Vertical hemipharyngolaryngectomy for hypopharyngeal cancer arising from the medial side of the right pyriform sinus. The tumor was excised under direct vision through a midline thyrotomy. CA indicates contralateral arytenoids; CV, contralateral vocal cord; IV, ipsilateral vocal cord; and T, tumor.
Operative field after tumor resection. C indicates cricoid cartilage; CA, contralateral arytenoids; CV, contralateral vocal cord; and E, esophagus.
The design of a radial forearm free flap. PL indicates palmaris longus tendon; SN, sensory nerve; and VP, vascular pedicles.
The glottic reconstruction. The palmaris longus tendon has been passed through the hole made in the thyroid-cricoid cartilage. CA indicates contralateral arytenoids; CV, contralateral vocal cord; F, flap; PL(AF), palmaris longus tendon (anterior fixation); and PL(PF), palmaris longus tendon (posterior fixation).
Schematic drawing of the types of vertical hemipharyngolaryngectomy (VHPL) based on the extent of resection. A, Limited VHPL (type I). B, Total VHPL (type II). C, Extended VHPL (type IIIa). D, Extended VHPL (type IIIb).
Kaplan-Meier disease-specific survival curve.
Customize your JAMA Network experience by selecting one or more topics from the list below.
Kim M, Joo Y, Cho K, Park J, Sun D. A Classification System for the Reconstruction of Vertical Hemipharyngolaryngectomy for Hypopharyngeal Squamous Cell Carcinoma. Arch Otolaryngol Head Neck Surg. 2011;137(1):88–94. doi:10.1001/archoto.2010.210
To evaluate microvascular reconstruction of a vertical hemipharyngolaryngectomy (VHPL) defect for hypopharyngeal squamous cell carcinoma.
Retrospective analysis of medical records.
Tertiary care referral center.
Thirty-two patients who underwent a VHPL.
Main Outcome Measures
Assess the surgical technique and safety of VHPL and review the functional parameters of swallowing and decannulation.
The classification was composed of 3 types of VHPL according to the extent of resection: limited VHPL (type I), resection at the lateral border of the conus elasticus to preserve both vocal cords (n = 10); total VHPL (type II), removal of a vertical section of the thyroid cartilage through the anterior commissure to the upper border of the cricoid cartilage with preservation of 1 vocal cord (n = 12); and extended VHPL (type III), inclusion of a supraglottic laryngectomy (type IIIa) (n = 6) or partial cricoid cartilage resection (type IIIb) (n = 4). A radial forearm free flap that included the palmaris longus tendon was used for reconstruction in 31 patients, and an anterolateral thigh flap was used in 1 patient. There was no perioperative mortality, and there was 100% free flap survival. Oral realimentation and tracheotomy weaning were achieved a mean of 33 and 32 days postoperatively, respectively. In 25 patients observed for longer than 6 months, the recurrence rate was 28% (7 of 25), and 5-year disease-specific survival was 64%.
Microvascular reconstruction of VHPL offers a wider resection with promising functional results for hypopharyngeal carcinoma.
Squamous cell carcinomas (SCCs) of the hypopharynx are generally treacherous because they typically have few symptoms until late in the course of the disease. Hypopharyngeal SCC is an aggressive cancer that is generally diagnosed at advanced stages and consequently has a poor prognosis and a low survival rate. The treatment of these tumors is designed to cure the patient of the cancer and to preserve or restore useful laryngeal and hypopharyngeal function. However, the need for extensive ablative surgery often coupled with radiotherapy renders many patients incapable of performing the basic human functions of swallowing and speech.1 Loss of such integral functions has a dramatically negative effect on a patient's quality of life, which is already threatened by the aggressive nature of this disease. Therefore, it is imperative to use a reliable reconstructive strategy with low morbidity that will allow the expedient restoration of speech and swallowing.
Seidenberg et al2 introduced revascularized free visceral flaps for pharyngoesophageal reconstruction in the form of the free jejunal flap in 1959. However, free flaps did not become widely used for hypopharyngeal reconstruction until after microvascular techniques were refined during the 1970s. Harii et al3 described the use of a tubed fasciocutaneous free flap for pharyngoesophageal reconstruction in 1985. The radial forearm fasciocutaneous free flap (RFFF) has been used as a patched graft in cases in which there is insufficient mucosa to achieve primary closure and as a tubed flap for reconstructing circumferential defects of the hypopharynx and cervical esophagus. Gilbert and Neligan4 reviewed the use of free-tissue transfer and vascularized carriers for laryngotracheal reconstruction, including a few trials that had reported successful functional preservation of the laryngopharynx.
