Comparison of Functional Outcomes After Endoscopic ...

Annals of Otology, Rhinology & Laryngology 115(11):827-832. © 2006 Annals Publishing Company. All rights reserved.

Comparison of Functional Outcomes After Endoscopic Versus Open-Neck Supraglottic Laryngectomies Giorgio Peretti, MD; Cesare Piazza, MD; Augusto Cattaneo, MD; Luigi De Benedetto, MD; Eva Martin, MD; Piero Nicolai, MD Objectives: Endoscopic supraglottic laryngectomy (ESL) by carbon dioxide laser for selected T1-T3 supraglottic squamous cell carcinotnas is a sound procedure with oncological results comparable to those obtained by open-neck supraglottic laryngectomy (ONSL). The aim of this study was to retrospectively evaluate functional outcomes after ESL in comparison with ONSL. Methods: We performed perceptual voice evaluation by GRBAS (grade, roughness, breathiness, asthenicity, strain), subjective analysis by Voice Handicap Index, objective analysis with the Multidimensional Voice Program, swallowing evaluation with the M. D. Anderson Dysphagia Inventory, video nasal endoscopic examination of swallowing, videofluoroscopy, and analysis of hospitalization time, need for and duration of feeding tube and tracheotomy, and complication and aspiration pneumonia rates in a group of 14 patients treated with ESL. These results were compared to those obtained in a historical group of 14 patients matched for T category who were treated with ONSL at the same institution. Statistical analysis was performed with the Mann-Whitney LI and Pearson x^ tests. Results: Comparison of comprehensive voice analysis, M. D. Anderson Dysphagia Inventory, and complication and aspiration rates showed no statistically significant differences between the two groups. However, significant differences were found for video nasal endoscopic examination of swallowing (p = .03), videofluoroscopy (p = .03), hospitalization (p = .0001), feeding tube duration (p = .0001), and tracheotomy duration (p = .0001). Conclusions: Endoscopic supraglottic laryngectomy had a significantly lower functional impact on swallowing than ONSL, even though it was not subjectively perceived by patients, and was associated with less morbidity and a shorter hospitalization time. Key Words: carbon dioxide laser, endoscopic supraglottic laryngectomy, open-neck supraglottic laryngectomy, supraglottic cancer, swallowing, vocal outcome.

INTRODUCTION

coregional control.'"^ One of the most evident advantages of an endoscopic procedure for supraglottic tumors is the reduced perioperative and postoperative morbidity, with consequent shorter hospitalization times and a more favorable cost-effectiveness ratio.'"'^ Nevertheless, to the best of our knowledge, only a limited number of reports'^"'^ have compared functional outcomes after traditional open-neck supraglottic laryngectomy (ONSL) and endoscopic supraglottic laryngectomy (ESL), and only 2 series with patients matched for T categories have been published.''^•'5 Moreover, no studies have evaluated swallowing by a comprehensive deglutition examination including subjective, endoscopic, and radiologic evaluations.

Fven though transcervical horizontal supraglottic laryngectomy is still considered the standard procedure for purely supraglottic carcinoma in a patient in whom an organ-preserving surgical treatment is suitable, growing evidence from the international literature has recently demonstrated comparable and reproducible oncological outcomes for Tl, T2, and selected T3 cancers treated endoscopically by carbon dioxide (C02) laser.'"^ Moreover, treatment of the neck, which invariably has a higher probability of finding occult nodal disease in even early-stage supraglottic carcinomas as compared to glottic cancers, can be substituted by a wait-and-see policy, or the patient can take advantage of delayed elective or simultaneous therapeutic neck dissections, or even complementary radiotherapy, according to the T and N categories, apparently without a decrease in lo-

Therefore, our aim was to retrospectively evaluate 2 groups of patients matched for T category and treated in the same institution with ESL and ONSL,

From the Departments of Otolaryngology (Peretti, Piazza, Cattaneo, De Benedetto, Nicolai) and Radiology (Martin), University of Brescia, Brescia, Italy. Presented at the meeting of the American Laryngological Association, Chicago, Illinois, May 19-20,2006. Correspondence: Giorgio Peretti, MD, Dept of Otolaryngology, University of Brescia, Piazza Spedali Civili 1,25123 Brescia, Italy.

