Transoral en bloc resection of superficial laryngeal and pharyngeal cancers

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1 ORIGINAL ARTICLE Transoral en bloc resection of superficial laryngeal and pharyngeal cancers Kenji Okami, MD, PhD, 1 * Koji Ebisumoto, MD, 1 Akihiro Sakai, MD, 1 Ryousuke Sugimoto, MD, 1 Daisuke Maki, MD, 1 Kosuke Saito, MD, 1 Shoji Kaneda, MD, 1 Masahiro Iida, MD, PhD, 1 Go Ogura, MD, PhD, 2 Naoya Nakamura, MD, PhD, 2 Koichiro Nishiyama, MD, PhD 1,3 1 Department of Otolaryngology, Tokai University, Isehara, Japan, 2 Department of Pathology, Tokai University, Isehara, Japan, 3 Nishiyama ENT Clinic, Yokohama, Japan. Accepted 25 May 2012 Published online 13 September 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. The objective of this study was to evaluate the efficacy and safety of minimally invasive transoral en bloc resection of superficial pharyngeal and laryngeal cancers. Methods. Forty-one superficial lesions (from 35 patients) were resected transorally under a surgical microscope using a monopolar cautery. Quality of life (QOL) was assessed using a questionnaire European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Head and Neck Cancer Module (EORTC QLQ-H&N35) 1 year after the surgery. Results. Twenty-eight hypopharyngeal, 5 oropharyngeal, and 8 laryngeal cancers were operated on using this method. The surgical field was widely exposed with a wide-caliber scope or extending laryngoscope. A bimanual procedure under a surgical microscope enabled us to achieve en bloc resection. The local control rate was 98%. No postoperative dyspnea or dysphagia was observed. Postoperative QOL scores were favorable. Conclusions. Our transoral en bloc resection technique can be easily adopted, and it effectively maintained QOL after treatment. VC 2012 Wiley Periodicals, Inc. Head Neck 35: , 2013 KEY WORDS: laryngeal functional preservation, minimally invasive surgery, transoral resection, endoscopic surgery, partial pharyngectomy INTRODUCTION The key to improving the prognosis of head and neck cancers is early detection of the primary cancer and treatment using minimally invasive surgery. 1 Early detection contributes to a reduction in morbidity and mortality. Despite the basic research for the cancer detection by molecular research, 1,2 the diagnosis at an early stage of head and neck cancer is still a matter of concern. Screening of high-risk patients, such as patients with esophageal cancer, is very important for early detection. About 10% to 15% of Japanese patients with esophageal cancer develop double primary cancer in the head and neck region. New optical devices, such as the Narrow Band Imaging (NBI) endoscopic system, which have been recently developed, have enabled us to detect early superficial lesions. 3 For such superficial lesions, minimally invasive surgery can be performed for organ and functional preservation. Transoral tumor resection is an option that achieves this purpose. Several minimally invasive surgeries have been recently reported. 4 7 In this report we introduce a new surgical technique for the en bloc resection of superficial pharyngeal and laryngeal cancers. The objective of this study was to evaluate the efficacy and safety of our technique. Postoperative quality of life (QOL) was also determined to evaluate functional preservation. *Corresponding author: K. Okami, Department of Otolaryngology, Tokai University, Isehara, Japan. okami@is.icc.u-tokai.ac.jp PATIENTS AND METHODS From 2008 to 2010, transoral en bloc resection was performed for 41 superficial pharyngeal and laryngeal cancers in 35 patients at Tokai University Hospital (Table 1). This surgery was indicated for T1 and T2 pharyngeal and supraglottic laryngeal cancers. Cancers with deep invasion into the muscular layer were not indicated for this type of surgery. The 35 patients included 34 male and 1 female patient. The average age was 66.5 years. The primary cancer sites were as follows: hypopharynx (n ¼ 28), oropharynx (n ¼ 5), and larynx (n ¼ 8). There were 32 T1 lesions and 9 T2 lesions. The numbers of these superficial cancers were about 1/3 of the advanced hypopharyngeal (76 cases), oropharyngeal (41 cases), and supraglottic laryngeal (21 cases) cancers treated by open surgery or chemoradiation within the same time period. Two-thirds of the patients had no throat symptom and the cancer was diagnosed by screening patients with esophageal cancer using the NBI endoscopic system. The other one third of patients complained of throat symptoms such as pain and irritable sensation or neck mass. Transoral resection was carried out under a surgical microscope using a modified laryngeal microsurgery technique. A Weerda-type distending laryngoscope (Karl Storz, Tuttlingen, Germany) or a large-caliber pharyngoscope (Nagashima, Tokyo, Japan) was used for expanding the surgical field (Figures 1A, B). After staining with 1.5% to 3% iodine, an incision line with a safety margin of 5 to 10 mm was marked from the unstained area. An incision was made and the mucosal lesion was dissected transorally using an electrocautery with a Colorado 1162 HEAD & NECK DOI /HED AUGUST 2013