The concept of a wide vertical hemipharyngolaryngectomy (VHPL) was first introduced by Chantrain et al5 in 1991. Their proposed procedure combines the resection of laterally localized extended pharyngolaryngeal tumors with immediate microsurgical reconstruction using an RFFF, including the palmaris longus tendon for glottis reconstruction. It eliminates the limitations of resections that are usually performed to avoid difficulty closing the resulting defect. In their study,5 this procedure showed good functional restoration of deglutition and phonation.
The primary objective of the present study was to evaluate the surgical technique and reconstructive method of VHPL according to the extent of hypopharyngeal SCC. In addition, we classified VHPL with immediate glottic and pharyngeal reconstruction according to the defect as a guideline for the clinical application of this procedure and reviewed the functional variables of swallowing and decannulation.
We retrospectively reviewed the records of 32 consecutive patients who underwent VHPL for hypopharyngeal SCC. The VHPL was performed by the senior author (M.-S.K.) between September 1, 1998, and June 30, 2009, at the Department of Otolaryngology–Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul. The diagnostic evaluations at presentation included a complete physical examination, panendoscopy, computed tomography or magnetic resonance imaging of the head and neck, chest radiography, and laboratory tests. We assessed the computed tomographic scans or magnetic resonance images to determine the regional lymph node status. The panendoscopy was mainly performed under general anesthesia, and it consisted of microlaryngoscopy, bronchoscopy, and esophagoscopy. The pharynx and upper esophagus were examined using a rigid hypopharyngoscope. If the inferior margin of the tumor involved the cervical esophagus, we changed the operation from VHPL to total laryngopharyngoesophagectomy. No patient had radiologic evidence of distant metastases at presentation, and all were treated with curative intent. The median patient age was 62.2 years (age range, 46-73 years); there were 31 men and 1 woman. The clinicopathologic profiles of the patients are summarized in Table 1. There were 20 patients (63%) with stage T2 cancer, 10 (31%) with stage T3 cancer, and 2 (6%) with stage T4 cancer. Cervical lymph node metastasis was present in 25 of 32 patients (78%). The patients were staged according to the 2002 American Joint Committee on Cancer staging system. Follow-up ranged from 2 to 112 months (mean, 32.2 months).
En bloc resection was performed through a midline thyrotomy, as reported previously.5 Laryngeal resection was performed under direct vision based on invasion of the tumor according to the classification of VHPL (Figure 1). The resection of the posterior pharyngeal wall was determined by a safe tumor margin of up to two-thirds of the lateral dimension of the pharyngeal wall. The inferior margin could be 2 cm below the upper margin of the cervical esophagus without causing any postoperative functional problems (Figure 2).
An RFFF that included the palmaris longus tendon was used for reconstruction in 31 patients, and an anterolateral thigh flap was used in 1 patient (Figure 3). Microvascular anastomoses were performed end to end with the superior thyroid artery or transverse cervical artery and with the external jugular vein or facial vein. A nerve anastomosis to a sensory branch of the superior laryngeal nerve was performed to restore sensation in 23 patients (72%). The flap was designed to be 1 cm larger than the defect to allow for contraction of the skin paddle before setting the flap with minimal tension and for postoperative radiotherapy. The median flap size was 56.1 cm2 (range, 42-80 cm2). In 22 patients (types II and III), in whom at least 1 side of the laryngopharynx was resected, the glottis was reconstructed using the palmaris longus tendon. Two holes were made in the middle portion, at the same level as the remaining contralateral vocal cord, hemithyroid cartilage, and cricoid cartilage. To create a vocal fold, the tendon was passed through these 2 holes in an anteroposterior direction and was sutured to make a neoglottis covered by a skin paddle, which acted as neomucosa of the larynx (Figure 4). By measuring the movement of the contralateral vocal cord, the proper size of the glottic chink was based on 5- to 6-mm abduction of the vocal cord. The pyriform sinus and posterior pharyngeal wall were reconstructed using the RFFF skin paddle.
