Video Fluoroscopic Evaluation After Glossectomy

ORIGINAL ARTICLE Video Fluoroscopic Evaluation After Glossectomy

Cristina Lemos Barbosa Furia, SP; Elisabete Carrara-de Angelis, SP; Nı´via Maria Silva Martins, SP; Ana Paula Branda˜o Barros, SP; Benjamin Carneiro, MD; Luiz Paulo Kowalski, MD

Background: The swallowing deficits that result from Results: All patients who underwent a partial glossec- oral or oropharyngeal resections vary considerably de- tomy had difficulties with formation and anteroposte- pending on the site, extension of the resection, and type rior propulsion of the bolus in the oral cavity and an of reconstruction. Most patients will experience some de- increase in oral transit time, which was more evident gree of dysphagia despite the reconstructive effort. Fur- with materials of thicker consistencies. All patients who thermore, a glossectomy is frequently associated with voice underwent a total or subtotal glossectomy with laryn- and speech difficulties. geal preservation had an increase in oral transit time and stasis of food in the oral cavity, the pharynx, and Objectives: To characterize swallowing in patients the superior esophageal sphincter. Of the 15 patients, 2 who underwent a glossectomy and to define the limits had moderate and asymptomatic aspiration. These 2 and the compensatory movements using video fluoro- patients had swallowing compensations, such as scopic analysis. increased buccal, mandibular, pharyngeal, and laryngeal activity and voluntary protection of the larynx dur- Design and Setting: Video fluoroscopic evaluation of ing swallowing. 15 patients who underwent glossectomies at the Centro de Tratamento e Pesquisa Hospital do Caˆncer A. C. Ca- Conclusions: This study demonstrates the effective- margo, Sa˜o Paulo, Brazil. ness of swallowing in patients who were enrolled in voice, speech, and swallowing rehabilitation after undergoing Patients: We examined 15 patients: 5 who underwent a a partial or total glossectomy. An increase in oral transit partial glossectomy, 2 who underwent a subtotal glossec- time was detected in all patients. Only 2 of the 10 pa- tomy, and 8 who underwent a total glossectomy with la- tients who underwent a total glossectomy had persis- ryngeal preservation and reconstruction with myocutane- tent asymptomatic aspiration. ous flaps (9 pectoralis major flaps and 1 latissimus dorsi flap). The 15 patients were enrolled in a program that in- cluded voice, speech, and swallowing rehabilitation. Arch Otolaryngol Head Neck Surg. 2000;126:378-383

ORMAL SWALLOWING is a the anterior palatine arch from which the dynamic and short pro- pharyngeal phase of swallowing begins. cess. The preparation The swallowing reflex is responsible for phase begins when the elevating and closing the larynx and for From the Departments of Voice, food is placed in the oral velopharyngeal closure, which prevents Speech, and Swallowing cavityN and undergoes mastication and ex- nasal reflux. Finally, the esophageal phase Rehabilitation (Mss Furia, tends until the tongue moves to central- of swallowing begins when the bolus Carrara-de Angelis, Martins, ize the bolus. In the oral phase, the tongue reaches the superior esophageal sphinc- and Barros), Imaging initiates an anteroposterior movement, di- ter (SES), and the region opens as a con- (Dr Carneiro), and Head and recting the food backward and generat- sequence of a complex set of events. Neck Surgery and Otolaryngology (Dr Kowalski), ing negative pressure in the oral cavity, and Glossectomies may result in dyspha- Centro de Tratamento e propels the bolus toward the pharynx. The gia, and the severity depends on the Pesquisa Hospital do Caˆncer normal transit time of the oral phase takes extension of resection, the mobility of the A. C. Camargo, Sa˜o Paulo, less than 1 second.1 By the undulatory residual portion, the type of reconstruc- Brazil. movement of the tongue, the bolus reaches tion, the involvement of other structures