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Peretti et al. Functional Outcomes After Endoscopic Supraglottic Laryngectomy

by comparing the perioperative complications and aspiration pneumonia rates, the need for tracheotomy and/or feeding tube, hospitalization time, and functional outcomes in terms of voice and swallowing. MATERIALS AND METHODS Between July 1988 and December 2005, 46 selected patients with supraglottic carcinoma (11 Tl, 29 T2, and 6 T3) underwent ESL by C02 laser at the Department of Otolaryngology of the University of Brescia, Italy. In order to compare the functional outcomes of ESL with those obtained by ONSL, we selected a group of 14 patients treated with C02 laser resection with the following inclusion criteria: no preoperative or postoperative chemotherapy and/ or radiotherapy, no extension of supraglottic laryngectomy to the base of the tongue and/or one arytenoid cartilage, a minimum oncological follow-up of 2 years, and no locoregional recurrence, distant metastases, or second tumors at the time of last consultation (October 2005). This group included 11 men and 3 women with a mean age of 67 years (range, 54 to 77 years). Postoperative staging according to the sixth edition of the TNM system'^ was as follows: 11 T2 NO, 1 T2 Nl, 1 T2 N2b, and 1 T3 NO. The preoperative diagnostic assessment included spirometry to assess for adequate pulmonary function (defined as a greater-than-50% ratio of forced expiratory volume in 1 second to forced vital capacity), videolaryngoscopy by rigid and flexible endoscopes, a computed tomographic scan or magnetic resonance imaging scan, and ultrasound examination of the neck. Moreover, intraoperative rigid endoscopy by 0° and angled telescopes was applied in order to properly evaluate the superficial tumor extension to adjacent laryngeal subsites. Complete exposure of the supraglottis was obtained by an adjustable bivalved laryngopharyngoscope, repeatedly modified in its position during surgery to get an optimal view of the surgical field. A Sharplan 1055 S C02 laser with an Acuspot 712 micromanipulator (Sharplan, Tel Aviv, Israel) with superpulse emission in continuous mode (from 2.5 to 5 W; 270-|im spot size) was used. Vessels that could not be coagulated by the laser, particularly at the level of the superior laryngeal pedicle in the aryepiglottic fold, were managed by monopolar cautery and/or hemostatic microclips. The endoscopic resections comprised 7 hemisupraglottic laryngectomies (ie, hemiepiglottectomy with removal of the ipsilateral aryepiglottic and false vocal folds) and 7 complete endoscopic supraglottic laryngectomies. Tumor resection was performed en bloc for small lesions and by transtumoral piecemeal resection in the case of bulky tumors. Frozen sections