The pharyngeal resection was based on the tumor margin. The classification comprised 3 types of VHPL based on the extent of the laryngeal resection (Figure 5): limited VHPL (type I), resection at the lateral border of the conus elasticus to preserve both vocal cords (Figure 5A); total VHPL (type II), removal of a vertical section of the thyroid cartilage through the anterior commissure to the upper border of the cricoid cartilage (Figure 5B); and extended VHPL (type III), inclusion of a supraglottic laryngectomy (type IIIa) (Figure 5C) or partial cricoid cartilage resection (type IIIb) (Figure 5D). The surgical procedures included 10 type I (31%), 12 type II (38%), 6 type IIIa (19%), and 4 type IIIb (13%) VHPLs.
There was no perioperative mortality, and there was 100% free flap survival. One patient required surgical reexploration for vascular compromise. In this series, the final resection margins were negative in the postoperative pathologic examination in 28 patients (88%). Full-dose postoperative irradiation or chemotherapy was indicated for 21 patients (66%). Twenty-five patients had longer than 6 months of follow-up, with a mean time of 34.6 months. Five-year disease-specific survival was 64% (Figure 6). After ablative surgery, 7 patients (28%) had recurrences, including 2 local, 1 regional, and 4 distant metastases. Of the 2 patients who had local recurrences, one received chemotherapy but died of the disease; the other patient underwent laser excision and radiotherapy and had no evident disease 6 months after laser excision and radiotherapy. The patient with regional recurrence died of the disease, and all the patients with distant metastases died of the disease.
Two patients (6%) developed glottic stenosis associated with the procedure. Two patients (6%) developed marginal necrosis of the flap, which resulted in pharyngocutaneous fistulas that were managed by healing with secondary intention after debriding the necrotic tissue in the flap. There were no enteric strictures related to the fistulas.
The functional outcome for swallowing and decannulation was analyzed (Table 2). The swallowing act of the 32 patients was evaluated by using videofluoroscopy 12 to 21 days postoperatively. The patients who underwent VHPL, except for 12 patients who had serious aspiration, had effective and near-normal swallowing. Finally, 28 patients (88%) could obtain all their nutritional needs orally, but 4 patients needed the assistance of a percutaneous endoscopic gastrostomy tube. Oral realimentation was achieved a mean of 33.0 days postoperatively: type I VHPL, 21.7 days (range, 10-28 days); type II VHPL, 35.9 days (range, 14-51 days); type IIIa VHPL, 35.6 days (range, 15-91 days); and type IIIb VHPL, 36.0 days (range, 23-47 days). Twenty-eight patients (88%) could be decannulated, whereas 4 patients required a tracheotomy tube. Tracheotomy weaning was achieved a mean of 63.7 days postoperatively. However, excluding patients with airway edema due to postoperative radiotherapy who needed to keep the tracheotomy tube until the end of radiotherapy, decannulation was possible by 31.9 days postoperatively: type I VHPL, 20.8 days (range, 13-28 days), type II VHPL, 32.0 days (range, 24-43 days), type IIIa VHPL, 56.3 days (range, 26-99 days), and type IIIb VHPL, 58.0 days (range, 38-86 days). There was no significant difference in the success of oral feeding (P > .33). Only decannulation time in type I VHPL was significantly faster than that in type II VHPL (P = .048).
Hypopharyngeal SCC is an aggressive cancer that is generally diagnosed at advanced stages and consequently has a poor prognosis and a low survival rate. Total laryngopharyngectomy with adjuvant radiotherapy remains the most widely used treatment in cases of late-stage disease.6 However, the resulting permanent tracheostoma with the associated loss of voice and impaired deglutition accounts for significant postoperative morbidity. Conservation surgery is rarely considered suitable in hypopharyngeal SCC for either oncologic reasons or patient factors, such as inadequate pulmonary reserve and postoperative swallowing disorders. Nevertheless, Plouin-Gaudon et al7 reported that 5-year overall survival was 50% and disease-specific survival was 65%, and successful laryngeal function preservation with local control was achieved in 80% of patients with selected pyriform sinus cancer.