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 in the region, and the patient’s motivation and capacity to adapt to the results of the surgery. PATIENTS AND METHODS The use of objective resources, such as video fluoroscopic evaluation, enables the visualization of the com- 1 From April 1, 1993, to March 31, 1997, 45 patients plete swallowing process. In 1983, Logemann sug- gested the use of video fluoroscopy to evaluate the underwent a subtotal or total glossectomy and 210 2 patients underwent a partial glossectomy at the De- dynamic swallowing process. Montesi et al and Costa 3 partment of Head and Neck Surgery and Otolaryn- et al reported that this type of examination allows for gology, Centro de Tratamento e Pesquisa Hospital do the definition of anatomical and functional swallowing Caˆncer A. C. Camargo, Sa˜o Paulo, Brazil. Between Au- dysfunctions that occur preoperatively and postopera- gust 15, 1997, and October 30, 1997, 15 patients who tively; the determination of possible oral feeding tech- underwent treatment at the Department of Voice, niques regarding quantity, consistency, and compen- Speech, and Swallowing Rehabilitation at the same sation; and the planning of a therapeutic approach. hospital participated as volunteers in the present The objectives of the present study are to charac- study. The patients underwent glossectomies (8 total, 2 subtotal [the presence of 10% of the base of the terize swallowing in patients who underwent a total, sub- tongue], and 5 partial) 3 to 50 months prior to the total, or partial glossectomy and to define the limits and video fluoroscopic evaluation. Of the 15 patients, only the compensatory maneuvers using video fluoroscopic 3 did not have complaints about swallowing. Two pa- evaluation. tients received food orally and by a nasogastric tube. The remaining 13 patients received oral feeding (pa- RESULTS tients who underwent total and subtotal glossectomies received liquid, thick liquid, and paste food and All patients swallowed the standardized quantities of liq- patients who underwent partial glossectomies re- uid, paste, and solid materials, although aspirations were ceived food of all consistencies). All patients received speech and voice therapy for a mean of 3 observed. months. Of the 15 patients, 11 used alcohol and to- Table 2 describes the events observed in the oral bacco. Table 1 shows the data regarding age, sex, and pharyngeal phases and the presence of aspiration, TNM staging,4 tumor site, histological type, extent penetration (the entry of food to the level of the vocal of resection, surgical procedure, reconstruction of the folds), and conclusion of swallowing (functional swal- esophageal region, and adjuvant treatment. lowing or mild or moderate aspiration) of each Video fluoroscopic evaluation of swallowing was patient. carried out at the Department of Imaging using ra- Regarding the swallowing mechanism of patients diographic equipment (model system 1600E; GE who underwent a total or subtotal glossectomy, we Medical Systems, Milwaukee, Wis) and was per- observed stasis in all areas of the oropharyngeal tract, formed jointly by a radiologist (B.C.) and a speech pathologist (C.L.B.F., E.C.-A., N.M.S.M., or A.P.B.B.). especially in the valleculae, the flap, the tongue stump Patients stood during the examination, and the fo- (in patients who underwent subtotal glossectomies), cus of the fluoroscopic image was defined anteriorly and the SES (Figure 1). In addition, we observed a by the lips, superiorly by the hard palate, posteri- reduction of laryngeal elevation and, consequently, a orly by the posterior pharyngeal wall, and inferiorly reduction of the SES opening. The oral transit time was by the bifurcation of the airway and esophagus (the longer for all food consistencies, especially for paste seventh cervical vertebra). Different types and quan- (Ͼ3 seconds). We less frequently observed the charac- tities of material were given during the anteroposte- teristic stasis of the anterior and lateral sulcus and the rior (profile) and lateral views. The material used was hard and soft palate (Table 2). liquid barium and paste barium. For patients who un- Two patients had asymptomatic aspiration after derwent a partial glossectomy, a solid material Figure 2 (cracker) also was given. The patients were in- swallowing ( ). Laryngeal penetration of food structed to swallow 2 or 3 types of material 3 times was observed before swallowing in 2 patients, during each (liquid, paste, and solid) in variable amounts. swallowing in 4 patients, and after swallowing in 8 The patients were directed to swallow both the liq- patients, but these patients were able to cough or clear uid and the paste in quantities of 3, 5, and 10 mL (3 their throats during this mechanism, eliminating the mL given with a spoon and 5 and 10 mL given with risk of aspiration. a syringe placed on the anterior portion of the oral All patients moved the food and their heads back- cavity) and to continuously swallow liquid from a cup ward. The patients used the following maneuvers: the (15-20 mL). For the solid material, the patients were supraglottic maneuver (the patients were taught how instructed to masticate the material well before swal- to close the airway before, during, and after degluti- lowing. The videotapes were analyzed jointly by 5 speech pathologists (C.L.B.F., E.C.-A., N.M.S.M., or tion) (8 patients), the Mendelsohn maneuver (the A.P.B.B.) experienced in video fluoroscopic evalua- patients were taught to hold the larynx elevated for a tion. The oral transit time for swallowing was evalu- longer period during deglutition) (2 patients), and ated following these criteria: for liquid, normal (Յ1 multiple deglutitions (2 patients). Compensatory second) or increased (Ͼ1 second) and for paste and movements of lip protrusion, suction, and intraoral solid, normal (Յ3 seconds) or increased (Ͼ3 space reduction through mandible movements also seconds). were fairly frequent (Figure 3). We detected functional swallowing in 8 patients and moderate aspiration after deglutition in 2 patients. One