were not routinely obtained at the end of the procedure. Two patients with cN+ disease underwent concomitant selective neck dissection (levels II to V), and the only pT3 patient of this series was treated by a 1-month-delayed selective neck dissection (levels II to IV) even though staged as cNO (later confirmed by postoperative histopathologic examination of cervical lymph nodes as pNO). The ESL group was compared to a historical group of 14 selected patients (13 men and 1 woman; mean age, 59 years; range, 48 to 75 years) treated with ONSL at the same institution between 1988 and 1995. The same inclusion criteria followed for the ESL group were also observed for recruitment of patients in the ONSL group. Patients were also matched with those of the ESL group for T category. The TNM staging of these patients was as follows: 1 Tl NO, 10 T2 NO, 1 T2 Nl, and 2 T3 NO. Eive patients underwent concomitant operations on the larynx and neck (selective neck dissection of levels II to IV or II to V), unilateral in 2 patients (both T2 NO) and bilateral in 3 patients (1 T2 Nl and 2 T3 NO). The patients of both groups were submitted to comparable postoperative swallowing rehabilitation protocols. Moreover, from an oncological point of view, they were periodically examined with a rigid or a flexible fiberoptic laryngoscope, and ultrasound evaluation of the neck was performed twice yearly for the first 2 years and every 12 months thereafter. We analyzed both ESL and ONSL patient groups at least 2 years after surgery using a protocol including retrospective clinical chart review focusing on complication and aspiration pneumonia rates; hospitalization time; need for and duration of feeding tube and tracheotomy; comprehensive voice assessment by means of subjective analysis by Voice Handicap Index (VHI),'^ perceptual voice evaluation (GRBAS scale),'^ and objective analysis by the Multidimensional Voice Program (MDVP); and deglutition assessment by the M. D. Anderson Dysphagia Inventory (MDADI),'^ video nasal endoscopic examination of swallowing (VEES) with blue food coloring, and videofluoroscopy (VES) during barium swallow. The VHI questionnaire scores were grouped in 5 different categories: score 0 (normal voice), scores 1 to 30 (slight dysphonia), scores 31 to 60 (moderate dysphonia), scores 61 to 90 (severe dysphonia), and scores 91 to 120 (very severe dysphonia).'^ Perceptual evaluation was accomplished by a panel of otolaryngologists and speech pathologists on a running speech voice sample and graded according to the GRBAS scale,'^ which consists of 5 domains:


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TABLE 1. RESULTS OF VOICE HANDICAP INDEX" QUESTIONNAIRE FOR ESL AND ONSL GROUPS Score 0 Score 1-30 Score 31-60 Score 61-90 Score 91-120 (Normal Voice) (Slight Dysphonia) (Moderate Dysphonia) (Severe Dysphonia) (Very Severe Dysphonia) ESL group (N= 14) 2 10 2 ONSL group (N= 14) 3 II 0 ESL — endoscopic supraglottic laryngectomy; ONSL — open-neck supraglottic laryngectomy.

grade (G), roughness (R), breathiness (B), asthenicity (A), and strain (S). Each patient was rated in all 5 domains on a grading scale ranging from 0 to 3. Score 0 corresponded to a normal voice, score 1 to a slight voice problem, score 2 to a moderate voice problem, and score 3 to a severe voice problem. Objective analysis including percent jitter, percent shimmer, and noise-to-harmonics ratio was performed with the MDVP on the sustained vowel /a/ uttered 3 times, with pitch and loudness held as constant as possible for at least 3 seconds. Subjective evaluation of dysphagia was performed with a self-administered questionnaire designed by Chen et al,!^ namely, the MDADI. The questionnaire is composed of 20 items, including 1 general question evaluating the global impact of swallowing on overall daily life, and 3 subscales (emotional, functional, and physical). From the answers given by the patients to each question, a score ranging from 0 (extremely low functioning) to 100 (high functioning) was obtained. We performed VEBS with a flexible digital videonasolaryngoscope coupled to a dedicated videoprocessor. Patients never received topical anesthetic and were evaluated during swallowing of blue-dyed semiliquid food with a flexible endoscope positioned above the epiglottis before and during the swallow and then advanced above the vocal folds after the swallow to precisely evaluate subglottic penetration and/or tracheal aspiration. All examinations were videorecorded and then evaluated and scored by a panel of otolaryngologists and speech pathologists. According to Donzelli et al,20 we graded such scores on a 3-point scale: 1, no food entering the laryngeal vestibule; 2, food entering the laryngeal vestibule, without penetration or aspiration; and 3, tracheal aspiration of food. We performed VFS by oral administration of liquid and semiliquid contrast media (barium or isoosmolar water-soluble contrast medium) in the right lateral and anteroposterior projections with rapid digital registration of swallowing (30 frames per second) using a Siregraph CF (Siemens, Forchheim, Germany). In order to obtain a clear correlation between VEES and VFS outcomes, the 3-point scale proposed by Donzelli et apo was also applied to radiologic examinations. Moreover, a comparison