2 TRANSORAL RESECTION OF PHARYNGEAL AND LARYNGEAL CANCERS TABLE 1. Characteristic Patient characteristics and outcomes. Value 41 lesions (35 patients) Primary site Hypopharynx 28 Oropharynx 5 Larynx 8 T status T1/T2 32/9 pt status ptis/pt1/pt2 10/13/18 Histopathology SCC 31 CIS 10 Lateral margin Negative 36 Positive 1 CIS 4 Deep margin All negative Positive p16 status Hypopharynx 2 Oropharynx 1 Larynx 0 PORT Positive margin 1 Multiple LN metastasis 1 Local relapse 1 Local control rate 97.6% Overall survival (2 y) 90% Cause-specific survival (2 y) 100% Oral intake start 1.1 postoperative day Tracheostomy 0 Tube feeding 0 Dysphagia 0 Abbreviations: SCC, squamous cell carcinoma; CIS, carcinoma in situ; LN, lymph node; PORT, post-operative radiation therapy. microdissection needle tip (Figure 1C) (Stryker, Kalamazoo, Michigan). The specimen was dissected en bloc bimanually (Figure 1D) on the proper layer just above the pharyngeal constrictor muscle with binocular vision under a surgical microscope. Countertraction with forceps was essential for this technique. The hemostat was made with an argon plasma coagulator (APC 300, ERBE, Marietta, Georgia) or a suction coagulator (Karl Storz). One patient with cervical lymph node metastasis underwent radical neck dissection simultaneously. Postoperative irradiation was indicated if a positive surgical margin or multiple lymph node metastases were present. The histopathologic results were assessed using serial sections stained with hematoxylin eosin to identify the lateral and deep margins. The survival rate was calculated using the Kaplan Meier method. Excluding deaths from other cancers and dropouts from follow-up, the postoperative QOL was assessed in 29 patients using a questionnaire (European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Head and Neck Cancer Module [EORTC QLQ-H&N35]) 8 1 year after the surgery. The Japanese version of the questionnaire consists of 35 items, which are incorporated into 13 symptom scores. Each score is converted to scales from 0 to 100 in accord with the EORTC manual. A higher score represents a lower QOL. This study was approved by the institutional review board, and the written informed consents were obtained from the patients before the operation. RESULTS Oncologic and clinical results are summarized in Table 1. There were 31 squamous cell carcinomas (SCCs) and 10 carcinomas in situ (CIS). The size of the resected tumors ranged from 3 to 38 mm. The surgical margin was negative in most cases and was positive for cancer infiltration in 1 case. CIS was recognized at the margin in 4 cases. Postoperative radiotherapy was indicated for 2 patients (1 positive margin and 1 multiple cervical lymph node metastasis). Local relapse was observed in 1 patient during the follow-up period from 13 to 36 months (local control rate: 97.6%). Using the Kaplan Meier method, the 2-year overall and cause-specific survival rates were 90% and 100%, respectively. Postoperative function was favorable. No tube feeding or tracheostomy was needed. No postoperative hemorrhage or subcutaneous emphysema was encountered in our case series. Oral intake was started on the first or second day after the surgery (average 1.1 days). None of the patients complained of dysphagia or speech dysfunction 1 year after the surgery. The QOL was also well maintained 1 year after the surgery. The average score was The scales for swallowing, eating, and speech were <10 (see Figure 2). Representative case: T2N0M0 oropharyngeal cancer Preoperatively, a faintly red tumor with an irregular mucosal surface was recognized in the right posterolateral wall of the oropharynx (Figure 3A). NBI clearly demonstrated the tumor as a brownish area with irregular proliferation of the mucosal microvessels (intraepithelial papillary capillary loop; Figure 3B). Under general anesthesia, the pharyngeal tumor was clearly exposed using a large-caliber pharyngoscope. After staining with iodine (Figure 4A), a surgical margin was marked with a safety margin of 10 mm (Figure 4B). After mucosal incision with an electrocautery, the tumor was resected en bloc bimanually just above the