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Extension of Adjuvant Treatment Patient No./ TNM Tumor Histological Tongue After Flap Age, y/Sex Staging† Site Type Resection, % Surgical Procedure Location Chemotherapy Radiotherapy 1/10/F T3 N0 M0 Oral cavity Sarcoma 100 Total glossectomy Latissimus Before None and base and SOHND dorsi of tongue 2/52/F T4 N0 M0 Oral cavity SCC 100 Total pelveglossectomy, Pectoralis None After and base amplified SOHND, major of tongue and MRND 3/71/M TX NX M0 Oral cavity and SCC 100 Total glossectomy and left Pectoralis After After tongue SOHND major 4/51/M TX NX M0 Floor of mouth SCC 100 Total pelveglossectomy, Pectoralis Before Before sectional mandibulectomy, major right RND, and left ESOHND 5/75/M TX N0 M0 Base of tongue SCC 100 Total glossectomy, RND, and Pectoralis None Before SOHND major 6/56/M T4 N2 M0 Floor of mouth SCC 100 Total pelveglossectomy, Pectoralis After After marginal mandibulectomy, major and bilateral MRND 7/61/M T3 N2c M0 Tongue SCC 100 Total pelveglossectomy, right Pectoralis None After RND, and left ESOHND major 8/54/M T3 N2b M0 Tongue SCC 100 Total glossectomy, right Pectoralis None Before ESOHND, and left RND major 9/52/M T3 N2b M0 Floor of mouth SCC 90 Subtotal pelveglossectomy and Pectoralis None After and tongue bilateral RND major 10/68/F T2 N0 M0 Tongue SCC 90 Subtotal pelveglossectomy, Pectoralis None After right ESOHND, and left major MRND 11/31/F TX NX M0 Floor of mouth Hemangioma 5-25 Partial glossectomy None None None 12/56/M T2 N0 M0 Floor of mouth SCC 25-50 Partial pelveglossectomy and Tongue None None and tongue SOHND 13/80/M TX NX M0 Tongue border SCC 5-25 Partial pelveglossectomy and None Before After left MRND 14/44/F T2 N0 M0 Tongue border SCC 5-25 Partial pelveglossectomy and None None None left ESOHND 15/53/M T4 N1 M0 Lower gum SCC 5-25 Pelveglossectomy, marginal None None After mandibulectomy, and MRND

*SOHND indicates supraomohyoid neck dissection (ND); SCC, squamous cell carcinoma; pelveglossectomy, partial glossectomy with pelvectomy (floor of the mouth resection); MRND, modified radical ND; RND, radical ND; and ESOHND, extended SOHND. †According to the Union Internationale Contre le Cancer.4

Table 2. Descriptions of Swallowing in 15 Patients Who Underwent Glossectomies*

Oral Phase Pharyngeal Phase Patient No. RVLV RBFP IOTT DSR SOC STS SF RLMT IVC RVC SV SP SSES RSESO RLE RGC SPS 1 No No Yes ...... Yes No ...... Yes ...... Yes ...... 2 No No Yes ...... No ...... Yes ... Yes Yes Yes ...... 3 No No Yes Yes ...... No ...... Yes ... Yes Yes Yes ...... 4 No No Yes Yes ...... No ...... Yes ... Yes Yes Yes ...... 5 No No Yes Yes ...... Yes No ... Yes Yes ... Yes Yes Yes ...... 6 No No Yes ... Yes ... Yes No ...... Yes Yes ...... Yes 7 No No Yes ...... Yes No ...... Yes Yes Yes Yes Yes ... Yes 8 No No Yes Yes Yes ... Yes No ...... Yes Yes Yes Yes Yes ...... 9 No No Yes ... Yes Yes Yes No ...... Yes Yes Yes ...... 10 No No Yes ... Yes Yes ... No ...... Yes ... Yes Yes Yes ... Yes 11 ...... Yes ...... Yes ...... 12 ...... Yes ... Yes ...... Yes ...... Yes ... Yes ...... Yes 13 Yes Yes Yes ... Yes ...... Yes ...... Yes ... Yes ...... 14 ...... Yes Yes ...... Yes Yes ... Yes ... Yes ...... 15 ...... Yes ...... Yes ...... Yes ......