0 0

0 0

between VEES and VFS results was performed to evaluate the intertest reliability in the specific scenario of swallowing after supraglottic resection. Statistical analysis was performed with the Mann-Whitney U test for comparison of continuous variables (ie, complication and aspiration pneumonia rates, hospitalization time, nasogastric feeding tube and tracheotomy duration, VHI score, GRBAS score, objective analysis by MDVP, and the MDADI score). The Pearson x^ test was applied to compare categorical variables (ie, VEES and VFS scores). A p value of less than .05 was considered statistically significant for both tests. RESULTS A retrospective review of charts in our patient population showed that complications occurred in 2 patients in the ESL group (postoperative bleeding that required endoscopic revision and electrocautery) and in 3 patients in the ONSL group (cervical wound partial dehiscence in 2 and postoperative bleeding in 1). No statistically significant difference was found with the Mann-Whitney U test. No aspiration pneumonia was reported in either group. Tracheotomy was performed in 2 of 14 patients (14.2%) and the cannula was removed after a mean of 4.5 days (range, 3 to 6 days) in the ESL group, whereas all patients in the ONSL group had tracheotomy (100%) and retained the cannula for a mean of 35.1 days (range, 12 to 48 days). No permanent tracheotomy was needed in either group. A nasogastric feeding tube was placed in 3 of 14 patients (21.4%) in the ESL group and was removed after a mean of 5.3 days (range, 3 to 13 days). In the ONSL group, 12 of 14 patients required a nasogastric feeding tube and 2 needed percutaneous endoscopic gastrostomy (100% of non-oral feeding after surgery); these remained in place for a mean of 18.9 days (range, 14 to 32 days). No permanent feeding tube was necessary in either group. The hospitalization times were 10.5 days (range, 4 to 24 days) for the ESL group and 26 days (range, 18 to 43 days) for the ONSL group. All of these differences were statistically significant (p = .0001) on the Mann-Whitney U test. The results of the VHI questionnaire are detailed in Table 1.' ^ Statistical analysis with the Mann-Whitney U test showed no significant difference between the ESL and ONSL groups. The mean values ob-


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was obtained in 75% of cases.

TABLE 2. MEAN RESULTS OF PERCEPTUAL VOICE EXAMINATION FOR EACH DOMAIN OF GRBAS GRADING SYSTEM'S Grade Roughness Breathiness Asthenicity Strain ESL group ONSL group

1.08

0.3

0.5

0.75

1.2

1.1

1

0.2

0.1

1.2

tained during perceptual voice examination for each domain of the GRBAS grading system are reported in Table 2.'^ Again, no statistically significant difference between the two groups was found on the Mann-Whitney U test. The results of objective voice evaluation by MDVP are summarized in Table 3; the values of the median and the 25th and 75th percentiles of jitter, shimmer, and noise-to-harmonics ratio for controls (normal population) and for both ESL and ONSL groups are reported. The Mann-Whitney U test failed to show statistically significant differences between the values of controls and ESL and ONSL patients. The mean scores obtained with the MDADI questionnaire were 84.1 (range, 69 to 100) and 85.3 (range, 66 to 98) for the ESL and ONSL groups, respectively. The Mann-Whitney U test did not show any statistically significant differences between the two groups. Table 4^^ summarizes the results obtained after VEES and VES in these groups, reporting the percentages of patients for each level according to the adopted 3-point scale. The Pearson %2 test showed a statistically significant difference between ESL and ONSL patients for both VEES (p = .03) and VES(p = .O3). Comparison between VEES and VES outcomes showed a strict correlation between these two tests (ie, patients were categorized in the same level according to Donzelli et apo by both tests) in 54% of patients. In 32% of subjects, VES overstaged patients previously evaluated by VEES (ie, patients classified as having normal swallowing at VEES showed vestibule penetration or tracheal aspiration at VES, and patients with simple vestibule penetration at VEES displayed frank aspiration at VES). If the VEES and VES outcomes were further simplified as normal (level 1) or altered swallowing (levels 2 and 3), concordance between these two tests

