TY - JOUR
AU - Daiko, Hiroyuki
AB - Abstract Hybrid endoscopy-assisted larynx-preserving esophagectomy is developed for cervical esophageal squamous cell carcinoma encroaching or extending above the upper esophageal sphincter. First, a cervical incision was surgically performed followed by cervical lymph node dissection. Second, the margin of cervical esophageal squamous cell carcinoma was endoscopically identified with iodine staining and marked endoscopically followed by semi-circumferential or circumferential endoscopic full-thickness excision around the lumen of the esophagus. The distal margin was surgically resected and reconstruction was performed. Among six consecutive patients with cervical esophageal squamous cell carcinoma undergoing hybrid endoscopy-assisted larynx-preserving esophagectomy, proximal surgical margin was histologically negative in five patients. During a median follow-up period of 15.5 months, all patients tolerated oral intake and were alive without evidence of recurrence. None of the patients experienced aspiration pneumonia, vocal disorder or postoperative anastomotic stricture. Hybrid endoscopy-assisted larynx-preserving esophagectomy could be a clinically feasible treatment for cervical esophageal squamous cell carcinoma providing accurate proximal resection margin with the benefit of laryngeal function preservation. cervical esophagus, squamous cell carcinoma, endoscopic resection, esophagectomy, larynx-preserving surgery Introduction Cervical esophageal cancer located between the cricoid cartilage and thoracic inlet is relatively rare, accounting for ~5% of all esophageal cancers (1, 2). The most common histopathological type of cervical esophageal cancer is squamous cell carcinoma, accounting for >90% of cervical esophageal cancer in the surveillance, epidemiology and end results database in the United States (3). Treatment of cervical esophageal squamous cell carcinoma (CESCC) differs from that of thoracic esophageal cancer because of the complicated anatomical structures around the cervical esophagus. Both surgical treatment and non-surgical treatment have been reported, and the optimal approach remains controversial (4–7). Cervical esophagectomy for invasive CESCC is the mainstay among available therapeutic modalities, similar to that for cervical esophageal adenocarcinoma (8, 9). However, disadvantage of cervical esophagectomy is that combined laryngectomy (laryngopharyngoesophagectomy) is often required for patients with tumors invading the pharynx, larynx and trachea. This may be required even for patients without direct pharyngeal invasion, in whom sufficient preservation of the esophagus to perform anastomosis with intestinal graft is difficult. Markedly reduced quality of life due to vocal and swallowing disorders poses a serious problem in patients undergoing combined laryngectomy. Daiko et al. (8) reported the postoperative complications and death in cervical esophagectomy were comparable to that of total laryngopharyngoesophagectomy. Thus, taking into consideration of the quality of life and surgical outcome, larynx-preserving surgery is preferred for patients in whom the tumor has not invaded the larynx, or trachea (10–14). However, it is challenging to identify the proximal margin of CESCC precisely during surgery. The usual methods for determining the proximal excision line, such as tumor palpation and/or oral margin clip palpation, can be unsatisfactory, particularly in lesions located in proximity to the upper esophageal sphincter. A rapid pathological diagnosis can be performed during surgery to ensure a carcinoma-free cut-end, but it is time-consuming. Given the background, our institution developed hybrid endoscopy-assisted larynx-preserving esophagectomy (HELP-E). This study aimed to evaluate the technical and clinical feasibility of HELP-E in patients with CESCC near the upper esophageal sphincter. Methods Patients This study included consecutive patients with CESCC undergoing HELP-E between August 2018 and March 2020. The depth of invasion was diagnosed with high definition esophagoscopy, and magnified endoscopy was performed as necessary. Enhanced computed tomography (CT) was used to stage lymph node metastasis. We proposed both options of surgery and chemoradiotherapy to all patients with CESCC, and the treatment strategy was determined by our multidisciplinary conference. The clinical indications for HELP-E were as follows: (i) a histologically proven CESCC extending close to the upper esophageal sphincter or invading hypopharynx, (ii) no direct invasion of larynx and trachea on CT scan and (iii) no intramural metastasis or submucosal extension proximally detected during preoperative esophagoscopy. Neoadjuvant chemotherapy was carried out if CT scan was positive