pharyngeal constrictor muscle (Figure 4C). Figure 4D shows the raw surface of the constrictor muscle. Figure 5A shows the en bloc resected specimen, which had sufficient surgical margins from the iodine-stained area. Hematoxylin eosin staining revealed the tumor to be a partially invasive SCC with a negative surgical margin (Figure 5B). One year after the surgery, the pharynx was clearly covered by the scar (Figure 5C), and the patient had no complaints of difficulty in swallowing or any speech dysfunction. DISCUSSION Several organ-preservation surgical approaches have been recently reported. One such approach is the endoscopic approach, including endoscopic mucosal resection or endoscopic submucosal dissection, which is mainly reported by endoscopists. 9 Head and neck surgeons are not accustomed to submucosal resection with a flexible endoscope, which cannot adopt a bimanual technique like open surgery can. So this technique demands that head and neck surgeons complete a special training before performing the procedure. Another approach is the transoral HEAD & NECK DOI /HED AUGUST

3 OKAMI ET AL. FIGURE 1. Equipment used for en bloc transoral resection. (A) Weerda-type distending laryngoscope. (B) A large-caliber pharyngoscope 15 cm in length; caliber of the oral side is cm and that of the anal side is cm. (C) A Colorado microdissection needle. (D) Operation setting of the en bloc transoral dissection with bimanual technique under a surgical microscope. Weerda-type distending laryngoscope or a large-caliber pharyngoscope was used to expand the pharynx and provide a wide view and a wide surgical field. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] approach, including transoral laser microsurgery (TLM), 4 transoral videolaryngoscopic surgery (TOVS), 5,6 and transoral robotic surgery (TORS). 7 Steiner reported that TLM, which was performed for various stages of pharyngeal and laryngeal cancers, resulted in high local control and functional preservation. 4 FIGURE 2. Quality of life 1 year after the surgery HEAD & NECK DOI /HED AUGUST 2013

4 TRANSORAL RESECTION OF PHARYNGEAL AND LARYNGEAL CANCERS FIGURE 3. A representative case (oropharyngeal cancer T2N0M0). (A) Superficial tumor on the posterolateral wall. (B) Narrow band imaging clearly demonstrated the superficial lesion with brownish area. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] They used a CO 2 laser to dissect the tumor in a fractionated manner. En bloc resection could not be applied to larger sized tumors. We could accomplish en bloc resection with a wide-caliber pharyngoscope or distending laryngoscope in this study. Although they maintained a wide surgical field, multiple changes in the position of the scope were necessary for larger tumors. The choice of opening device is important. Recently, the Feyh Kastenbauer pharyngeal retractor has been used to expand the surgical field. 5,6 TOVS is a unique surgical technique developed by Shiotani and colleagues. 5,6 They used a rigid videoendoscope provided with a high-definition camera and laparoscopic surgical instruments for en bloc resection of pharyngeal and supraglottic cancers. Their system provides a broad field of view and a wide working space. Although surgeons do not observe the surgical field on the monitor in 3D view, as they would with a surgical microscope, the high-definition image is close and clear enough for this surgical procedure. This technique is very effective for minimally invasive surgery, and consequently, we are planning to simultaneously adopt this system. Although TORS is widely used in the United States, it is expensive and thus may not be available in some parts of the world. TORS has not been approved by the Ministry of Health, Labor, and Welfare in Japan. Should TORS become available in the near future, it can be introduced as a minimally invasive surgical technique. There are several advantages in our method. It is a modification of the classical laryngomicrosurgery and based on the regular operative technique like open surgery. Thus, it is easily adopted by otolaryngologists who are used to the laryngomicrosurgery and open surgical maneuvers. Although the laser surgery has been widely used, TLM reported by Steiner 10 requires a special technique and training. By their system, only small carcinomas are amenable to en bloc resection. For large lesions, the tumors are resected by multifractionation. However, the pathologic evaluation for the deep and lateral margins or invasive manner of depth become very complicated without en bloc resection. Moreover, a special training is required for the fractional dissection 5,6 and reconstruction