*RVLV indicates reduced vertical lingual movement; RBFP, reduced bolus formation and propulsion; IOTT, increased oral transit time; DSR, delayed swallowing reflex; SOC, stasis in oral cavity (lateral and anterior sulcus and hard and soft palate); STS, stasis in tongue stump; SF, stasis in the flap; RLMT, reduced lateral movement of the tongue; IVC, inefficient velophyaryngeal closure; RVC, reduced vestibule closure; SV, stasis in valleculae; SP, stasis in pharynx; SSES, stasis in superior esophogeal sphincter; RSESO, reduced superior esophageal sphincter; RLE, reduced laryngeal elevation; RGC, reduced glottic closure; SPS, stasis in pyriform sinus; and ellipses, not applicable.

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 patient (patient 5) underwent a gastrostomy, and an- in 1953; because of the risk of postsurgical aspiration, a other patient (patient 8) underwent a total laryngec- total laryngectomy was carried out at the same time as the tomy. In patient 8, the swallowing mechanism after the glossectomy.5,6 Total glossectomy with laryngeal preser- laryngectomy was functional with liquid, thick liquid, and vation was proposed by Kothary and DeSouza7 in 1973, paste. We observed compensatory maneuvers that and since then the functional results of the technique have increased the oral phase, but the patient showed stasis been discussed, but few objective studies have been de- in the flap and the oropharynx, and the presence of a veloped. cricopharyngeal bar, which increased the oropharyn- The tongue is a fundamental organ for normal dy- geal transit time. The patient maintained the nutri- namic swallowing, and it is involved not only in the prepa- tional status. ration of the food and the formation of the bolus but also During follow-up, 1 patient died of cancer recur- in the dynamic pharyngeal phase of swallowing. The un- rence, 2 were alive with recurrence (1 underwent a derstanding of the physiology of swallowing, the se- gastrostomy because of a second primary tumor in quelae resulting from tongue resections, and the pos- the esophagus and 1 had a second primary tumor in the soft palate), and 7 were alive with no evidence of disease. Patients who underwent partial glossectomies showed an increase in oral transit time for paste foods, stasis in the oral cavity (anterior and lateral sulcus and hard and soft palate), a reduction of anteroposterior propulsion of the tongue, and an increase in the number of deglutitions to clear the valleculae (Table 2). Aspiration before deglutition and after penetration was observed in 1 patient who used the supraglottic maneuver of airway protection, the maximization of tongue stump mobility, and the control of the bolus in the oral cavity, which was eventually cleared. The types of maneuvers used were lip protrusion (3 patients) and suction and lowering of the mandible (1 patient). Suction and lowering of the mandible allowed for more participation of the buccinator muscles, which helped to diminish the intraoral space, to increase the intraoral pressure, and, consequently, to eject the food.

COMMENT Figure 1. Video fluoroscopic evaluation of a patient who underwent a total The issue of the functionality of swallowing after a total glossectomy. The image shows stasis in the oral cavity, valleculae, and glossectomy dates from the proposition of the technique superior esophageal sphincter.

Penetration Aspiration

Before During After Before During After Outcome No No No No No No Functional swallowing No No Yes No No No Functional swallowing Yes Yes Yes No No No Functional swallowing No Yes Yes No No No Functional swallowing Yes Yes Yes No No Yes Moderate aspiration No No Yes No No No Functional swallowing No Yes Yes No No No Functional swallowing No No Yes No No Yes Moderate aspiration No No No No No No Functional swallowing No No Yes No No No Functional swallowing No No No No No No Functional swallowing No No No No No No Functional swallowing No No No No No No Functional swallowing No No Yes Yes No No Mild aspiration No No No No No No Functional swallowing

Figure 2. Video fluoroscopic evaluation of a patient who underwent a total glossectomy. The image shows aspiration after swallowing.