for nodal metastasis (15). The clinical stage was classified according to the Union for International Cancer Control tumor-node-metastasis classification (seventh edition). This study was approved by the institutional review board in our hospital. Written informed consent was obtained from all patients. Hybrid endoscopy-assisted larynx-preserving esophagectomy HELP-E is a surgical and endoscopic collaborative approach during surgery to preserve the laryngeal function (Fig. 1; Supplementary Material, Video 1). HELP-E utilizes endoscopic full-thickness excision techniques to achieve minimal proximal margin of CESCC during open cervical esophagectomy. The general procedures are shown as follows: (i) First, in those where the distal tumor margin is limited to within the cervical esophagus, the distal margin of a CESCC is surgically excised at the level of upper thoracic esophagus. Subtotal esophagectomy can also be performed prior to cervical esophagectomy when the tumor has invaded the thoracic esophagus, or when there are multiple lesions in the thoracic esophagus. (ii) A left cervical incision is surgically performed. Superior mediastinal lymph node accessible from the cervical incision is dissected. As per standard cervical esophagectomy, cervical paraesophageal lymph nodes from either sides of the cervical esophagus are cleared. (iii) A curved rigid laryngoscope (Nagashima Medical Instruments Company, Ltd., Tokyo, Japan), which can display an open view of the hypopharynx as well as the upper esophageal sphincter, was used by an otolaryngologist. (iv) An endoscopist introduces a flexible gastroscope (GIF-260J, Olympus Medical, Japan) perorally and identifies the CESCC with chromoendoscopy using iodine staining. Endoscopic markings are made with the use of Dual knife J (KD-665U, Olympus Medical, Japan) 2 mm above the proximal margin of the CESCC. (v) Circumferential or semi-circumferential endoscopic full-thickness excision is performed around the markings with a needle knife (KD-1L-1, Olympus Medical, Japan), and then extended with IT-2 knife (KD-611L, Olympus Medical, Japan) under the guidance and tissue traction by the operating surgeon. After partial excision, the remaining tissue proximal to the resected lesion is pulled distally with the use of nylon sutures for anastomosis reconstruction. During endoscopic full-thickness excision, the insulated tip of IT-2 knife can be identified extraluminally from the open surgical field. In the case of semi-circumferential excision, the resection of the proximal margin is surgically completed and guided under direct endoscopic observation. (vi) After circumferential excision of the proximal side, either a free jejunum or gastric tube reconstruction is performed at the discretion of the operating surgeon. All procedures were performed by qualified expert esophageal surgeons of the Japan Esophageal Society and a qualified expert endoscopist of the Japanese Gastroenterological Endoscopy Society. Figure 1. Open in new tabDownload slide HELP-E for CESCC. (A) Preoperative esophagoscopy showed a shallow depressed lesion on the left wall of the cervical esophagus endoscopically 1 cm from upper esophageal sphincter. (B) Chromoendoscopy with iodine staining revealed a lugol-voiding lesion with distinct margin. A targeted biopsy revealed squamous cell carcinoma. (C) Left cervical incision. (D) Endoscopic marking 2 mm away from the proximal border of the lesion. (E) Endoscopic full-thickness excision was performed using needle knife and IT-2 knife near esophageal sphincter. (F) The endoscopic luminal excision was extended under guidance and tissue traction by surgeon. (G) Circumferential endoscopic excision was completed. Thereafter, free jejunum reconstruction was performed. (H) The resected specimen with iodine staining. (I) The resected specimen histologically revealed 7 by 5 mm, 0-IIc, pT1b-SM3, pN0, M0, free proximal and distal margin. Figure 1. Open in new tabDownload slide HELP-E for CESCC. (A) Preoperative esophagoscopy showed a shallow depressed lesion on the left wall of the cervical esophagus endoscopically 1 cm from upper esophageal sphincter. (B) Chromoendoscopy with iodine staining revealed a lugol-voiding lesion with distinct margin. A targeted biopsy revealed squamous cell carcinoma. (C) Left cervical incision. (D) Endoscopic marking 2 mm away from the proximal border of the lesion. (E) Endoscopic full-thickness excision was performed using needle knife and IT-2 knife near esophageal sphincter. (F) The endoscopic luminal excision was extended under guidance and tissue traction by surgeon. (G) Circumferential endoscopic excision was completed. Thereafter, free jejunum reconstruction was performed. (H) The resected specimen with iodine staining. (I) The resected specimen