Pharyngolaryngeal reconstruction remains a challenge for the head and neck surgeon. Lefebvre8 stressed the possibility of function preservation surgery for advanced laryngopharyngeal cancer even in selected patients with rare indications. Surgical reconstruction should be measured by the ability to reestablish the patient's ability to speak and swallow quickly. During the past 50 years, several pharyngolaryngeal reconstruction methods have been developed. The myocutaneous flap, gastric pull-up, and jejunal free flap techniques are the most popular contemporary methods of pharyngolaryngeal reconstruction. Disa et al9 reported the use of microvascular reconstruction of the hypopharynx according to the defect classification and suggested a treatment algorithm. However, their report was for hypopharyngeal reconstruction only and not for laryngeal reconstruction. Of the various methods, the radial forearm fasciocutaneous free flap offers some potential advantages over the other reconstruction methods.10 It has thin, long vascular pedicles and is a reliable flap. It can be easily used in procedures and can be performed with a 2-team approach. Another advantage is the addition of a sensory component via the antebrachial cutaneous nerve, which is harvested as a composite flap with the palmaris longus tendon and improves functional reconstruction.
The most challenging problem in all partial laryngectomies is glottic insufficiency resulting from partial or subtotal removal of the laryngeal sphincter.10,11 Such insufficiency is responsible for temporary or definitive speech and swallowing disorders. Functional perturbations and, consequently, rehabilitation parallel the extension of the resection. Therefore, when the glottic plane is resected, all techniques that produce a reduced tracheal inlet can lead to better functional results. Only a few trials have reconstructed the larynx using free flaps after partial laryngopharyngectomy. Chantrain et al5,11 reported wide VHPL with immediate glottis and pharyngeal reconstruction using a radial forearm flap, but they examined only 4 patients and did not report the long-term follow-up or functional results. Urken et al12 used the forearm free flap and a costochondral cartilage graft for reconstruction of hemicricoid and hemilaryngopharyngectomy defects. In their series, half of the patients developed fistulas, and the swallowing results were not addressed. In 1994 and 1997, Delaere et al13,14 introduced the concept of vascularized carriers for laryngopharyngeal reconstruction. They focused on creating a vascularized segment of autologous trachea with a vascularized facial free flap in a 1-stage procedure. Nakatsuka et al15 reported the successful preservation of the larynx after resecting the posterior pharyngeal wall of the hypopharynx, but that procedure is possible only when the tumor has not invaded the larynx; furthermore, they did not comment on the laryngeal reconstruction. Compared with these techniques, VHPL is a simple 1-stage procedure, and reconstruction requires only an RFFF composite flap. In addition, this procedure enables physiologic speech and swallowing without a permanent tracheostoma.
By improving the surgical technique and accumulating experiences with VHPL, we should be able to modify this procedure according to the extent of the primary tumor, with the goal of preserving laryngeal function. With a type I VHPL, both vocal cords are preserved. For a type I VHPL, tumor involving on 1 side of the pyriform sinus and minimally invading the larynx, the resection can be made lateral to the conus elasticus with no need for glottic reconstruction. In type II and III VHPLs, at least 1 side of the entire hemilarynx vertically and parts of the pharynx and cervical esophagus are resected. In such cases, we need to reconstruct a neoglottis. The palmaris longus tendon is used as the frame for the neoglottis, acting like a vocal ligament, and a skin paddle is used to cover the tendon, similar to the mucosa covering the vocal ligament, as reported previously.5
To successfully re-create the glottic plane and sphincter function, we followed several principles: (1) ensure adequate support for the glottic chink with a tendon of sufficient tension, (2) make a chink of proper size on the neoglottis to allow complete closure and prevent aspiration, (3) preserve a patent airway with a neoglottic chink of proper size (approximately 5-6 mm), and (4) attempt to make an anterior commissure in the neoglottis, not only for good shape but also for better functional results. Other important points in laryngeal reconstruction are maintaining the height of the posterior buttress at the level of the arytenoid cartilage on the normal side and avoiding a straight suture line by making a Z-plasty to prevent a stricture on closing of the pharyngoesophagus with the flap.
