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  Table of Contents  
Year : 2019  |  Volume : 56  |  Issue : 1  |  Page : 9-14

Oncological outcome following TORS in HPV negative supraglottic carcinoma

Department of Surgical Oncology, BLK Super Specialty Hospital, Pusa Road, Delhi, India

Date of Web Publication4-Apr-2019

Correspondence Address:
Karan Gupta
Department of Surgical Oncology, BLK Super Specialty Hospital, Pusa Road, Delhi
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_172_18

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 » Abstract 

Objective: The aim of this study was to determine the oncological and functional outcomes following transoral robotic surgery (TORS) in human papilloma virus negative supraglottic cancers.
Study Design: A prospective observational study at a tertiary cancer care center, New Delhi, India.
Materials and Methods: From February, 2013 to December, 2015, 45 patients with supraglottic lesions underwent TORS using the da Vinci® surgical system.
Results: Forty-five patients underwent TORS for supraglottic laryngectomy (SGL), with all patients undergoing bilateral neck dissection. The most common site was Ary-epiglottic fold. 47.9% were cT1 and 52.1% were cT2. Average robotic set-up time was 8.8 min and average robotic operative time was 42.9 min. A positive or close margin was seen in 12 patients (26.7%) on frozen, which were revised intraoperatively. On final histology, 3 (6.7%) patients had a margin of <5 mm. The average closest margin was 5.7 mm. Patients tolerated oral feeds within 2 weeks of procedure. All patients were HPV negative. Postoperatively, all patients had adequate swallowing and speech. Follow-up ranged from 24 to 58 months. Thirty-eight (84.4%) patients were alive and disease free.
Conclusion: TORS is a safe, feasible, minimally invasive, and oncologically safe procedure in patients with early HPV supraglottic cancers. It has less morbidity and offers benefits in terms of early airway and feeding rehabilitation and avoids complications resulting from radiation therapy for these patients.

Keywords: Feasibility study, minimally invasive, oncological outcome, supraglottic laryngectomy, transoral robotic surgery (TORS)

How to cite this article:
Dabas S, Gupta K, Ranjan R, Sharma AK, Shukla H. Oncological outcome following TORS in HPV negative supraglottic carcinoma. Indian J Cancer 2019;56:9-14

How to cite this URL:
Dabas S, Gupta K, Ranjan R, Sharma AK, Shukla H. Oncological outcome following TORS in HPV negative supraglottic carcinoma. Indian J Cancer [serial online] 2019 [cited 2022 Jul 6];56:9-14. Available from:

 » Introduction Top

Laryngeal cancer is the seventh most common cause of cancer in males in India. In 2012, an estimated 25,446 new cases were diagnosed, and 17,560 Indians lost their lives due to laryngeal cancer.[1] In India, the incidence of laryngeal cancer has been reported to be 1.26–8.18 per 100,000 population in different regions of the country.[2] In a study from south India, supraglottic carcinoma formed approximately 19.4% of the total laryngeal cancer cases.[3]

The treatment options for supraglottic squamous cell carcinoma (SCC) at present include primary chemoradiation (CTRT), transoral laser microsurgery (TLM), and open surgical resection.[4],[5],[6] Surgical treatments (TLM or open surgery) avoid the acute and delayed toxicities associated with chemoradiation. However, TLM is a technically difficult surgical procedure, with a long learning curve and a longer surgical time.

With the advent of the da Vinci robotic surgical system, the ease of transoral procedures in the head and neck region has dramatically improved. The system provides a minimally invasive access to oropharyngeal and laryngeal surgeries. Weinstein et al. in 2007 were the first to report a good functional and oncological outcome following TORS for supraglottic carcinoma.[7] The robotic system provides a better visualization of the surgical field with the use of the 30° telescope along with the three-dimensional (3D) view. Moreover, with seven degrees of freedom attained with the robotic system, the dexterity of the surgeon improves.

The main aim of this study was to evaluate the functional and oncological outcome of transoral robot-assisted surgery to perform supraglottic laryngectomy (SGL) in cases of SCC of supraglottis.

 » Materials and Methods Top

A prospective study was performed from February, 2013 to December, 2015 to evaluate the surgical feasibility, safety, functional outcome, and oncological outcome of transoral robotic surgery (TORS) to perform SGL in cases of SCC of supraglottis. The study was conducted according to the principles set out in the Declaration of Helsinki 1964 and all subsequent revisions. Informed consent was obtained for the study, and relevant institutional review board approved the study. A total of 46 patients were included in the study. The inclusion and exclusion criteria are listed in [Table 1].
Table 1: Showing the inclusion and exclusion criteria of the study

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The surgical intervention was performed with the patient under general anesthesia with a nasotracheal intubation. Tracheostomy was performed in few patients who were deemed to have higher risk of aspiration and difficult airway or in patients where it was thought that the nasotracheal tube would interfere with surgical resection. A Ryles tube insertion or percutaneous gastrostomy (PEG) was performed for maintaining adequate feeding postoperatively. PEG was considered in patients who had lesions near the midline and where the risk of postoperative aspiration was considered high.