histologically revealed 7 by 5 mm, 0-IIc, pT1b-SM3, pN0, M0, free proximal and distal margin. Follow-up and assessment This study assessed the treatment outcomes and adverse events of HELP-E. Vocal and swallowing function after HELP-E were assessed at scheduled follow-up outpatient clinic. Surveillance with esophagogastroduodenoscopy and CT scan was performed 6 and 12 months following HELP-E. Results A total of 20 patients underwent cervical esophagectomy including total laryngoesophagectomy between August 2018 and March 2020. Among them, six consecutive patients with CESCC meeting the indications underwent HELP-E (Table 1). They consisted of one male and five female patients with a median age of 68.5 (range 55–75) years. Four patients had clinical stage IA cancer, one had stage IIB cancer and one with stage IIIA cancer. Five patients had CESCC encroaching within 1 cm of the upper esophageal sphincter endoscopically and one had CESCC with superficial invasion of the hypopharynx. Neoadjuvant chemotherapy was performed in two patients with clinical lymph node metastasis on CT scan. One patient received 5-fluorouracil plus cisplatin and the other received 5-fluorouracil, docetaxel and cisplatin (Case 3 and Case 6, respectively). Endoscopic resection was not performed in two patients; one had cT1a CESCC with multiple synchronous invasive thoracic esophageal cancer (Case 1) and the other had extensive cT1a-MM superficial CESCC involving the entire luminal circumference, which was 40 mm in length endoscopically (Case 2). Semi-circumferential endoscopic excision was performed in four patients and circumferential endoscopic resection was completed in two patients. In one patient with CESCC superficially invading the hypopharynx (Case 4, Type 0-IIb+ Is, cT1b-SM2), a semi-circumferential endoscopic excision was made at the proximal markings to ensure maximum space and adequate tissue remnant for surgical reconstruction. In terms of the surgical outcome, cervical esophagectomy was performed in four patients. Subtotal esophagectomy was performed in two patients (Case 1 and 5) who had multiple lesions in the thoracic esophagus. Free jejunal reconstruction was performed in four patients and a gastric tube was placed in two patients. As for intraoperative complication, minor injury of the tracheal membrane occurred in one patient and a temporal mini-tracheostomy was performed (Case 2) (Table 1). Table 1 Surgical and histological results Case . year . Gender . Surgery . Reconstruction . Size, mm . Macroscopic type . pT . pN . PM . ly . v . 1a 59 F Subtotal esophagectomy Gastric tube 8 Type 0-IIc T1a-LPM 0 0 0 0 2b 75 F Cervical esophagectomy Free jejunum 45 Type 0-IIc T1a-LPM 0 0 0 0 3 55 F Cervical esophagectomy Free jejunum 7 Type 0-IIc T1b-SM3 0 0 0 0 4 70 F Cervical esophagectomy Free jejunum 25 Type 0-IIb+Is T1b-SM2 0 1 0 0 5c 67 F Subtotal esophagectomy Gastric tube 17 Type 0-IIc T1b-SM2 0 0 0 0 6 70 M Cervical esophagectomy Free jejunum 43 Type 2 T3 1 0 0 1 Case . year . Gender . Surgery . Reconstruction . Size, mm . Macroscopic type . pT . pN . PM . ly . v . 1a 59 F Subtotal esophagectomy Gastric tube 8 Type 0-IIc T1a-LPM 0 0 0 0 2b 75 F Cervical esophagectomy Free jejunum 45 Type 0-IIc T1a-LPM 0 0 0 0 3 55 F Cervical esophagectomy Free jejunum 7 Type 0-IIc T1b-SM3 0 0 0 0 4 70 F Cervical esophagectomy Free jejunum 25 Type 0-IIb+Is T1b-SM2 0 1 0 0 5c 67 F Subtotal esophagectomy Gastric tube 17 Type 0-IIc T1b-SM2 0 0 0 0 6 70 M Cervical esophagectomy Free jejunum 43 Type 2 T3 1 0 0 1 PM: proximal margin, ly: lymphatic invasion, v: venous inavsion aA CESCC with multiple thoracic invasive esophageal cancers. bA CESCC involving complete luminal circumference. cA CESCC with a thoracic superficial esophageal cancer. Open in new tab Table 1 Surgical and histological results Case . year . Gender . Surgery . Reconstruction . Size, mm . Macroscopic type . pT . pN . PM . ly . v . 1a 59 F Subtotal esophagectomy Gastric tube 8 Type 0-IIc T1a-LPM 0 0 0 0 2b 75 F Cervical esophagectomy Free jejunum 45 Type 0-IIc T1a-LPM 0 0 0 0 3 55 F Cervical esophagectomy Free jejunum 7 Type 0-IIc T1b-SM3 0 0 0 0 4 70 F Cervical esophagectomy Free jejunum 25 Type 0-IIb+Is T1b-SM2 0 1 0 0 5c 67 F Subtotal esophagectomy Gastric tube 17 Type 0-IIc T1b-SM2 0 0 0 0 6 70 M Cervical esophagectomy Free jejunum 43 Type 2 T3 1 0 0 1 Case . year . Gender . Surgery . Reconstruction . Size, mm . Macroscopic type . pT . pN . PM . ly . v . 