A VHPL allows the resection of advanced lateralized laryngeal tumors extending to the arytenoid cartilage and advanced lateralized hypopharyngeal tumors extending to the laryngeal wall of the pyriform sinus, even with arytenoid fixation (T3) or extension to the thyroid cartilage (T4) in selected patients. It offers a wider resection for hypopharyngeal SCC invading the larynx, with promising functional results. Compared with a total pharyngolaryngectomy, a VHPL allows wide resection of advanced tumors with similarly safe hypopharyngeal and lingual margins. In this series, the resection margins were positive in 4 patients (13%) who had T4a (n = 1), T3 (n = 2), and T2 (n = 1) lesions. Three patients received postoperative irradiation or chemotherapy, and 1 patient refused radiotherapy. Of the 4 patients who had positive margins, 2 died of the disease, and 2 had no evident disease.
Scharpf and Esclamado16 analyzed recurrence and survival after hypopharyngeal ablative surgery with RFFF reconstruction without laryngeal preservation in 28 patients. In a median 20-month follow-up period, there were 14 recurrences (50.0%): 4 distant, 5 local, 4 regional, and 1 regional and distant. In the present study, it is difficult to analyze the oncologic results owing to short follow-up periods. However, during a mean follow-up of 32.2 months, there were recurrences in 7 patients. Of the 6 patients with T2N0M0 tumor, 2 died of disease. One patient with positive resection margins did not receive radiotherapy and had local recurrence; the other patient had distant metastases. Five-year disease-specific survival was 64%. With the limited follow-up (12 patients were observed for <12 months), the results suggest that hypopharyngeal ablative surgery with preservation of the larynx does not have any harmful effects in terms of disease recurrence.
The good functional outcome in the present experience attests to the value of this technique. A VHPL satisfies the requisite outcome of expedient restoration of swallowing and decannulation. Some patients tolerated oral feeding with a soft diet, although they might have experienced occasional aspiration episodes in the first 3 postoperative months. Therefore, good pulmonary function reserve, motivation, and psychological support are important factors for patients undergoing swallowing rehabilitation.
Although the use of organ preservation with concurrent chemoradiotherapy to treat advanced head and neck cancers has become more popular in recent years, radical surgery with postoperative radiotherapy or concurrent chemoradiotherapy is still the standard treatment for hypopharyngeal SCC in many institutions, especially for patients with advanced T3-T4 disease, in whom cure with concurrent chemoradiotherapy will likely result in tracheostomy or feeding tube dependence. At The Catholic University of Korea, in principle, the choice of radical therapies is surgery, including partial pharyngectomy, and neck lymph node metastasis is treated by means of neck dissection. Postoperative irradiation or chemotherapy is conducted in patients with multiple lymph node metastases. The present study demonstrates excellent oncologic and functional outcomes with primary surgery for the treatment of hypopharyngeal SCC. We think that surgery offers the best opportunity to identify patients in whom postoperative irradiation or chemotherapy may be most appropriately applied.
There were some limitations in this study. The main limitation was the retrospective analysis. A second limitation was the small number of patients who received VHPL for hypopharyngeal SCC. Third, patients with hypopharyngeal SCC at different T categories were not equally distributed. Last, the median follow-up time of this study was rather short. It was thought that there were limitations of the overall and disease-specific survival data.
In conclusion, VHPL offers a wider resection with promising functional results in hypopharyngeal SCC, and the present classification of VHPL based on the extent of the tumor offers guidelines for better functional reconstruction.
Correspondence: Min-Sik Kim, MD, PhD, Department of Otolaryngology–Head and Neck Surgery, Seoul St Mary's Hospital, Banpo-dong Seocho-gu 505, The Catholic University of Korea, Seoul, Korea 137-040 (firstname.lastname@example.org).
Submitted for Publication: March 31, 2010; final revision received May 27, 2010; accepted July 22, 2010.
Author Contributions: All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Kim and Joo. Acquisition of data: Kim, Joo, Park, and Sun. Analysis and interpretation of data: Kim and Cho. Drafting of the manuscript: Kim, Joo, Cho, Park, and Sun. Critical revision of the manuscript for important intellectual content: Kim. Statistical analysis: Kim, Joo, Cho, Park, and Sun. Obtained funding: Kim. Administrative, technical, and material support: Kim. Study supervision: Kim.
Financial Disclosure: None reported.
Previous Presentations: This study was presented at the American Head and Neck Society Annual Meeting; April 28, 2010; Las Vegas, Nevada.