DISCUSSION In ONSL, removal of the supraglottic carcinoma implies resection or detachment of the uninvolved extrinsic infrahyoid muscles, part of the laryngeal framework, and healthy soft tissues of the endolaryngeal supraglottis itself in a standard fashion due to the reconstructive needs. The continuity of the aerodigestive tract is in fact obtained by performing a thyrohyoidopexy after impaction of the base of the tongue and the residual laryngeal structures, which is possible only if a symmetrical resection has been performed. Even though preservation of the main trunk and posterior descending branch of the internal division of the superior laryngeal nerve can be obtained by a meticulous dissection ,2' temporarily insensate residual laryngeal and hypopharyngeal mucosa can negatively affect swallowing rehabilitation even for prolonged periods of time.^^ Indeed, a tracheotomy for postoperative edema and a feeding tube for exclusion of the surgical wounds from mechanical stress and food contamination are to be considered mandatory after ONSL. In contrast, endoscopic treatment of supraglottic cancer allows the possibility of performing a custom-tailored tumor resection according to the site and local extension of the individual lesion to be treated.'"^ In fact, a modulated endoscopic resection ranging from suprahyoid epiglottectomy to comprehensive supraglottic laryngectomy can be effectively performed in selected supraglottic cancers even without affecting the extrinsic musculature, the laryngeal framework, or the superior laryngeal nerves proximal to the larynx. Moreover, uninvolved soft tissues adjacent to the tumor can be left undisturbed within a safe margin of a few millimeters, and no symmetrical resection is needed for reconstructive purposes, because the supraglottic wound is left to heai by secondary intention. All of these advantages are reflected by a statistically significant faster rehabilitation after ESL, with a reduced need for tracheotomy or a feeding tube, as confirmed by the results of the present series and those of other authors.'"^-^"'^ Even though the present study does not quantitatively focus on economic concerns, our data relating to the hospitalization

TABLE 3. VOCAL PARAMETERS EVALUATED IN ACOUSTIC ANALYSIS BY MULTIDIMENSIONAL VOICE PROGRAM Fundamental Frequency (Hz) Jitter Shimmer Noise-to-Harmonics Ratio

Controls ESL group ONSL group

Median

Interquartile Range

Median

Interquartile Range

Median

Interquartile Range

Median

Interquartile Range

Ml.95 143.05 116.02

119.37-143.48 119.43-170.10 101.10-161.60

0.69 1.31 1.53

0.50-0.89 0.58-2.43 0.90-1.93

4.32 6.89 6.24

3.14-6.63 5.55-8.10 5.48-8.41

0.14 0.16 0.15

0.13-0.15 0.14-0.19 0.14-0.22

Peretti et al. Functional Outcomes After Endoscopic Supraglottic Laryngectomy TABLE 4. VEES AND VFS OUTCOMES IN ESL AND ONSL PATIENTS VEES(%) ESL ONSL Group Group Level 1 Level 2 Level 3

64 28 8

21 43 36

VFS (%) ESL ONSL Group Group 58 21 21

20 0 80

VEES — video nasal endoscopic examination of swallowing; VFS — videofluoroscopy.

time clearly show a favorable cost-effectiveness ratio of ESL, with a reduction of more than 50% in hospital stay compared with ONSL. Other indirect costs to the family and social environment (eg, days missing from work, time and cost for swallowing rehabilitation, and treatment of complications) cannot be precisely evaluated in the present series, but they undoubtedly diminished in a parallel fashion. As expected, the choice between an endoscopic or an open-neck approach to purely supraglottic carcinomas does not produce a significantly different impact on voice quality. The subtle differences due to prelaryngeal muscle resection, alteration of the laryngeal position in the neck with ensuing shortening of the vocal tract, possible impairment of laryngeal mucosal sensation and cricothyroid muscle activity, and cervical fibrosis consequent to a transcervical procedure are probably not able to be demonstrated by the state-of-the-art comprehensive voice evaluation protocol described by Dejonckere et al,^-' particularly in a small population such as the present one. Evaluation of swallowing was the main goal of the present study and was therefore performed by a multiperspective view, including subjective evaluation by the MDADI questionnaire and objective examination by both VEES and VFS performed by dedicated otolaryngologists and radiologists. The MDADI apparently did not reveal significant impairment of swallowing, which was described by both ESL and ONSL patients as fair and without a significant negative impact on the daily quality of life. Concerning subjective evaluations like this, one could argue that a meaningful comparison between swallowing function after these procedures could be effectively done only by patients treated by ESL followed by ONSL, which are virtually impossible to find. Therefore, in our opinion, the MDADI should be considered as a useful tool to evaluate subjective swallowing after a single procedure, even though it loses part of its value when applied to a comparative study between different approaches. The limited value of the MDADI in comparative studies has been confirmed in the present series by