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 6 ryngeal characteristics, and an increase in laryngeal elevation. 5 Another frequent compensation found in patients

4 who underwent a total or partial glossectomy was the increase in activity of the lips and the mandible, as Mas- 3 sengill et al11 and Kothary and DeSouza7 previously de- 12 13 Frequency, % Frequency, 2 scribed. Aguilar et al and Logemann et al described the importance of rehabilitation programs involving oral 1 feeding, exercises for oral structure mobility, control of

0 consistency and texture of food, and facilitation of pos- SLP ILP SLS ILS DM RM AM PM LE tures adopted during meals. Compensatory Movements Partial tongue resections with primary closure (the Figure 3. Compensatory movements in patients after undergoing a total suture of the tongue to the floor of the mouth) cause a glossectomy. SLP indicates superior lip protrusion; ILP, inferior lip temporary dysphagia due to edema and/or difficulties in protrusion; SLS, superior lip suction; ILS, inferior lip suction; DM, down triggering the swallowing reflex. In addition to these mandible; RM, retract mandible; AM, anterior mandible; PM, pharyngeal symptoms, we also observed the reduction of tongue movements; and LE, laryngeal elevation. elevation, the anterior and lateral movement of the tongue, and the impairment of speech, mastication, and sible compensatory maneuvers is essential to improve swallowing. Esophageal reconstruction with primary rehabilitation. closure will generate swallowing difficulties during In our study, the main findings regarding swallow- oral transit, such as the accumulation of food in the ing after a glossectomy were the presence of stasis (es- oral cavity, especially in the lateral sulcus, or even the pecially in the flap) of the valleculae, the pharynx, and inability to contain food in the oral cavity using the the SES. Penetration before swallowing is due to alter- lips. We observed the following results: difficulty in ations in oral-motor control; penetration during swal- forming and retaining the food; increase in oral transit lowing indicates inadequate airway closure; and pen- time, especially for paste materials; stasis in the ante- etration after swallowing occurs when there is stasis. rior and lateral sulcus, hard palate, and valleculae; Eight patients were able to clear the occasional penetra- reduction of lingual propulsion; and increase in the tion of food and eliminate the risk of aspiration through number of swallows used in an attempt to clear the compensatory and airway protection maneuvers. valleculae. The compensations developed by patients Although large residues of material accumulated in the who underwent partial glossectomies were similar to oral cavity and the pharynx and inadequate airway pro- the compensations described for patients who under- tection may result in persistent aspirations, aspiration went total glossectomies, that is, using mainly lip pro- was detected in only 2 patients. Materials that accumu- trusion and suction. lated in the oral cavity, owing to the lack of food pro- Cancer and its treatment (surgery, radiotherapy, pulsion, were compensated for by moving the head and/or chemotherapy), especially when involving the backward, which helped with oral clearing because of stomatognathic and respiratory systems, can alter the gravity. In 2 patients, static materials in the oropharyn- voice, the speech, and the swallowing mechanism.14-17 geal region were moved by multiple deglutitions. The Although glossectomies impose limits to the process of Mendelsohn maneuver was used to address specifically deglutition, they still allow, most of the time, for func- the presence of stasis in the SES region because it tional deglutition. The study of swallowing using video enabled an increase in laryngeal elevation and, conse- fluoroscopic evaluation is considered the criterion stan- quently, a longer period of SES opening.8,9 The supra- dard for the diagnosis and planning of treatment of glottic maneuver was proved effective in 8 patients. these patients. Since swallowing is a dynamic and quick Montesi et al2 described similar results in 23 patients process, the possibility of recording the examination on with oral cancer (not only tongue cancer): poor oral videotape guarantees a continuous analysis of limits processing (25%), retention of the bolus in the pharynx and compensations of patients who underwent glossec- (41%), penetration of the bolus in the airway (37%), tomies. and dysfunctional mobility of the SES (9%). The 2 patients with aspiration received preopera- Accepted for publication December 21, 1999. tive radiotherapy: one was 75 years of age and the other Presented at the annual meeting of the American Head excessively used alcohol and did not benefit from the re- and Neck Society, Palm Desert, Calif, April 26, 1999. habilitation program. Pauloski et al10 described a signifi- Reprints: Luiz Paulo Kowalski, MD, Centro de Trata- cant reduction in the oral and pharyngeal phases of swal- mento e Pesquisa Hospital do Caˆncer A. C. Camargo, Rua lowing in patients who underwent radiotherapy. They Professor Antoˆnio Prudente, 211 Liberdade, 01509–010 Sa˜o reported an increase in the oral transit time in materials Paulo, Brazil (e-mail: [email protected]). of paste consistency, a reduction in the efficiency of oropharyngeal swallowing, an increase in pharyngeal resi- REFERENCES due, and a reduction of the opening period of the SES. All patients in the present study underwent radio- 1. Logemann JA. Evaluation and Treatment of Swallowing Disorders. San Diego, therapy except 1 patient who required a shorter reha- Calif: College Hill Press; 1983. bilitation time, had a better compensation of all oropha- 2. Montesi A, Pesaresi A, Serri L, Salmistraro D, Cavalli ML, Segoni A. Dynamic

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