The da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA) was set up, as previously described by Weinstein et al.[7],[8] Proper surgical exposure was attained with the use of a Feyh–Kastenbauer retractor (Gyrus-Medical, Tuttlingen, Germany). A binocular endoscope of 0° and 30° were used to gain 3D vision. Five millimeter diameter instruments namely Maryland dissector and monopolar cautery spatula arms were used. The surgeon was seated at the console of the da Vinci system while an assistant positioned at the head of the patient assisted with the suction and retractor.

Bilateral open neck dissection was performed immediately before the TORS. Adjuvant treatment in the form of chemoradiation or radiation was finally taken after the final histopathological report.

The data collected in this study included the demographic characteristics (age and sex) of the patients, tumor site, clinical and pathologic stage (based on the TNM classification system from the Union for International Cancer Control, seventh edition, 2009), margin status, type of SGL, perioperative complications, total length of hospital stay, rate and length of tracheostomy, rate and length of feeding tube or percutaneous endoscopic gastrostomy (PEG) tube dependency, and postoperative adjuvant therapy.

The type of SGL was identified according to the European Laryngological Society classification system.[9]

The endpoints of the study were determined according to the feasibility, safety, and assessment of the surgical margins. Feasibility was measured by the ability to perform TORS without the need for conversion to an open surgery. The safety was assessed by the incidence of perioperative complications, as well as functional outcomes, including the rate of dependency on PEG and tracheostomy. Postoperative swallow function was assessed by a physiotherapist and physician with fiberoptic endoscopic evaluation. The oncological outcome was assessed by rate of recurrence, disease-free survival, and overall survival at a minimal follow-up of 24 months and a mean follow-up of 41 months.

 » Results Top

A total of 46 patients of SCC of supraglottis who underwent TORS from February, 2013 to December, 2015 were included in the study. All patients were p16 negative on the preoperative biopsy. The demographic characters of the patients are shown in [Table 2].
Table 2: Demographic details of the patients (n=46)

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The clinicopathological details of the patients are presented in [Table 3].
Table 3: Clinicopathological details of the patients (n=46)

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Feasibility and safety

Average robotic set-up time was 8.8 min (range, 6–14 min) and average robotic operative time was 42.9 min (range, 35–58 min). Average blood loss during surgery was 33 ± 15 ml. Superior laryngeal artery (SLA) ligation was performed in 31 patients.

One patient had to be converted to open surgery because of difficulty in access due to trismus, and was excluded from the final analysis.

A positive or close margin was seen in 12 patients (26.7%) on frozen, which were revised intraoperatively. On final histology, 3 (6.7%) patients had margins <5 mm. Average closest margin on final histology was 5.7 mm.

Functional outcome

Patients whom it was suspected on preoperative evaluation that the nasotracheal intubation would hinder with the surgical resection or who might aspirate after the surgery or those who had difficult intubation due to decreased mouth opening, underwent preoperative tracheostomy. Twenty-four (53.3%) patients required tracheostomy, and 11 (24.4%) patients underwent PEG for feeding, and rest 34 patients had nasogastric tube placement. All except 3 patients were successfully decannulated after surgery. Six (13.3%) patients were dependent on long-term nasogastric tube/PEG feeding. Patients started tolerating oral feeds within 2 weeks of procedure (mean, 8.4 days), with the nasogastric tube removed within 2–3 weeks postoperatively (mean, 14.2 days) after performing a functional endoscopic evaluation of swallowing to evaluate for swallowing function and ruling out aspiration. The average hospital stay was 10.3 days (range, 7–23 days) [Table 4].
Table 4: Functional outcome of the patients

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Adverse events

Postoperative complications in the form of primary hemorrhage required active intervention in 2 patients. The bleed was identified from a small branch of the superior laryngeal artery and was managed by clipping under direct laryngoscopic visualization. Two patients developed aspiration pneumonitis, which was managed by intravenous antibiotics and prolonged nasogastric tube feeding.