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the statistically different outcomes obtained by objective examinations of swallowing. Both VEES and VFS provide the possibility of direct quantification of swallowing problems after supraglottic resection, with reasonable intertest reliability already shown by others^'^ and confirmed by our data, even though they measure different aspects of deglutition itself. In fact, VEES is mainly focused on the anatomic and functional alterations that can impair food transit in the oropharyngeal and hypopharyngeal cavities. Moreover, it can be successfully applied to direct the postoperative swallowing rehabilitation program,'" which we consider of paramount importance, both in patients with signs of aspiration (and therefore temporarily feeding tube-dependent) and in those without major deglutition problems, in regaining a normal or near-normal diet as early as possible. Nonetheless, even in experienced hands, VEES may provide false-negative results (particularly in cases of minimal food penetration during the early phase of deglutition) due to the "whiteout phase" of swallowing, when the endoscope does not show anything for velopharyngeal contact and pharyngeal wall contraction.25>26 In contrast, VFS shows only 2-dimensional dynamic images and gives little insight into the anatomic details, but gives the unique possibility to detect even minor aspiration in the subglottis and trachea throughout each phase of deglutition. On the basis of the present experience, we strongly suggest that the combination of VEES and VFS be used for further studies focused on a comprehensive examination of swallowing impairment. Interestingly, in both groups, VFS showed a higher than expected percentage of patients in level 3 (tracheal aspiration of liquid bolus) according to the 3-point scale proposed by Donzelli et al,20 even though with a silent history of aspiration pneumonia or subjective dysphagia. Moreover, this rate reached an extraordinary 80% in ONSL patients, which is nearly 4 times that observed in the ESL group, who nonetheless displayed a non-negligible 21% rate of aspiration. Such a noticeable difference is certainly due in part to the different amount of soft endolaryngeal tissues removed in the ESL group, in which half of the patients underwent less than a comprehensive ESL, thus maintaining some sphincteric function of the residual epiglottis and ipsilateral aryepiglottic and false vocal folds. At any rate, in our opinion, this is not a point of criticism for the present study; it represents indeed the essential advantage of endoscopic versus open-neck surgery. The above-mentioned objective data reinforce our belief that an early and effective rehabilitation pro-

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Peretti et al, Functional Outcomes After Fndoscopic Supraglottic Laryngectomy

gram for swallowing should always be performed in both ONSL and ESL patients, even considering the reduced burden of associated morbidity in the latter group. These results also raise the possibility of late pulmonary complications in patients treated for supraglottic cancer, who are typically advanced in age and have chronic obstructive pulmonary disease and a higher risk of cerebrovascular events, even years after the oncological procedure itself. In this light, an endoscopic approach to these tumors, reducing the incidence of food aspiration, should therefore be considered particularly intriguing for elderly and/or neurologically compromised subjects.^

In conclusion, ESL is a surgical approach that, in the presence of selected patients (with adequate exposure of the endolarynx) and tumors (Tl, T2, and T3 with minimal invasion of the preepiglottic space), permits good and reproducible oncological results comparable to those of standard ONSL. Moreover, the possibility of endoscopically tailoring the supraglottic resection to spare uninvolved adjacent tissues greatly reduces perioperative morbidity, social costs, and swallowing problems, even though the vast majority of the dysphagic symptoms usually do not subjectively affect the daily quality of life of patients, even those treated with ONSL.

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