Transoral CO2 laser microsurgery for Tis-T3 supraglottic squamous cell carcinomas

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Eur Arch Otorhinolaryngol (2010) 267:1735–1742 DOI 10.1007/s00405-010-1284-1

LARYNGOLOGY

Transoral CO2 laser microsurgery for Tis-T3 supraglottic squamous cell carcinomas Giorgio Peretti • Cesare Piazza • Mohssen Ansarin Luigi De Benedetto • Daniela Cocco • Augusto Cattaneo • Piero Nicolai • Fausto Chiesa



Received: 11 August 2009 / Accepted: 7 May 2010 / Published online: 25 May 2010 Ó Springer-Verlag 2010

Abstract Eighty patients affected by supraglottic cancer were treated by transoral carbon dioxide laser surgery between 1989 and 2006 in two Italian institutions. Patient staging was as follows: 2 pTis, 20 pT1, 38 pT2, and 20 pT3. Simultaneous or 1-month delayed neck dissection (ND) was performed on 27 (34%) patients, unilaterally in 10 and bilaterally in 17. The pN category was as follows: 9 pN0, 6 pN1, 8 pN2b, and 4 pN2c. A total of 16 (20%) patients received complementary radiotherapy (RT) and 5 (6%) were subjected to chemo-RT for persistent tumor after re-excision due to positive margins, multiple lymph nodes, and/or extracapsular spread after ND. The last follow-up was in December 2008. The 5-year overall, diseasespecific and disease-free survivals, local control with laser alone, and organ preservation rates calculated by Kaplan– Meier analysis were 84.4, 97.4, 88.3, 96, and 97.2%, respectively. Univariate analysis showed a statistically significant impact on disease-free survival, local control with laser alone, and organ preservation of pT category (p = 0.009, p = 0.01, and p = 0.03, respectively), while pN category and tumor stage negatively influenced diseasefree survival (p = 0.007 and p = 0.01, respectively). This series confirms the good overall oncologic outcomes obtained by transoral laser surgery for Tis, T1, T2, and

G. Peretti (&)  C. Piazza  L. De Benedetto  D. Cocco  P. Nicolai Department of Otorhinolaryngology, Head and Neck Surgery, University of Brescia, Piazza Spedali Civili 1, 25123 Brescia, Italy e-mail: [email protected] M. Ansarin  A. Cattaneo  F. Chiesa Department of Head and Neck Surgery, European Institute of Oncology, Milan, Italy

selected T3 supraglottic cancer with minimal pre-epiglottic space involvement. Keywords Transoral laser surgery  Carbon dioxide laser  Laryngeal cancer  Supraglottic cancer  Conservative laryngeal surgery

Introduction The ideal treatment for supraglottic squamous cell carcinoma (SCC) is still a matter of debate. Radiotherapy (RT) with or without chemotherapy (CHT) and open-neck conservative surgery such as horizontal supraglottic laryngectomy (HSL) or, in case of glottic involvement, supracricoid partial laryngectomy with cricohyoidopexy (SCPL-CHP) are considered to be the most established treatment options [1–7]. In the last two decades, however, the use of endoscopic supraglottic laryngectomy (ESL) by carbon dioxide laser has been increasingly popularized as a feasible approach to Tis, T1, T2, and selected T3 supraglottic SCC [8–11]. The main advantage of ESL is represented by the possibility of tailoring surgical resection to the precise three-dimensional extension of the tumor with preservation of the adjacent healthy subsites. When valid concepts of surgical oncology are followed, the uninvolved contralateral supraglottic structures in the case of a lateralized tumor, for example, can be reasonably spared, thus reducing postoperative morbidity and functional sequelae [12]. In light of this, the European Laryngological Society introduced a proposal for classification of ESLs encompassing four types of procedures: Type I or limited excision of only one supraglottic subsite for small superficial lesions of the free edge of the epiglottis, aryepiglottic fold, arytenoid

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cartilage, or ventricular fold; Type II, or supraglottic laryngectomy without resection of the pre-epiglottic space (distinguished into a Type IIa resection or suprahyoid epiglottectomy, and a Type IIb resection or total epiglottectomy); Type III or complete supraglottic laryngectomy with resection of the pre-epiglottic space, without (Type IIIa) or with (Type IIIb) extension to the ventricular fold; Type IV or lateral supraglottic laryngectomy, suitable for tumors of the aryepiglottic and pharyngoepiglottic folds, which may include the resection of the ventricular fold (Type IVa) or the arytenoid cartilage (Type IVb) [13]. The aim of this paper was to present the experience of two Italian institutions sharing common treatment protocols and surgical expertise in endoscopic management by transoral carbon dioxide laser microsurgery for Tis-T3 supraglottic SCC, focusing on oncologic results, postoperative course, and complications.