Adjuvant treatment

On the final histology, 3 (6.7%) patients had margins <5 mm. A total of 26 (57.7%) patients had stage III/IV disease and required either radiation or chemoradiation on the basis of the final histopathology in view of high stage, multiple nodal positivity or positive or close margins. Nineteen patients (42.2%) were stage I/II and did not require any adjuvant treatment after TORS SGL [Table 5].
Table 5: Oncological outcome of patients (n=45)

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In the adjuvant setting, the radiation dosage was limited to 60 Gy in 30 fractions with or without 5–6 cycles of weekly inj. cisplatin.

Oncological follow-up

The mean follow-up was 41 months (range, 24–58 months). All 45 patients were on regular follow-up. Two (4.4%) patients expired due to nononcological causes. Five (11.1%) patients had locoregional recurrence on follow-up, of which 3 expired due to the disease. Thirty-eight patients are on regular follow-up with no evidence of disease and are doing well, with an overall disease-free survival of 84.4% and an overall survival of 88.9%.

 » Discussion Top

The standard treatment options for SCC of supraglottis include chemoradiation (CRT), open transcervical resection, and TLM. At present the aim of treatment for SCC of supraglottis is good oncological outcome along with organ preservation, resulting in functional and structural preservation.

The major advantage of surgical treatment modality is the ability to precisely map the disease extent and the ability to attain the final pathological staging of the patient. It also helps to evaluate the nodal status of the patient. These benefit in the planning of adjuvant treatment in form of radiation or chemoradiation, and can thus prevent irradiation in early stage tumors. This helps to avoid early and late complications of chemoradiation, as well as helps to keep chemoradiation in reserve in cases of recurrence or second primary carcinoma. This is important because patients treated for a supraglottic SCC have a high five-year survival rate,[10] and are at a risk of developing a second primary carcinoma in the range of 9–40% according to various studies.[11],[12],[13] Moreover, in the adjuvant settings, the radiation dose delivered is 60 Gy as compared to 70 Gy given upfront, which reduces the radiation related toxicities significantly, as was seen in our study.

The classical surgical approach for supraglottic cancers was the open transcervical approach, which provided adequate exposure and tactile feedback. However, the approach had a lot of drawbacks in the form of compulsory need for tracheostomy and prolonged nasogastric tube or PEG feeding.[14] Further, this approach led to prolonged hospitalization and delayed recovery of the patient, which delayed early rehabilitation of the patient. This led to a considerable financial burden both on the patient and the hospital.

Subsequently, as a result of a lot of morbidity associated with the open surgical approach and also with an aim of organ preservation, supraglottic carcinomas were treated with chemoradiation. However, this approach is also not free from complications in the form of early and delayed radiation resulted toxicities. The addition of chemotherapy to the radiation regimen further potentiates the toxicities of radiotherapy. Moreover, patients undergoing chemoradiation have a longer dependence on feeding tubes.[15],[16] Use of chemoradiation as the primary treatment modality for early supraglottic carcinomas limits the use of the same in cases of recurrence or second primary cancers. Also, re-radiation is further associated with enhanced toxicity and morbidity.

To overcome these complications associated with open surgical techniques and CRT, there was development of minimally invasive technique of surgery using TLM. The aim of this approach was to attain good oncological results with early functional rehabilitation and early recovery of the patients. TLM has shortened the duration of hospitalization as all patients undergoing TLM do not require tracheostomy. Moreover, patients could be started on oral feeds earlier as compared to open surgery. For oncological outcomes, TLM compares well with open surgery for proper tumor visualization and resection.[4],[5],[17],[18] However, TLM has certain inherent problems, as there is a long learning curve associated with the technique. In addition, gaining adequate exposure is of upmost importance which might become difficult in Indian patients due to the high incidence of submucous fibrosis associated with areca nut use.

With the advent of the da Vinci robotic surgical system and the use of the same in head and neck as TORS, a lot of the drawbacks of TLM have been eliminated. TORS provides the advantage of four hands. The endoscopic 0° and 30° vision provides a magnified 3D vision unparallel to the one attained in TLM. TORS also significantly reduces the operating time of the surgery. In addition, the learning curve is much less compared to TLM.[19] In a study comparing TORS to TLM for resection of supraglottic cancers, TORS was found to be as safe and effective as compared to TLM and the overall operative time was shorter than TLM.[20]

HPV status seems to affect the prognosis and outcome in patients with supraglottic carcinoma, similar to the effect on prognosis in outcome seen in oropharyngeal cancers. In a study by Xu et al., the three-year overall survival rate and progression-free survival rate were higher in HPV-positive than that in HPV-negative patients, however, the difference was not statistically significant.[21]

