh free flap; RA, rectus abdominus; RFFF, radial forearm free flap; FOCF, fibular osteocutaneous free flap; ICF, iliac crest free flap. 142

4 Time TABLE III. Perioperative Swallowing Efficiency. N Mean penetration-aspiration score (SD, range) Mean swallowing transit time, sec (SD, range) Pre-op (0.4, 0-1) 1.21 (0.8, ) 12 mos post-op (0.4,0-1) 7.15 (3.4, ) Change (0.0,0) þ5.94 (2.92, ) Abbreviations: N, number of patients; SD, standard deviation; sec, seconds; Pre-op, preoperative; mos, months; post-op, postoperative. patients were tracheostomy-free at initial hospital discharge. All but one had their tracheostomy reversed by 12 months post-surgery. This patient could phonate, but her speech could barely be understood preoperatively and not at all postoperatively. Quality of life scores are summarized in Table V. Of the eight patients living at 6 and 12 months post-surgery, all attended 100% of speech and swallowing rehabilitation sessions for the first 3 postoperative months. Four patients attended <25% of the remaining and were reliant on G-Tubes, while the remainder achieved oral diets. It is worth noting that all four patients with poor attendance lived >100km from the hospital. DISCUSSION Many authors have questioned the validity of total glossectomy without laryngectomy for fear of aspiration and poor speech. 32 With the development of free flaps, functional reconstructions have become increasingly possible. However, many centers continue to avoid such heroic treatments without analyzing functional outcomes. 3 All patients of this study had advanced SCC of the tongue ablated via TGLP with negative margins. During reconstruction, several key factors were followed to promote functional recovery: laryngeal suspension, 13,17 21 preserving the superior laryngeal nerve, 4 large flap volume and shape, 13,21 and utilizing sensate flaps. 16,33 The ALTF was chosen as it provides substantial bulk and width and allows for sensory neurotization. The flap was shaped with a central mound that was approximately 1 = 3 larger than desired to allow for tissue atrophy and fibrosis post-rt. The goal was to create a protuberant neo tongue that provided palate-glossal contact during phonation and deglutition. 13,20,21 This allowed bolus propulsion by closure of the mandible to initiate the pharyngeal phase of swallowing. Other authors have described similar reconstructions with the rectus abdominus free flap, as it holds similar properties to the ALTF. 8,11,13,21 Other emerging techniques, involve functional muscle transfer with motor neurotization, which can lead to increased neo tongue mobility and maintained bulk. 13 Complications were minimal in this study and similar to other reported rates. 8,11,13,21 No instances of short term pneumonia were identified and only two cases of significant aspiration pneumonia were found at 1 year post-surgery. Patients who experienced this complication were previously deemed unsafe to swallow, but had decided to proceed with an oral diet. Keeping aspiration pneumonia rates low is likely aided by regular functional assessments, which aid in patient education and rehabilitation. 29,33,35 At 1 year post-surgery seven (87.5%) patients consumed oral diets. All patients able to swallow did not aspirate. However, three patients spent more than 5 seconds per swallow, and thus, opted for G-Tubes. A normal swallowing transit time is considered < 2 seconds. By more than doubling this time, some patients spent a significant amount of their day eating. As such, they may have felt that quality of life was improved with G-Tubes. With a lack of functional outcomes standardization, it is challenging to compare results of the literature. 29,34,35 Therefore, the simplest comparable outcome was chosen: G-Tube rate. Systematic review showed that most reconstructions were carried out with ALTF or rectus abdominus flaps. Most authors avoided RFFF due to lack of tissue bulk. 22 Studies specifically reporting follow-up time found that at 12 months follow-up, a quarter of patients with TGLP, free flap reconstruction, and adjuvant RT succeed in avoiding G-Tubes by maintaining adequate oral nutrition. Other studies, which did not specify follow-up times, demonstrated 30 85% G- Tube independence rates. 