of the fractionally excised specimens. The en bloc resection can be carried out by bimanual manipulation with traction and countertraction techniques and the dissection in accord with the proper tissue layers. Furthermore, it is also highly cost-effective. For en bloc resection a wide surgical view and working space are essential, which were achieved by using a Weerdatype distending laryngoscope, a large-caliber pharyngoscope, and a Colorado microdissection needle tip, which can be equipped at relatively low cost; moreover, the running cost is negligible. The initial and running costs of TORS are very expensive, demanding that surgeons undergo special training. In some countries, such as Japan, TORS is not yet approved by the government. The money-saving effect of national economy is also noteworthy. Our minimally invasive technique, which treats the FIGURE 4. Intraoperative findings ($: epiglottis). (A) Unstained lesion on the posterolateral wall. (B) Marking with a 10-mm safety margin. (C) Submucosal dissection with countertraction provided using forceps. (D) Raw surface after resection. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] HEAD & NECK DOI /HED AUGUST

5 OKAMI ET AL. FIGURE 5. Pathological and postoperative findings. (A) Resected superficial cancer. (B) Partially invasive carcinoma (hematoxylin eosin stain, original magnification, 40). (C) Scar formation 1 year after the surgery. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] cancer at an early stage, leads to a shorter hospital stay and diminishing the health care cost. The disadvantage of our system is the problem of field of view and working space. The field of view is relatively narrow, and en bloc resection is difficult for larger tumors. Observing the blind area in the narrow operative field is very difficult. Those problems could be solved by introducing the TOVS system developed by Shiotani and colleagues and Feyh Kastenbauer pharyngeal retractor. 5,6 Although the follow-up period is short, we had only 1 case of a local relapse (local control rate: 97.6%). Causespecific survival was 100% and postoperative functional outcomes were favorable. These results suggest that our technique is oncologically safe and function preserving. However, use of this technique is still controversial. Its use is currently confined to superficial cancers with or without lymph node metastasis. This technique can also be performed for cases with deep muscle invasion, as reported by other authors. 4,7 As the indication for use of this technique has expanded, delayed lymph node relapse will become a matter of importance. The correlation between lymph node metastasis and the depth of the invasion will be analyzed in the near future. In our series 1 patient had multiple lymph nodes metastases from T1 superficial hypopharyngeal cancer. The depth of the tumor of this patient was 1 mm. Recently, Tomifuji et al 11 reported that the tumor depth as a predictor of the lymph node metastasis. From their results the patients with tumor depth >1 mm have high incidence of lymph node metastasis. The tumor depth or vessel infiltration should be investigated correlated with the developing lymph node metastasis. Regarding the postoperative function, previous reports focused on the need for tube feeding and tracheostomy, the length of time before oral intake can be resumed, and the final status of diet. 4 7 Steiner et al 4 analyzed the duration of nasogastric tube feeding. They reported that 27.1% of patients in their study could resume oral intake on the first day after the surgery and the remaining patients were tube fed for 1 week. Their functional outcomes were very good with respect to wide and deep resection. According to the report by Shiotani et al, 5 patients resumed oral intake 5.9 days after the surgery and finally they could achieve normal diet. They recently published the QOL scores using the functional outcome swallowing scale and the communication score, suggesting a rapid recovery of eating and speaking compared with the open surgery or chemoradiation. 6 Although postoperative swallowing after TORS was evaluated by the possibility of oral intake, the time course of QOL after the surgery was recently reported by the group formed by Weinstein and O Malley. 