In the literature till date, there is no prospective single institutional study regarding the safety and functional and oncological outcome in HPV-negative supraglottic SCC. In this study, we found that the use of TORS to perform SGL is applicable to early-stage HPV negative supraglottic carcinomas, with a good outcome. No adverse complications were encountered, and only 1 patient required conversion to open surgery. This case of conversion was due to insufficient exposure of the surgical field due to limited mouth opening as a result of submucous fibrosis. Similar results were seen in another retrospective multi-institutional feasibility study done by Razafindranaly et al.[22]

In our study, the average robotic set-up time was 8.8 min (range, 6-14 min) and average robotic operative time was 42.9 min (range, 35-58 min). Average blood loss during surgery was 33 ± 15 ml. Twenty-four patients (53.3%) underwent tracheostomy for airway management, out of which 21 were successfully decannulated on an average of 6.3 postoperative day. Only 3 (6.7%) patients required a prolonged tracheostomy for airway management and aspiration. Various studies have quoted the requirement of tracheostomy in such patients from 0% to 78%.[22],[23],[24],[25] Patients with TORS tend to get decannulated early as compared to patients undergoing open transcervical surgery.[26] Moreover, our rates of prolonged tracheostomy were comparable to the rates of permanent tracheostomy (7.7%) in patients who underwent TLM, as reported by Cabanillas et al.[27]

In our study, 2 (4.4%) patients had aspiration pneumonitis. There was no increase in the incidence of pneumonitis in TORS as compared to open transcervical surgery or TLM. The incidence of aspiration pneumonitis in patients undergoing TLM has been reported in the literature to range from 2 to 11.5%,[4],[27],[28] whereas in patients undergoing open surgery the rates can be as high as 40%.[29] In the study by Razafindranaly et al.,[22] the rate of aspiration pneumonitis after TORS was 23%, which was much higher than our result of 4.4%, which could have been due to their low rates of temporary tracheostomy (24%) compared to 53.3% in our study; moreover, 24% patients were started on oral feeds within 24 h of the surgery, which could have increased the chances of aspiration pneumonitis. Thus, an elective temporary tracheostomy and proper postoperative swallowing evaluation could decrease the incidence of pneumonitis in patients undergoing TORS.

All patients had some form of feeding tube, either Ryles tube or percutaneous gastrostomy tube placed at the time of surgery. On an average, the oral feed was started on the 8.4 postoperative day with removal of the feeding tube on the 14.2 postoperative day. Only 6 (13.3%) of the patients were dependent on long-term PEG feeding for nutrition. In various studies for TORS, the long-term dependence on enteral feeding tube ranges from 9.5% to 22%.[22],[23] TORS allows for a faster and better compliance to oral food intake as compared to open transcervical surgery. In a study by Park et al.,[26] the patients who underwent robotic-assisted surgery were started orally on an average of 8.1 days as compared to 18.5 days after open transcervical surgery. Similarly, our results of TORS are comparable to TLM for SGL. Canis et al.[4] reported that 5% of the patients required gastrostomy lasting 2 to 42 months and 2% underwent permanent gastrostomy after TLM SGL.

Compared to the duration of enteral feeding tube in patients who undergo CRT, the duration was found to be shorter in our study for patients undergoing TORS. Due to early and late toxicities of CRT such as mucositis, xerostomia, and stricture, patients complain of dysphagia and odynophagia, leading to prolonged dependence on feeding tubes for proper nutrition, both during the treatment and even after that. In a meta-analysis by Machtay et al., it was found that 20.4% of the patients required enteral feeding tube for more than 2 years after completion of the treatment.[15]

On further evaluation of the margins of resection during the surgery, 12 (26.7%) patients had either close (<5 mm) or positive (<1 mm) margin on frozen section intraoperatively. The margins were revised in all these patients. On final histopathology, 3 (6.5%) patients had close (<5 mm) margin, but no patient had positive margin. This was in conjunction with various studies where negative margins were obtained in all patients.[23],[24],[25],[30] In our study, the average closest margin attained for all patients who underwent TORS SGL was 5.7 mm. This stresses the importance of availability of frozen section in all cases of TORS as this can significantly reduce the margin positivity rates.

One of the major concerns after TORS has been secondary hemorrhage. Two (4.4%) patients developed postoperative bleeding requiring re-exploration. The study by Weinstein et al.[31] reported approximately 5% incidence of postoperative bleeding following TORS for any otolaryngology site. Our results correlated well with theirs and are also similar to postoperative bleeding incidence reported after TLM in the range of 9–11.5%.[17],[21] There was no correlation between ligation of the SLA and incidence of bleed. Of the 2 patients who bled, one underwent SLA ligation and one did not.

One of the aims of this study was to re-examine the clinical and pathologic staging variation that would lead to a decision for adjuvant therapy and to evaluate the merit of up-front surgery in providing risk assessment through surgical pathology. With TORS we could provide the exact pathological staging for need of any adjuvant treatment, which is usually missed with upfront radiation/chemoradiotherapy and might lead to under treatment of certain patients with occult metastasis in the neck not picked up on any imaging leading to a false understaging and undertreatment of the patient. Further, after TORS the exact pathological staging provides a better guide for need for adjuvant treatment either in the form of radiotherapy alone or chemoradiotherapy. Some may argue that the tri-modality therapy should be avoided at all costs; however, there may be benefits if surgery allows for reduced radiation dose to the pharyngeal constrictors. Dose to the superior pharyngeal constrictors is a predictor of late radiation associated dysphagia.[32]

De-intensification of adjuvant therapy is possible when using upfront TORS. Previous reports have described that 50% to 72% of stage I/II tumors in our series were able to avoid all adjuvant therapy, whereas in our series all patients of stage I/II tumors could avoid adjuvant treatment. In previous studies, 34% to 49% of stage III/IV tumors were spared chemotherapy. whereas in our study 88.5% of stage III/IV patients could avoid chemotherapy.[33],[34] Moreover, 42.3% of the patients of stage I/II who would have received upfront definitive radiotherapy avoided it completely due to upfront surgery. These represent another instance of de-intensification, with possible long-term quality of life benefits.

In this study involving 26 patients of stage III/IV, 23 (51.1%) patients required postoperative radiotherapy and only 3 (6.1%) patients required chemoradiotherapy. Moreover, the dose of radiotherapy was decreased from 70 Gy/35# in upfront setting to 56–60 Gy/28–30# with or without 5–6 cycles of weekly inj. cisplatin. This reduction in postoperative radiation dosage plays a big role in improved functional outcome in these patients, with nearly 86.7% of all patients having normal swallowing within 3 months of completion of the treatment. The stricture rates and prolonged dependence to tube feeding is nearly 50% and 30%, respectively, when the dose received by the pharynx and larynx is 70 Gy. Also, the aspiration risk and dysphagia risk increase to >50% with radiation doses above 65 Gy.[32] Moreover, the addition of chemotherapy to radiotherapy tends to increase the Grade III–IV toxicities from 52 to 89.5%.[35] Similar increase in Grade III/IV toxicities up to 30.6% with addition of chemotherapy to radiotherapy was also seen in the GORETEC Trial (94-0).[36] Thus, with the addition of TORS to the treatment algorithm, we could completely avoid any adjuvant treatment in nearly 42% of the patients and also reduced the dosage of radiotherapy with avoidance of chemotherapy in a majority of patients requiring adjuvant treatment. This dose reduction in terms of total radiation dose and chemotherapy received would certainly lead to better functional outcomes, with no impact on oncological outcome, as seen in our study.

In our series, 19 (42.2%) patients were stage I or II and did not require any adjuvant treatment after TORS SGL, and the disease-free survival at the mean follow-up of 37 months (range, 20–53 months) for stage I/II was 84.2%. Of the 26 (57.7%) patients who were stage III/IV and received adjuvant radiotherapy/chemoradiotherapy after TORS SGL, 22 (84.6%) were disease free at mean follow-up of 41 months. The overall disease-free survival was 84.4% and overall survival was 88.9%. Local control rates of conventional supraglottic laryngectomy range 90–100% for T1, 80–97% for T2, and 71–94% for T4 carcinomas.[37],[38] Bocca et al.[39] reported a two-year local recurrence rate of 16.5% (stage I and II) and 21.5% (stage III and IV) for open surgery. Primary radiotherapy can achieve local control rates of 77–100% in supraglottic T1 cancers and 62–83% in T2 cancers.[39],[40],[41],[42],[43] Using the TLM, Ambrosch et al.[44] achieved a local control of 89% in early T1-2 supraglottic carcinoma. Canis et al.[4] achieved 91% for early disease and 85% for advanced disease. Our results are similar to all other treatment modalities for supraglottic cancers, and thus TORS SGL is also an oncologically safe option of treatment for supraglottic SCC.

 » Conclusion Top

This is a first of its kind single institutional study which evaluated oncological outcome in HPV-negative supraglottic SCC. This study demonstrated that TORS SGL performed for early primary stage supraglottic SCC is feasible and safe, with good functional and oncological outcome. It seems to have less morbidity and offers benefits in terms of early airway and feeding rehabilitation and can avoid complications resulting from higher dose radiation therapy with or without chemotherapy for these patients; however, it needs to be confirmed in the long term. Long-term oncological outcome and five-year survival still needs to be evaluated for TORS SGL.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 » References Top

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]

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