1a 59 F Subtotal esophagectomy Gastric tube 8 Type 0-IIc T1a-LPM 0 0 0 0 2b 75 F Cervical esophagectomy Free jejunum 45 Type 0-IIc T1a-LPM 0 0 0 0 3 55 F Cervical esophagectomy Free jejunum 7 Type 0-IIc T1b-SM3 0 0 0 0 4 70 F Cervical esophagectomy Free jejunum 25 Type 0-IIb+Is T1b-SM2 0 1 0 0 5c 67 F Subtotal esophagectomy Gastric tube 17 Type 0-IIc T1b-SM2 0 0 0 0 6 70 M Cervical esophagectomy Free jejunum 43 Type 2 T3 1 0 0 1 PM: proximal margin, ly: lymphatic invasion, v: venous inavsion aA CESCC with multiple thoracic invasive esophageal cancers. bA CESCC involving complete luminal circumference. cA CESCC with a thoracic superficial esophageal cancer. Open in new tab Histologically, proximal surgical margin was negative in five patients and positive in the patient with CESCC superficially invading the hypopharynx in whom the proximal endoscopic excision was made at the markings (Table 1). In terms of the postoperative morbidities, emergency surgery was required due to jejunal graft thrombosis in one patient. None of the patients experienced nerve paralysis. All patients could tolerate oral intake without requiring tube feeding during the median hospital stay of 14.5 (range 10–19) days. After a median follow-up period of 15.5 (range 4–20) months, all patients were alive without local and distant recurrence. None of the patients developed aspiration pneumonia, postoperative anastomotic stricture or dysphagia. Discussion This case series demonstrated the efficacy of HELP-E for CESCC encroaching or extending above the upper esophageal sphincter. The proximal margin could be easily identified by flexible endoscopic approach with iodine staining similar to standard endoscopic resection, which allowed the proximal excision line to be clearly determined during cervical esophagectomy. Laryngeal function such as vocalization and swallowing could be preserved in all patients without any local or distant metastasis. Recently, endoscopic full-thickness resection has been developed as a novel minimally invasive local resection of gastric subepithelial tumors with minimal margin (16, 17). Favorable short- and long-term outcomes of laparoscopic and endoscopic collaborative surgery (LECS) were demonstrated (18, 19). We applied the concept to the described hybrid esophagectomy to ensure minimal yet adequate proximal excision and laryngeal function preservation. To the best of our knowledge, this is the first report of cervical esophagectomy combined with endoscopic full-thickness excision. There were several publications of larynx-preserving surgery for CESCC, particularly in cancer invasion of the hypopharynx (10–14). Generally, it is challenging to precisely determine the proximal margin during a larynx-preserving surgery. Among these studies, Nakajima et al. (13) utilized a transnasal ultrathin endoscopic examination with iodine staining using a curved rigid laryngoscope. Although a transnasal endoscope is ideal for endoscopic examination within the limited space of the hypopharynx and cervical esophagus, it is solely for endoscopic guidance during surgery and another device is required for the proximal excision. Watanabe et al. (14) reported the efficacy of hybrid larynx-preserving surgery with endoscopic laryngopharyngeal surgery (ELPS) and open surgery. ELPS is a minimally invasive transoral surgery for superficial pharyngolaryngeal cancer using a curved laryngeal forceps and a curved electrosurgical needle knife under the guidance of flexible endoscope (20). Although ELPS is a feasible procedure, allowing for proximal margin identification and pharyngeal mucosa and muscle dissection, the curved forceps and needle knife cannot gain access to the cervical esophagus through the upper esophageal sphincter. Thus, our flexible endoscopic approach is thought to be more reasonable and technically less demanding than ELPS for hybrid surgery for CESCC without pharyngeal invasion. The following two factors are important in larynx-preserving surgery: the proximal resection margin of the CESSC must be accurate, and sufficient swallowing preserved to prevent postoperative aspiration pneumonia (10, 11). When determining the proximal margin, there is no clear evidence of optimal margin. Because CESCC frequently extends submucosally upwards to involve the hypopharynx, a proximal surgical margin of at least 2–3 cm is reported to be necessary (11). Thus, preoperative evaluation of the proximal margin is essential, and careful patient selection is desirable. It is necessary to confirm superficial invasion of the proximal side on preoperative endoscopy, and HELP-E is contraindicated for CESCC with marked subepithelial extension. Also, the proximal margin could become indistinct after neoadjuvant chemotherapy. Thus, detailed endoscopic evaluation is essential before neoadjuvant treatment to measure the distance between the proximal margin and the upper esophageal sphincter. The indication for HELP-E should be discussed and determined before neoadjuvant chemotherapy in a multidisciplinary conference. In our case series, the proximal margin was histologically positive in one CESCC with