12 They used the patient-reported short-form health survey and the performance status scale. Eating and diet function were decreased at 6 months but returned to baseline 12 months after the surgery. There was a significant difference between the TORS only group and the TORS with chemoradiation group. In our study, oral intake was started 1.1 postoperative day and neither tracheostomy nor tube feeding was necessary. It is because of the width and depth of the resection area compared with the other methods. The indication of this operation might be expanded, which affects the postoperative swallowing and speech function. In this study, we assessed the QOL 1 year after the surgery using the EORTC QLQ-H&N35, which is a wellestablished method to examine health-related QOL in long-term survivors of head and neck cancer. 13 It has been translated into many languages and is widely used all over the world. Our patients did not complain of difficulty in swallowing or speech disturbances 1 year after the surgery. However, the swallowing function is affected not only by the surgery but by other factors such as aging, systemic complications, history of other surgeries, and radiation therapy. Time-course change is also an important factor. We are planning a prospective study to evaluate swallowing function before and after the surgery using a questionnaire and videofluorographic or videoendoscopic examination of swallowing. Comparison of preoperative and postoperative swallowing function is a matter for future research. In this case series, two thirds of the cancers were diagnosed by screening patients with esophageal cancer. Double primary cancers of the head and neck occurring with esophageal cancers are now well known in Japan. The usefulness of the NBI endoscopic system for detecting early-stage cancers has been previously reported. 3 In accord with the development of the new optical devices and the establishment of the screening system, early-stage 1166 HEAD & NECK DOI /HED AUGUST 2013

6 TRANSORAL RESECTION OF PHARYNGEAL AND LARYNGEAL CANCERS cancers will be detected before symptoms occur and use of the minimally invasive surgery described in this study will be more common and significantly better for organ and functional preservation. In fact, the numbers of superficial cancers in our institute are increasing rapidly, which account for a third of the advanced cancers. As mentioned in the introduction, the treatment for superficial cancers at an early stage will be more feasible and cost-effective with the systems described here. CONCLUSIONS Microscopic transoral en bloc resection was applied to superficial pharyngeal and supraglottic cancers. With this surgical technique, en bloc resection was achieved with a wide view and a good surgical field. The oncologic outcome was satisfactory and the postoperative function was favorable. REFERENCES 1. Spafford MF, Koch WM, Reed AL, et al. Detection of head and neck squamous cell carcinoma among exfoliated oral mucosal cells by microsatellite analysis. Clin Cancer Res 2001;7: Okami K, Imate Y, Hashimoto Y, Kamada T, Takahashi M. Molecular detection of cancer cells in saliva from oral and pharyngeal cancer patients. Tokai J Exp Clin Med 2002;27: Watanabe A, Taniguchi M, Tsujie H, Hosokawa M, Fujita M, Sasaki S. The value of narrow band imaging endoscope for early head and neck cancers. Otolaryngol Head Neck Surg 2008;138: Steiner W, Ambrosch P. Endoscopic laser surgery of the upper aerodigestive tract. New York: Thieme; pp Shiotani A, Tomifuji M, Araki K, Yamashita T, Saito K. Videolaryngoscopic transoral en bloc resection of supraglottic and hypopharyngeal cancers using laparoscopic surgical instruments. Ann Otol Rhinol Laryngol 2010;119: Yamashita T, Tomifuji M, Araki K, Kurioka T, Shiotani A. Endoscopic transoral oropharyngectomy using laparoscopic surgical instruments. Head Neck 2011;33: Weinstein GS, O Malley BW Jr, Snyder W, Hockstein NG. Transoral robotic surgery: supraglottic partial laryngectomy. Ann Otol Rhinol Laryngol 2007;116: EORTC group for research into Quality of Life. index.htm 9. Muto M, Satake H, Yano T, et al. Long-term outcome of transoral organpreserving pharyngeal endoscopic resection for superficial pharyngeal cancer. Gastrointest Endosc 2011;74: Ambrosch P, Kron M, Steiner W. Carbon dioxide laser microsurgery for early supraglottic carcinoma. Ann Otol Rhinol Laryngol 1998;107: Tomifuji M, Imanishi Y, Araki K, et al. Tumor depth as a predictor of lymph node metastasis of supraglottic and hypopharyngeal cancers. Ann Surg Oncol 2010;18: Leonhardt FD, Quon H, Abrahão M, O Malley BW Jr, Weinstein GS. Transoral robotic surgery for oropharyngeal carcinoma and its impact on patient-reported quality of life and function. Head Neck 2012;34: Bjordal K, de Graeff A, Fayers PM, et al. A 12 country field study of the EORTC QLQ-C30 (version 3.0) and the head and neck cancer specific module (EORTC QLQ-H&N35) in head and neck patients. EORTC Quality of Life Group. Eur J Cancer 2000;36: HEAD & NECK DOI /HED AUGUST