36,37 While these results are encouraging, one must keep in mind that numbers are low and many institutions may not report negative results. Preoperative single word and sentence intelligibility were impaired and highly varied. All mean post-treatment scores decreased, especially those for single word intelligibility, which dropped on the order of 30%. Although testing single word intelligibility may be a more sensitive test, it is not as clinically important as mean sentence intelligibility, which allows the listener to incorporate contextual clues to fill in gaps. These scores only dropped by 15%, and show that despite total TABLE IV. Perioperative Speech Intelligibility by Speech Therapy Attendance. Mean single word intelligibility, % (SD, range) Mean sentence intelligibility, % (SD, range) Time N <25% Attendance >80% Attendance All <25% Attendance >80% Attendance All Pre-op 8 71 (44, 6-96) 87 (11, 76-96) 78 (31, 6-96) 74 (45, 7-100) 84 (32, ) 78 (36, 7-100) 12 mos post-op 8 31 (30, 0-68) 57 (15, 38-70) 44 (26, 0-70) 53 (41, 0-98) 79 (9, 67-85) 66 (31, 0-85) Change 0 40 (29, ) 30 (5, ) 35 (20, ) 21 (19, ) 4 (24, ) 12 (21, ) Abbreviations: N, number of patients; SD, standard deviation; sec, seconds; Pre-op, pre-operative; mos, months; post-op, post-operative. 143

5 TABLE V. Peri-operative quality of life scores. results may over estimate function in the salvage total glossectomy scenario Time N Mean EORTC H&N 35 score (SD, range) Pre-op (8.7, 49-72) 12 mos post-op (12.8, 41-78) Change (15.7, ) Abbreviations: N, number of patients; EORTC, European Organization for Research and Treatment of Cancer; SD, standard deviation; Pre-op, preoperative; mos, months; post-op, postoperative. glossectomy, patients could retain good intelligibility. While other studies have shown that extensive glossectomy patients fail to achieve acceptable speech, 35,38 that is not supported here. Patients who regularly attended swallowing and speech therapy sessions appeared to have superior functional outcomes. They had a lower rate of G-Tube reliance and produced more intelligible speech. Although, the difference was not as pronounced for -word intelligibility, it was noticeable for mean sentence intelligibility. Patients who attended >80% of sessions experienced minimal change in sentence intelligibility ( 4%) and had mean scores of nearly 80%. Such outcomes have been postulated in previous studies where success was predicted to be greater in motivated patients attending rehabilitation programs. 3,4,11,39 Quality of life scores were found to marginally decrease postoperatively, which indicates an improvement. The result is surprising, as swallowing and speech functional were found to have deteriorated. This lack of correlation could be due to improved pain control, peace of mind after tumor ablation or due to strong social supports. Few studies exist that have used validated quality of life measures in extensive glossectomy patients. In one of the more objective studies, it was shown that total glossectomy patients can achieve good quality of life. 35 Other studies have shown that patients who are motivated, have emotional support from their families, attend regular follow-up visits with their physicians, and attend rehabilitation sessions with speech language pathologists have the highest quality of life and often the best outcomes. 3,7,40 Perhaps, preoperative counseling including preparing the patient and their family for the challenges ahead played a role in maintaining quality of life in TGLP patients. The weaknesses of this study are inherently due to a small sample size and selection bias. For example, only those who were able to swallow could perform swallowing function tests and not all patients who could swallow agreed to be tested. Moreover, testing could only be carried out in those who survived. When comparing groups based on rehabilitation attendance, the small sample size prohibited any meaningful statistical analyses. As such, interpretations of these group comparisons must be taken with caution. Lastly it must be kept in mind that this study focused on patients undergoing primary surgery. It is known that functional outcomes tend to deteriorate in post- RT salvage cases; therefore, these CONCLUSION This is the first study to demonstrate objectively measured functional outcomes for patients undergoing extensive glossectomy. Moreover, available data from the literature have been combined to provide a comprehensive data set. The results show that 24% of patients with TGLP, free flap reconstruction, and adjuvant RT can achieve safe, swallowing function. Those who fail in this endeavor are limited by swallowing transit time. Speech intelligibility can reach near preoperative levels and quality of life can improve in this unfortunate population. 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