Patients and methods Demographics Between January 1989 and December 2006, 290 patients affected by Tis-T3 supraglottic SCC were treated at an academic institution (Department of Otorhinolaryngology, Head and Neck Surgery, University of Brescia, Italy) and a national cancer institute (Department of Head and Neck Surgery, European Institute of Oncology, Milan, Italy). As much as 44 (15%) underwent RT or CHT-RT, 166 (57%) were treated by open-neck HSL, and 80 (28%) by ESL. Distribution of cases between the two institutions was as follows: 218 (75%) treated at the University of Brescia (between 1989 and 2006) and 72 (25%) at the European Institute of Oncology of Milan (between 1994 and 2006). A cross-tabulation of T categories versus treatment is reported in Table 1. Among the group of 80 patients treated by transoral CO2 laser surgery, 62 were males and 18 females (age range, 42–81 years; mean, 64.5); 71 (89%) patients had never been treated before, while 9 (11%) had been previously treated by laser resection for glottic SCC. Distribution of

endoscopically treated cases between the two institutions was as follows: 49 (61%) treated at the University of Brescia (between 1989 and 2006) and 31 (39%) at the European Institute of Oncology of Milan (between 2000 and 2006). A total of 75 (94%) subjects were endoscopically treated after January 2000 (Fig. 1). Diagnostic, therapeutic, and follow-up procedures Preoperative evaluation was based on flexible fibrolaryngoscopy and/or rigid videolaryngoscopy with a 70° telescope. Moreover, intraoperative rigid endoscopy with 0° and angled telescopes (Karl Storz, Tuttlingen, Germany) was accomplished during microlaryngoscopy under general anesthesia. CT or MRI was added to preoperative evaluation in the majority of cases and avoided only for selected cT1 with a superficial pattern of growth. Ultrasound examination of the neck was performed in every patient, and fine needle aspiration cytology only in the case of suspected lymph node metastases. Tumor excision was always performed under microlaryngoscopy. A Sharplan 1055 S carbon dioxide laser (Sharplan, Tel Aviv, Israel) with superpulse delivery in continuous mode (1–5 W), coupled since 1996 to an Acuspot 712 micromanipulator (270-micron spot size), was used at the University of Brescia. A 25 W Martin CO2 Laser (Martin, Tuttlingen, Germany) with a beam spot of 150 lm diameter used in the superpulse continuous mode, with output power set to 0.8–7.4 W, was employed in the European Institute of Oncology. Laryngeal exposure was

HLS

ELS

180 160 140 120 100 80 60

Table 1 Cross-tabulation of T categories versus treatment 40

RT/CRT n = 44

HSL n = 166

ESL n = 80

Tis

2

1

2

T1

30

6

20

T2

11

90

38

T3

1

69

20

RT/CRT radiotherapy/chemoradiotherapy; HSL open-neck horizontal supraglottic laryngectomy; ESL endoscopic supraglottic laryngectomy

123

20 0 1989-2000

2000-2006

Years Fig. 1 Distribution of cases treated by endoscopic supraglottic laryngectomy (ESL) versus open-neck horizontal supraglottic laryngectomy (HSL) for SCC cancer before and after 2000

Eur Arch Otorhinolaryngol (2010) 267:1735–1742

obtained using a wide range of different laryngoscopes as the Lindholm (Pilling, Philadelphia, PA) and the Steiner’s bivalved adjustable laryngopharyngoscope (Karl Storz, Tuttlingen, Germany). Less frequently, we used Dedo or Dedo-Ossoff laryngoscopes (Pilling, Philadelphia, PA), and the latter is particularly indicated for difficult anatomical conditions. Endoscopic resections were performed by en bloc or piecemeal techniques according to a number of variables such as laryngeal exposure, T category, tumor site, and size. ESLs performed were retrospectively classified according to the European Laryngological Society classification [13]. Surgical specimens were sent to a dedicated pathologist marking one designated edge with black ink. In case of resections performed by piecemeal technique, a diagram of the larynx with indications of the procedure performed was sent together with the specimen. The most critical margins were indicated by the surgeon. In the present series, all ESLs were performed with curative intent. Our indications included supraglottic SCC ranging from cT1 to selected cT3 for minimal pre-epiglottic space involvement (i.e., with preservation of a rim of healthy fat tissue between the front of the tumor progression and the thyrohyoid membrane). Contraindications for ESL were: (1) massive infiltration of the pre-epiglottic space, (2) laryngeal framework involvement, (3) fixation of the true vocal cord due to crico-arytenoid joint and/or paraglottic space encroachment, and (4) inadequate endoscopic exposure of the larynx. Tumors were classified according to the 2002 TNM classification proposed by the AJCC-UICC [14, 15]. The neck management strategy was modulated according to the cT and cN categories. Therefore, for all cT1N0 and small cT2N0 (i.e., T2 with a volume comparable to that of a T1 but encroaching on two adjacent subsites, as in the case of a tumor centered between the supra- and the infra-hyoid epiglottis), we did not perform neck dissection (ND). For bulky cT2N0 and all cT3N0, we performed delayed selective ND (levels II-IV), which was planned 1 month after ESL or elective RT on the neck if it was needed for complementary treatment in the T stage. In case of cN? patients, ND was performed simultaneously with the endoscopic procedure (bilaterally in case of cN [1 or for tumors crossing the midline). In case of close surgical margins, a careful endoscopic follow-up with monthly fiberoptic controls was chosen. In case of positive margins, retreatment was planned after completion of the healing process (30–40 days). The criteria for adjuvant RT or CHT-RT was determined by the presence of tumor in the second surgical specimen after retreatment for positive margins and by the presence of metastasis in more than two lymph nodes or extracapsular spread. In such cases, we preferred complementary RT or

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CHT-RT, both on the T and N sites, instead of open-neck partial laryngectomy followed by complementary RT on the N site only for the high risk of prolonged airway edema usually observed after irradiation of patients treated by HSL or SCPL. Major postoperative complications (in which surgical treatment was deemed necessary), need for nasogastric feeding tube or tracheotomy, and hospitalization time were retrospectively analyzed by review of clinical charts. All patients began swallowing in the rehabilitation period during hospitalization and were discharged only when adequate semi-liquid or normal oral feeding was possible. The last follow-up was obtained in December 2008 and ranged from 6 to 180 months (mean, 51). Statistical analysis was performed using the SPSS statistical package. Five-year survival curves were estimated by the Kaplan– Meier method. The entry point was the date of surgery. The end point for overall survival was the date of death or the date of last consultation for patients who were alive at the end of the study (censored observations). For analysis of disease-specific survival data, patients who died of unrelated causes were considered as censored observations at the date of death. The end point for disease-free survival was the date of the first recurrence. Patients who died without any recurrence were considered as censored observations at the date of death. The end point for local control with laser alone was the date of local recurrence requiring open-neck surgery or non-surgical salvage treatment. Patients who died without salvage treatment other than laser surgery were considered as censored observations at the date of death. The end point of the organ preservation rate was the date of total laryngectomy. Patients who died without losing their larynx were considered as censored observations at the date of death. The prognostic value on disease-free survival, local control with laser alone, and organ preservation was tested by univariate analysis with the log-rank test for the following variables: pT and pN categories, tumor stage, positive surgical margins, previous treatment, complementary RT or CHT-RT, involvement of the glottis and/or arytenoids, and extension to the oro- and/or hypopharynx.

Results The postoperative staging of the present population is detailed in Table 2. The ESLs were classified as follows: 10 Type I (9 ventriculectomy and 1 arytenoid mucosectomy), 2 Type IIa, 5 Type IIb, 4 Type IIIa, 40 Type IIIb, 16 Type IVa, and 3 Type IVb. ND was performed in 27 (34%) patients, unilaterally in 10 and bilaterally in 17. ND was accomplished simultaneously with endoscopic procedure in 12 patients, while it was delayed by 1 month in 15.

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Table 2 Pathologic staging of the entire patient population (n = 80) pT

Patients

pN

Patients

Tis

2

N0

2

T1

20

N0

18

N1

1

N2b ecs? T2

38

T3

20

1

N0

30

N1

4

N2b

2

N2b ecs?

1

N2c ecs?

1

N0

12

N1 N2b

1 2

N2b ecs?

2

N2c

3

Ten patients received an endoscopic re-excision for positive margins after primary resection. In only seven out of ten patients, residual tumor (persistence) was found on histopathologic examination of the second surgical specimen. A total of 16 (20%) patients received complementary RT and 5 (6%) postoperative CHT-RT for persistent tumor after retreatmet for positive margins, multiple lymph nodes, and/or extracapsular spread. At the last follow-up, 1 (1%) patient died of laryngeal cancer (pT3N2b with extracapsular spread, refusing both

postoperative RT and salvage surgery), 14 (18%) died of unrelated causes (7 lung cancer, 1 brain cancer, 4 acute myocardial infarction, 1 lung embolism, and 1 gastric hemorrhage), and 2 (2%) were lost to follow-up. Persistent primary lesion was found in 1 (1%) patient at 5 months after surgery. Six (9%) patients developed recurrences, three at the level of the primary site and three at regional lymph nodes (from 8 to 47 months after treatment, mean 25). One (1%) developed a second laryngeal tumor after 68 months. Salvage therapy encompassed transoral retreatment in two cases, endoscopic retreatment followed by RT in two, total laryngectomy in one, ND in two, and ND followed by RT in two. One patient refused salvage therapy. In Table 3, the data for patients with persistence, recurrence, or second laryngeal tumor are detailed. The mean hospitalization time was 10 days (range, 2–59). Temporary tracheotomy was performed in 23 (29%) patients and removed after a median of 7 days (range, 1–300). Of these, 16 (70%) tracheotomies were performed during the first phase of our learning curve (1989–2002), while the rest were deemed necessary for inadequate supraglottic visualization, fear of postoperative edema after simultaneous bilateral neck dissection, or intraoperative diffuse bleeding. A total of 33 (41%) patients required a nasogastric feeding tube for a mean time of 7 days (range, 2–20). One (1%) patient died during the 3rd postoperative day for acute myocardial infarction. Major complications occurred in three (4%) patients and were represented by early postoperative bleeding of the superior laryngeal vascular pedicle

Table 3 Data of patients with persistence, recurrence, or second laryngeal tumor No.

Staging of the index tumor

Surgical treatment

Surgical margins

Complementary treatment

1

pT3N0

Type IIIb

R0



2

pT2N2b ecs?

Type IVa ? unilateral ND

R0



3

pT3N2c

Type IIIb ? bilateral ND

R0

4

pT2N0

Type IIIb

5

pT3N2c

6

Time elapsed after primary treatment (months)

Site of persistence, recurrence, or second tumor

Salvage therapy

Status

5

Larynx

Laser ? RT

NED, 33 months

8

Neck

ND ? RT

NED, 73 months

Refused RT

13

Neck



DOD, 20 months

R0



20

Larynx

Laser

NED, 72 months

Type IIIb ? bilateral ND

R0

RT on T-N

26

Larynx

TL

DOC for lung cancer, 57 months

pT3N0

Type IIIb ? bilateral ND

R1

RT on T-N

44

Neck

ND

NED, 45 months

7

pT3N2b ecs?

Type IVa ? unilateral ND

R1

CHT-RT

47

Larynx

Laser

NED, 47 months

8

pTisN0

Type I

R0



68

Larynx

Laser ? RT

NED, 124 months

TL total laryngectomy; NED no evidence of disease; DOD died of disease; DOC died of other causes

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Eur Arch Otorhinolaryngol (2010) 267:1735–1742 Table 4 Univariate analysis by the log-rank test

Variables

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Pts

Estimated 5-year disease-free survival

Estimated 5-year control with laser

Estimated 5-year organ preservation

Tis-T1

22

100%

100%

100%

T2

38

94.6%

100%

100%

T3

20

pT categories

59.6%

83%

88.2%

p = 0.009

p = 0.01

p = 0.03

pN Categories N0

62

93.3%

96.6%

98.3%

N1

6

100%

100%

100%

N2

12

58.3%

88.9%

88.9%

p = 0.007

p = NS

p = NS

50

97.9%

100%

100%

30

72.4%

88.9%

92.2%

p = 0.01

p = NS

p = NS

Tumor stage 0, I, II III, IV Margins Negative

70

92.3%

96.9%

98.3%

Positive

10

66.7%

90%

90%

p = NS

p = NS

p = NS

Negative margins

70

92.3%

96.9%

98.3%

Negative retreatment

3

100%

100%

100%

Positive retreatment

7

60%

85.7%

85.7%

p = NS

p = NS

p = NS

77.8%

88.9%

100%

Previous treatment Yes

9

No

71

89.7%

96.8%

96.8%

p = NS

p = NS

p = NS

Complementary RT or CHT-RT Yes

22

73.8%

85.4%

90%

No

58

94.6%

100%

100%

p = NS

p = NS

p = NS 100%

Involvement of the glottis and/or arytenoids Yes

14

92.9%

92.9%

No

66

87%

96.6%

96.6%

p = NS

p = NS

p = NS 93.3%

Involvement of the pharynx Yes

15

70%

93.3%

No

65

93.3%

96.6%

98.2%

p = NS

p = NS

p = NS

(managed by endoscopic revision of the surgical field) in two and persistent tracheocervical fistula after temporary tracheotomy (managed by pedicled fasciocutaneous deltopectoral flap) in one. The 5-year overall, disease-specific and disease-free survivals, local control with laser alone, and organ preservation rates were 84.4, 97.4, 88.3, 96, and 97.2%, respectively. Univariate analysis (detailed in Table 4) showed a statistically significant impact on disease-free survival, local control with laser alone, and organ

preservation of pT category (p = 0.009, p = 0.01, and p = 0.03, respectively), while pN category and tumor stage negatively influenced only disease-free survival (p = 0.007 and p = 0.01, respectively).

Discussion A wide spectrum of therapeutic choices for Tis-T3 supraglottic SCC has been reported. As a general rule, its

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management should be unimodal (by surgery or RT alone) for Tis, T1, and T2 lesions, reserving a multimodal strategy (combination of different therapeutic approaches such as open-neck surgery, RT, or CHT-RT) to the advanced T categories. In a retrospective study by Sua´rez et al. performed on 168 patients affected by supraglottic pT1-pT3 SCC treated by open-neck HSL with or without postoperative RT, the analysis of local relapse by T category showed similar results for T1 (2.4%), T2 (9.3%), and T3 (5.3%) lesions [6]. Another retrospective study by Herranz-Gonza´lez et al. [7] evaluating 110 patients affected by supraglottic pT1-pT4 SCC treated by open-neck HSL with ND and postoperative RT in selected pN? cases, reported a 3-year local control rate of 94.6%, without a significant impact of the pT category. Concerning the unimodal treatment of these lesions by RT, loco-regional control rates have been reported to range between 71 and 92% for T1 lesions and between 59 and 83% for T2 [1, 2]. Relatively few reports have been published concerning treatment of supraglottic SCC by transoral laser microsurgery compared to the overwhelming number of papers about endoscopic management of glottic tumors. The first author to describe the potential of transoral surgery by carbon dioxide laser in removing a supraglottic SCC was Vaughan in 1978 [8]. He reported the endoscopic successful treatment of two cases of epiglottic carcinoma, two of the aryepiglottic fold, and two of the false vocal fold. Davis et al. [9] in 1983 described 20 cases treated by transoral laser supraglottic partial laryngectomy (only 4 were performed with curative intent). In a subsequent paper, Davis [10] described a series of 14 patients treated by endoscopic supraglottic resection followed by complementary RT. In 1990, Zeitels et al. [11] described transoral epiglottectomy by CO2 laser based on a large institutional experience of 51 patients. Of these, only 27 subjects were affected by malignant supraglottic tumors and only 7 received radical resections (R0). The remaining procedures had been performed to obtain a biopsy of the lesion or to debulk it before another form of treatment. The first report with a significant cohort of subjects (99 patients) and long-term follow-up can be accredited to Steiner and Ambrosch in 1996 [16]. The reported local recurrence rates of 9.5% for stage I and II disease and 19.5% for stage III and IV were extremely encouraging. Two years later, Iro et al. described their experience with 141 patients submitted to transoral laser resection, associated with neck dissection (50%), postoperative RT (45% of cases), or CHT-RT (6%). The 5-year local control rate was 86.1% for stage I, 74.6% for stage II, 75.4% for stage III, and 78.4% for stage IV [17]. However, with a smaller series, similar oncologic results have been confirmed by other authors in the last 15 years [18–23].

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In the present series, we used the pTNM categories instead of the cTNM ones because we believe that this is the only reliable method to present results from a surgical cohort of patients. This can indeed hamper the possibility of comparison between surgical and non-surgical reports though, in our opinion, this remains an unsormountable problem. The 5-year disease-free survival (88.3%) and the 5-year organ preservation rate (97.2%) of this series compare favorably with those reported in the above-mentioned studies. Moreover, our univariate analysis suggests that the pT3 category, pN2 category, and disease stages III–IV are the only statistically significant variables influencing disease-free survival rates. This finding, in our opinion, strongly supports the indication of ESL in selected T3 supraglottic SCC with minimal pre-epiglottic space involvement, reserving open-neck approaches to tumors with pre-epiglottic space infiltration reaching the thyrohyoid membrane and/or anterior extralaryngeal spreading. Concerning the two surgical techniques herein applied (en bloc vs. piecemeal), at present we are not able to make fruitful comparisons in terms of oncologic outcomes due to small numbers. Piecemeal resection gives us a better visualization of surgical margins in case of bulky lesions, apparently without consequences on dissemination of neoplastic cells to the neck or distant sites. However, this could certainly represent a subject for future studies on larger series. Though positive margins (R1), in our experience, do not have a negative impact on any of the evaluated end points in univariate analysis, every effort should be made always to obtain clear margins during the first endoscopic procedure (by using intraoperative frozen sections) or with a second-look intervention (in case of positive surgical margins at histopathologic report of the entire specimen) to limit the application of multimodal therapeutic strategies. In case of tumor detection in the surgical specimen after endoscopic re-excision, the choice among an open partial laryngectomy (either HSL or SCPL-CHP), complementary RT, and CHT-RT must be balanced in face of different variables related to the tumor, metastatic lymph nodes, and patient’s characteristics. However, loco-regional control and organ preservation are not the only parameters that define the success of an oncologic treatment modality. The functional results in terms of perioperative morbidity and complications, hospitalization time, need and duration of drugs and medications, nasogastric or gastric feeding tubes and tracheotomy are other important elements that must be taken into account when planning a therapeutic approach. The present data, as well as other recent publications, clearly confirm a more limited morbidity of ESL compared to open-neck conservative procedures [12, 24]. Reducing postoperative respiratory and swallowing sequelae may also play an

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essential role in the elderly (especially over 70 years of age) and in those affected by severe chronic obstructive pulmonary disease. Avoiding or reducing the duration of tracheotomy dependence and speeding up swallowing rehabilitation are essential in the management of these fragile and debilitated patients. In this regard, ESL does not seem to have any of the limitations concerning the general health status of the patient (in terms of respiratory and cardiovascular function, and neurologic integrity) to be strictly evaluated for open-neck conservative laryngeal surgery and organ preservation protocols. Moreover, though this study was not designed to describe the costeffectiveness gain of ESL, it is evident that improvements in the above-mentioned aspects of perioperative patient management will be accompanied by a decrease in healthcare costs.

Conclusion An endoscopic approach to supraglottic SCC allows performing a custom-tailored tumor excision, working with the microscope in the operating field under conditions of ideal lighting and minimal bleeding. The tumor can be removed within safe narrow margins, thus sparing uninvolved adjacent mucosa, laryngeal framework, vessels, and nerves. Tumor resection can be also three dimensionally modulated and does not have the limitations of traditional surgery, such as subsequent reconstruction in terms of tension of the pexy and symmetry of the residual laryngeal structures. Other advantages of transoral laser microsurgery for supraglottic SCC include the possibility of accurately staging the lesion, and converting to an open-neck conservative approach whenever the tumor exceeds the expected limits of preoperative evaluation. When appropriately planned and performed, ESL allows local control and organ preservation rates comparable to those observed with other therapeutic modalities. No negative impact on regional control has been observed whenever a careful follow-up of neck status is performed. Moreover, in case of persistent or recurrent disease, all treatment options, including redo laser resection, conservative open-neck surgery, and organ preservation protocols still remain available. Conflict of interest statement interest.

The authors have no conflict of

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