superficial invasion of the pharynx. Based on our previous experience, we were unlikely to experience local recurrence after pharyngeal and esophageal endoscopic submucosal dissection (ESD) with minimal margin. Therefore, we intentionally marked and resected the proximal edge to minimize the resection area of hypopharynx (21, 22). We believe it is clinically acceptable to perform the endoscopic proximal excision at the marking for superficial pharyngeal extension. Another important issue is the prevention of postoperative complication. Kadota et al. (11) reported that free jejunal reconstruction may decrease postoperative aspiration because the function of the lower esophageal sphincter is preserved, and the free jejunum can work as a valve to prevent reflux of digestive fluid. Shiozaki et al. (10) reported that the combination of laryngeal suspension and cricopharyngeal myotomy was effective. To ensure an adequate margin, preoperative chemotherapy or chemoradiotherapy is recommended. On the other hand, preoperative radiotherapy or chemoradiotherapy is a known risk factor for wound complications such as pharyngocutaneous fistulas in patients with head and neck cancers (23–25). Furthermore, Watanabe et al. (14) raised the issue that adjuvant radiotherapy to the larynx after larynx-preserving surgery would increase the risk of developing postoperative dysphagia. Because postoperative complication can cause fatal infection or aspiration pneumonia, HELP-E is contraindicated for patients undergoing preoperative radiotherapy. Although one patient received neoadjuvant chemotherapy in this study, further investigations are warranted to assess the risk and benefit of neoadjuvant and adjuvant chemotherapy in the study subjects. The comparison of treatment outcomes of CESCC between surgery and definitive chemoradiotherapy remains controversial (5–7, 13). In our study, none of the patients experienced aspiration pneumonia or required tracheotomy. However, some studies reported that permanent tracheotomy may be required (13). Selection among the available treatment options should be made with due consideration given to quality life of the patients, and the advantage and disadvantage of each treatment option. With regard to the quality of life in the patients who received chemoradiotherapy, the prolonged pharyngeal pain and the accompanying difficulty in swallowing also lead to poor quality of life. A retrospective comparative study showed that there was no significant difference in the short-term and long-term quality of life achieved between the two treatment options (26). In addition, an extensive ESD has been regarded as an acceptable treatment, as the strategy for prevention of post-ESD stricture developed over time (27, 28). However, ESD performed for lesions located in the cervical esophagus is a risk factor of post-ESD stricture refractory to steroid treatment (29). Given the high-risk of post-ESD stricture owing to narrow luminal space, HELP-E is a valuable alternative for an extensive superficial CESCC involving the entire luminal circumference. This study has several limitations. First, the study was a single-center retrospective study with a small sample size. In addition, the follow-up period was relatively short for evaluating treatment outcomes. Moreover, HELP-E was performed in collaboration between expert esophageal surgeons and endoscopist. Further prospective studies are warranted to evaluate treatment outcomes of HELP-E and the optimal clinical indication for CESCC located in proximity to the upper esophageal sphincter or invading the hypopharynx. In conclusion, HELP-E could be a clinically feasible treatment for CESCC providing accurate proximal resection margin with the benefit of laryngeal function preservation. Author contributions S.A.: Conception, data collection and drafting of the article. J.O., S.N., H.S., S.Y., I.O. and Y.S.: Critical revision of the article for important intellectual content. H.D.: Conception, critical revision of the article for important intellectual content and final approval of the article. Acknowledgements We thank Dr Shih Yea Sylvia Wu for her kind support of this article. Funding None. 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Endosc Int Open 2017 ; 5 : E736 – e41 . Google Scholar PubMed OpenURL Placeholder Text WorldCat © The Author(s) 2021. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Novel hybrid endoscopy-assisted larynx-preserving esophagectomy for cervical esophageal cancer (with video)
JF - Japanese Journal of Clinical Oncology
DO - 10.1093/jjco/hyab045
DA - 2021-04-14
UR - https://www.deepdyve.com/lp/oxford-university-press/novel-hybrid-endoscopy-assisted-larynx-preserving-esophagectomy-for-WIgQOdMgt3
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -